Balance Function Assessment and Management, 3e (Jan 19, 2020)_(1635501881)_(‎Plural Pub Inc) 9781635501889, 1635501881, 9781635501995

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BALANCE FUNCTION ASSESSMENT AND MANAGEMENT Third Edition GARY P. JACOBSON NEIL T. SHEPARD KAMRAN BARIN | ROBERT F. BURKARD KRISTEN JANKY I DEVIN L MCCASLIN Caloric Test

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Balance Function Assessment and Management Third Edition

Editor-in-Chief for Audiology

Brad A. Stach, PhD

Balance Function Assessment and Management Third Edition

Gary P. Jacobson, PhD Neil T. Shepard, PhD Kamran Barin, PhD Robert F. Burkard, PhD Kristen Janky, AuD, PhD Devin L. McCaslin, PhD

5521 Ruffin Road San Diego, CA 92123 e-mail: [email protected] Website: https://www.pluralpublishing.com

Copyright © 2021 by Plural Publishing, Inc. Typeset in 10/12 Palatino by Flanagan’s Publishing Services, Inc. Printed in the United States of America by Integrated Books International All rights, including that of translation, reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, recording, or otherwise, including photocopying, recording, taping, Web distribution, or information storage and retrieval systems without the prior written consent of the publisher. For permission to use material from this text, contact us by Telephone:  (866) 758-7251 Fax:  (888) 758-7255 e-mail: [email protected] Every attempt has been made to contact the copyright holders for material originally printed in another source. If any have been inadvertently overlooked, the publishers will gladly make the necessary arrangements at the first opportunity. Disclaimer: Please note that ancillary content (such as documents, audio, and video, etc.) may not be included as published in the original print version of this book. Library of Congress Cataloging-in-Publication Data Names: Jacobson, Gary P., editor. | Shepard, Neil T., editor. | Barin, Kamran, editor. | Burkard, Robert F., 1953- editor. | Janky, Kristen, editor. | McCaslin, Devin L. (Devin Lochlan), editor. Title: Balance function assessment and management / [edited by] Gary P. Jacobson, Neil T. Shepard, Kamran Barin, Robert F. Burkard, Kristen Janky, Devin L. McCaslin. Description: Third edition. | San Diego, CA: Plural Publishing, [2021] | Includes bibliographical references and index. Identifiers: LCCN 2019035307 | ISBN 9781635501889 (hardcover) | ISBN 1635501881 (hardcover) | ISBN 9781635501995 (ebook) Subjects: MESH: Vestibular Diseases — diagnosis | Vestibular Diseases — therapy | Vestibular Function Tests — methods | Vertigo | Dizziness Classification: LCC RF260 | NLM WV 255 | DDC 617.8/82 — dc23 LC record available at https://lccn.loc.gov/2019035307

Contents Preface ix About the Editors xi Contributors xiii



1

An Historical Perspective of the Perception of Vertigo, Dizziness, and Vestibular Medicine Christopher K. Zalewski



2

Ontogeny of the Vestibular System and Balance Timothy A. Jones and Sherri M. Jones

15



3

Practical Anatomy and Physiology of the Ocular Motor System Scott D. Z. Eggers

43



4

Practical Anatomy and Physiology of the Vestibular System Jamie M. Bogle and Robert F. Burkard

69



5

Practical Biomechanics and Physiology of Balance Lewis M. Nashner

87



6

Clinical Neurophysiology of Vestibular Compensation Kamran Barin

105



7

The Vertigo Case History Jay A. Gantz, Belinda C. Sinks, and Joel A. Goebel

125



8

Assessing Dizziness-Related Quality of Life Erin G. Piker, Gary P. Jacobson, and Craig W. Newman

143



9

Bedside Assessment of the Vestibular System Carrie W. Hoppes, Karen H. Lambert, and Devin L. McCaslin

167

10 Eye Movement Recording and Ocular Motility Testing Neil T. Shepard, Michael C. Schubert, and Scott D. Z. Eggers

189

11 Positional Testing and Treatment Richard A. Clendaniel

225

12 Caloric Testing Kamran Barin

257

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13 Rotational Vestibular Assessment Christopher K. Zalewski

283

14 The Video Head Impulse Test (vHIT) Ian S. Curthoys, Hamish G. MacDougall, Leigh A. McGarvie, Konrad P. Weber, David Szmulewicz, Leonardo Manzari, Ann M. Burgess, and G. Michael Halmagyi

333

15 Computerized Dynamic Posturography:  Methodology and Interpretations Lewis M. Nashner and Neil T. Shepard

365

16 Vestibular-Evoked Myogenic Potentials (VEMPs) Devin L. McCaslin and Gary P. Jacobson

399

17 Electrocochleography (ECochG) Paul R. Kileny and Devin L. McCaslin

439

18 Pediatric Vestibular Testing Kristen Janky and Neil T. Shepard

457

19 Vestibular Balance Therapy for Children Jennifer B. Christy

479

20

Medical Management of Vertigo That Is Otologic in Origin Brian Neff and R. Mark Wiet

489

21

Surgical Management of Vertigo That Is Otologic in Origin R. Mark Wiet

501

22

Neurologic Origins of Dizziness and Vertigo Joseph M. Furman and Susan L. Whitney

519

23

Behavioral Factors in Dizziness and Vertigo Jeffrey P. Staab

529

24

Vestibular Rehabilitation Susan L. Whitney and Joseph M. Furman

549

25

The Aging Vestibular System: Implications for Rehabilitation Dara Meldrum and Courtney D. Hall

577

26

Topographical Localization of Vestibular System Impairment Gary P. Jacobson, Erin G. Piker, Richard A. Roberts, Devin L. McCaslin, and Nabih M. Ramadan

597

27

Challenging Cases Neil T. Shepard

617

Appendix I

Pathophysiology Signs and Symptoms of Dizziness Neil T. Shepard

629

Contents vii

Appendix II

Coding and Billing Robert F. Burkard, Neil T. Shepard, and Stuart Trembath

645

Appendix III Interprofessional Education and Practice Neil T. Shepard and Robert F. Burkard

653

Appendix IV Specialty Rotational Vestibular Assessments Christopher K. Zalewski

659

Index 689

Preface On behalf of the editors and authors, we would like to welcome you to the third edition of Balance Function Assessment and Management. Notable updates to this edition include the first chapter that reviews “An Historical Perspective of the Perception of Vertigo and Dizziness and Vestibular Medicine.” We have also included new chapters on the topics of “Vestibular Balance Therapy for Children” (Chapter 19) and “The Aging Vestibular System: Implications for Rehabilitation” (Chapter 25). Further, this edition includes a chapter on “Challenging Cases” (Chapter 27) and we end this textbook with four appendices covering “Pathophysiological Signs and Symptoms of Dizziness,” “Coding and Billing,” “Interprofessional Education and Practice,” and “Specialty Rotational Vestibular Assessments.” In response to the comments from read-

ers of the second edition, we have reduced the length of the textbook by making it more concise. Finally, the reader will note that this third edition has been edited by six nationally and internationally known clinical scientists in the area of dizziness, vertigo, and chronic unsteadiness. . These editors include Kamran Barin, PhD, Robert F. Burkard, PhD, Kristen Janky, AuD, PhD, and Devin L. McCaslin, PhD. We are grateful for the participation of these talented individuals in the planning, development, and realization of this third edition. It has been our objective from the first edition of Balance Function Assessment and Management to produce a textbook for both the student and the practitioner that treats comprehensively the assessment and management of dizziness. To the extent that we have achieved this goal, you, the reader, will be the judge. Gary P. Jacobson, PhD  Neil T. Shepard, PhD

ix

About the Editors Gary P. Jacobson, PhD, is Professor in the Department of Hearing and Speech Sciences and Director of the Divisions of Audiology and Vestibular Sciences at the Vanderbilt University Medical Center. Prior to that he served as the Director, Division of Audiology for the Henry Ford Health System. He completed his undergraduate studies at California State University at Fullerton. He received his MS in Communicative Disorders (Audiology) at the University of Wisconsin–Stevens Point and received his PhD from Kent State University. He is a past-editor of the American Journal of Audiology (ASHA) and is the current Editor-in-Chief of the Journal of the American Academy of Audiology (AAA). Dr. Jacobson has authored or co-authored 120 peer-reviewed publications and has co-edited four textbooks in the area of vestibular system function. Dr. Jacobson is a Fellow of ASHA and recipient of ASHA’s highest honor, the Honors of the Association. Dr. Jacobson received the Lifetime Achievement Award from the American Balance Society. Lastly, he received both the Distinguished Achievement Award and the Jerger Career Award for Research in Audiology from the American Academy of Audiology.

cal assessment and rehabilitation of balance disorder patients and clinical research endeavors related to both assessment and rehabilitation. Kamran Barin, PhD, is Assistant Professor Emeritus, Department of Otolaryngology–Head and Neck Surgery and Department of Speech and Hearing Science, The Ohio State University. He established and served as the Director of Balance Disorders Clinic at the Ohio State University Medical Center for over 25 years until his retirement in June 2011. Dr. Barin received his Master’s and Doctorate degrees in Electrical/Biomedical Engineering from The Ohio State University. He has published over 80 articles and book chapters and has taught national and international courses and seminars in different areas of vestibular assessment and rehabilitation. Dr. Barin has served on the Board of Directors of the Vestibular Disorders Association (VeDA) since 2017 and is currently a consultant to Interacoustics and Bertec Corporation. He previously served as a consultant to Otometrics. Robert F. Burkard, PhD, is a Professor in the Department of Rehabilitation Science, University at Buffalo. His research interests include calibration, auditory electrophysiology (in particular, auditory evoked potentials), vestibular/balance function/dysfunction, functional imaging, and aging. His professional interests include health care economics and interprofessional education/practice.

Neil T. Shepard, PhD, is former Chair of the Division of Audiology and Director of the Dizziness and Balance Disorders Program at the Mayo Clinic in Rochester, Minnesota. As Professor of Audiology, Mayo Clinical School of Medicine — Emeritus, Dr. Shepard continues with a clinical private practice in Missoula, Montana for the assessment and recommendations for treatment of patients reporting dizziness and balance disorder symptoms. He is also involved with research through the Mayo Clinic and clinical evaluations in the Neural Injury Center at the University of Montana. He received his undergraduate and masters training in Electrical and Biomedical Engineering from the University of Kentucky and Massachusetts Institute of Technology. He completed his PhD in auditory electrophysiology and clinical audiology from the University of Iowa in 1979. He has specialized in clinical electrophysiology for both the auditory and vestibular systems. His activity over the past 40 years has concentrated on the clini-

Kristen Janky, AuD, PhD, is the Clinical Coordinator of Vestibular Clinical Services and Director of the Vestibular and Balance Research Laboratory at Boys Town National Research Hospital. She received her PhD from the University of Nebraska and completed a post-doctoral fellowship at Johns Hopkins University. Her research focus is on the clinical assessment of dizziness and balance disorders in patients of all ages, with a particular emphasis on vestibular assessment and management in the pediatric population. She currently serves on the Editorial Board for the American Journal of Audiology and is President-Elect of the American Balance Society. xi

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Devin L. McCaslin, PhD, received a Master’s degree in Audiology from Wayne State University and a PhD in Hearing Science from The Ohio State University. He currently serves as the Director of the Vestibular and Balance Laboratory at the Mayo Clinic in Rochester and is an Associate Professor in the Mayo Clinic College of Medicine. He has authored and coauthored publications that cover the areas of tinnitus, dizziness,

auditory function, and outcome measures development. Dr. McCaslin’s major academic, clinical, and research interests relate to clinical electrophysiology, vestibular assessment, and the application of artificial intelligence to manage and treat dizzy patients. He also serves as the Deputy Editor-in-Chief of the Journal of the American Academy of Audiology and is the Past President of the American Balance Society.

Contributors Kamran Barin, PhD Assistant Professor Emeritus Department of Otolaryngology–Head and Neck Surgery Department of Speech and Hearing Science The Ohio State University Columbus, Ohio Chapter 6 and Chapter 12 Jamie M. Bogle, AuD, PhD Chair, Division of Audiology Mayo Clinic Arizona Assistant Professor of Audiology Mayo Clinic College of Medicine and Science Chapter 4 Ann M. Burgess, PhD Postdoctoral Research Fellow School of Psychology University of Sydney Sydney, Australia Chapter 14 Robert F. Burkard, PhD Professor Department of Rehabilitation Science University at Buffalo Buffalo, New York Chapter 4, Appendix II, and Appendix III Jennifer B. Christy, PT, PhD Associate Professor Program Director, Doctor of Physical Therapy Program Department of Physical Therapy University of Birmingham Birmingham, Alabama Chapter 19 Richard A. Clendaniel, PT, PhD Duke University School of Medicine Doctor of Physical Therapy Division Durham, North Carolina Chapter 11

Ian S. Curthoys, PhD Emeritus Professor of Vestibular Function School of Psychology University of Sydney Sydney, Australia Chapter 14 Scott D. Z. Eggers, MD Associate Professor of Neurology College of Medicine and Science Mayo Clinic Rochester, Minnesota Chapter 3 and Chapter 10 Joseph M. Furman, MD, PhD, FAAN Professor Department of Otolaryngology, Neurology, Physical Therapy, and Bioengineering University of Pittsburgh Pittsburgh, Pennsylvania Chapter 22 and Chapter 24 Jay A. Gantz, MD, PhD Otolaryngology Resident Department of Otolaryngology–Head and Neck Surgery Washington University School of Medicine St. Louis, Missouri Chapter 7 Joel A. Goebel, MD, FACS, FRCS Professor and Director Dizziness and Balance Centre Department of Otolaryngology–Head and Neck Surgery Washington University School of Medicine St. Louis, Missouri Chapter 7 Courtney D. Hall, PT, PhD Research Health Science Specialist James H. Quillen VA Medical Center, Professor East Tennessee State University Johnson City, Tennessee Chapter 25 xiii

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G. Michael Halmagyi, MD Neurology Department Royal Prince Alfred Hospital University of Sydney Sydney, Australia Chapter 14 Carrie W. Hoppes, PT, PhD, NCS, CCS Deputy Director Army–Baylor University Doctoral Program in Physical Therapy Chapter 9 Gary P. Jacobson, PhD Professor Director of the Division of Audiology Vanderbilt Bill Wilkerson Center Vanderbilt University Medical Center Nashville, Tennessee Chapter 8, Chapter 16, and Chapter 26 Kristen Janky, PhD Director Vestibular and Balance Research Laboratory Boys Town National Research Hospital Omaha, Nebraska Chapter 18 Sherri M. Jones, PhD Dean, College of Education and Human Sciences University of Nebraska–Lincoln Lincoln, Nebraska Chapter 2 Timothy A. Jones, PhD Professor Emeritus Department of Special Education and Communication Disorders College of Education and Human Sciences University of Nebraska–Lincoln Lincoln, Nebraska Chapter 2 Paul R. Kileny, PhD, FAAA, F-ASHA, BCS-IOM Professor Academic Program Director Audiology and Electrophysiology University of Michigan Health System Ann Arbor, Michigan Chapter 17

Karen H. Lambert PT, DPT, NCS Physical Therapist Bodies in Balance Physical Therapy Chapter 9 Hamish G. MacDougall, PhD GPRWMF Research Fellow Faculty of Science, School of Psychology University of Sydney Sydney, Australia Chapter 14 Leonardo Manzari, MD MSA ENT Academy Center Cassino (FR) Italy Chapter 14 Devin L. McCaslin, PhD Director Vestibular and Balance Laboratory Associate Professor Mayo Clinic College of Medicine Rochester, Minnesota Chapter 9, Chapter 16, Chapter 17, and Chapter 26 Leigh A. McGarvie Biomedical Engineer Royal Prince Albert Hospital Sydney, Australia Chapter 14 Dara Meldrum, BSc, MSc, PhD Research Fellow School of Medicine Trinity College Dublin Dublin, Ireland Chapter 25 Lewis M. Nashner, ScD Partner NPGMedical, LLC Consultant Bertec Corp. Intelligent Automation, Inc. Chapter 5 and Chapter 15 Brian Neff, MD Associate Professor of Otolaryngology Mayo Clinic College of Medicine and Science Mayo Clinic Rochester, Minnesota Chapter 20

Contributors xv

Craig W. Newman, PhD Section Head, Allied Hearing Speech and Balance Services (Retired) Head and Neck Institute Cleveland Clinic Cleveland, Ohio Chapter 8 Erin G. Piker, AuD, PhD Assistant Professor James Madison University Harrisonburg, Virginia Chapter 8 and Chapter 26 Nabih M. Ramadan, MD, MBA, FAAN, FAHS Director of Neuro-Hospitalist Program Carle Foundation Hospital Urbana, Illinois Chapter 26 Richard A. Roberts, PhD Vice Chair of Clinical Operations Assistant Professor Deptartment of Hearing and Speech Sciences Division of Vestibular Sciences Vanderbilt University Medical Center Nashville, Tennessee Chapter 26 Michael C. Schubert, PT, PhD Associate Professor Department of Otolaryngology–Head and Neck Surgery Department of Physical Medicine and Rehabilitation Johns Hopkins University School of Medicine Baltimore, Maryland Chapter 10 Neil T. Shepard, PhD Professor Emeritus Former Chair of Division of Audiology and Director of Dizziness and Balance Disorders Program Mayo Clinic Rochester, Minnesota Chapter 10, Chapter 15, Chapter 18, Chapter 27, Appendix I, Appendix II, and Appendix III Belinda C. Sinks, AuD, CCC-A Dizziness and Balance Center Department of Otolaryngology–Head and Neck Surgery Washington University School of Medicine St. Louis, Missouri Chapter 7

Jeffrey P. Staab, MD, MS Professor of Psychiatry Consultant, Department of Psychiatry and Psychology Department of Otorhinolaryngology–Head and Neck Surgery Mayo Clinic Rochester, Minnesota Chapter 23 David Szmulewicz, MB, BS (HONS), PhD, FRACP Neurologist and Neuro-Otologist Royal Victorian Eye and Ear Hospital Australia Department of Neurology Alfred Hospital Victoria, Australia Chapter 14 Stuart Trembath MA, CCC-A Audiologist Hearing Associates, P.C. Mason City, Iowa Appendix II Konrad P. Weber, MD Senior Physician Interdisciplinary Center for Vertigo and Neurological Visual Disorders Departments of Neurology and Ophthalmology University Hospital Zürich University of Zürich Zürich, Switzerland Chapter 14 Susan L. Whitney, DPT, PhD, NCS, ATC, FAPA Professor in Physical Therapy and Otolaryngology School of Health and Rehabilitation University of Pittsburgh Pittsburgh, Pennsylvania Chapter 22 and Chapter 24 R. Mark Wiet, MD, FACS Section Head of Otology, Neurotology, and Lateral Skull Base Surgery Director Acoustic Neuroma Program Director Auditory Implant Program Assistant Professor Departments of Otorhinolaryngology–Head and Neck Surgery, Neurosurgery, and Communication Disorders and Science Rush University Medical Center Chicago, Illinois Chapter 20 and Chapter 21

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Christopher K. Zalewski, PhD National Institutes of Health–NIDCD Otolaryngology Branch, Audiology Bethesda, Maryland Chapter 1, Chapter 13, and Appendix IV

1 An Historical Perspective of the Perception of Vertigo, Dizziness, and Vestibular Medicine Christopher K. Zalewski

Historical Beginnings and Commonplace Misdirection

vertigo would not occur for almost another two centuries. The historical recount of this elusive discovery is, in many ways, similar to other medical discoveries. It is one that is shrouded with misdirection and debate, as well as highlighted with triumph and tragedy. For some historical discoveries, storied misdirection is not uncommon during a time period when written accounts were sparse and interpretation of science was more philosophical than fact. One of the most poignant misdirections is that of Charles Darwin’s legacy. Although Charles Robert Darwin (c. 1809–1882) is universally recognized as the Father of Evolution and Natural Selection, largely due to his published work On the Origin of Species in 1859, public acknowledgment is seldom given to Alfred Russel Wallace (c. 1823–1913), who was instrumental in the independent conceptualization and propagation of the original framework for the theory of natural selection in his papers “On the Law which has Regulated the Introduction of New Species” (1855) and “On the Tendencies of Varieties to Depart Indefinitely From the Original Type” (1858), the latter paper being directly sent to Darwin by Wallace himself. Interestingly, the overshadowing of Alfred Russel Wallace by Charles Darwin was not the first time controversy surrounded the crediting of the Darwin namesake for introducing and revolutionizing a groundbreaking

Most medical histories can, at some point in time, always be brought back to Aristotle. Along with Hippocrates of Kos (c. 460–370 bc; Figure 1–1), Plato (c. 428/7 or 424/3–348/7 bc; Figure 1–2), and Socrates (c. 470–399 bc; Figure 1–3), Aristotle (c. 384–322 bc; Figure 1–4) was arguably one of the greatest philosophers and early scientists in history. He was not only the first to introduce the scientific study of all the human senses, he also provided the first written account of vertigo in 330 bc (Ross, 1927). Why is it that to those who are very drunk everything seems to revolve in a circle, and as soon as the wine takes a hold of them they cannot see objects at a distance? . . . [O]bjects near at hand are not seen in their proper places, but appear to revolve in a circle. (p. 892a)

And although the philosophical pondering of alcoholinduced dizziness does have its medical and vestibular merit, the actual attribution for the discovery of the physiologic link between the vestibular system and

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Balance Function Assessment and Management

Figure 1–1.  Hippocrates of Kos (460– 370 bc).

Figure 1–2.  Plato (428/7 or 424/3– 348/7 bc).

Figure 1–3. Socrates (470–399 bc).

William Charles Wells and Erasmus Darwin: The Dueling “Vestibular Philosophers”

Figure 1–4.  Aristotle (384–322 bc).

scientific theory. Charles’s grandfather, Erasmus Darwin, is often given credit for the earliest work on the origins of vertigo and nystagmus, rather than a young scientist by the name of William Charles Wells.

William Charles Wells was a scientist for whom the story surrounding the discovery of the vestibular sixth sense begins. Some 65 years before Charles Darwin published On the Origin of Species, Charles Darwin’s grandfather, Erasmus Darwin (c. 1731–1802; Figure 1–5), in collaboration with Robert Waring Darwin (c. 1766–1848), the father of Charles Darwin, published a section entitled “Of Vertigo” in Zoonomia; or, The Laws of Organic Life (Vol I) in 1794. This work nearly erased Charles Wells’s sentinel work on the discovery of the relationship between vertigo and nystagmus. As such, Zoonomia’s account of life, medicine, and early theories of evolution, including rudimentary ideas of vertigo and dizziness, is the reason that initial descriptions of vertigo are often attributed to Erasmus Darwin. It is Erasmus Darwin’s contributions to medicine, nature, and life that are highly acknowledged as one of the pinnacles of human physiology and thought. His four editions of the two volumes of Zoonomia have been recognized as among the most comprehensive and foundational works from which theories of modern medicine and philosophy have originated. As such, Darwin’s recognition for theories on dizziness and



1.  An Historical Perspective of the Perception of Vertigo, Dizziness, and Vestibular Medicine

Figure 1–6. Thomas Willis (1621–1675).

Figure 1–5.  Erasmus Darwin (1731–1802).

vertigo in Zoonomia all but dismissed the literary work published a mere two years earlier by Charles Wells, an essay that (correctly) refuted the current belief surrounding the sensation of vertigo at the time.

From Visual Vertigo to Visual After-Images: The Emergence of the Sixth Sense At the turn of the eighteenth century, Darwin’s published views on vertigo and dizziness continued to propagate the well-accepted notion at the time, that vertigo and dizziness were a disturbance of “visual processing.” The idea of “visual vertigo” was first offered by Thomas Willis (c. 1621–1675; Figure 1–6) in 1661 in his publication De Anima Brutorum quae Hominis Vitals ac Sentitiva Exercitationes Duae [The Beasts and the Man’s Life: 2 Exercises]. Here, Willis suggested that vertigo occurred solely from a disturbance of vision due to animal spirits in the central nervous system. Later in 1737, Julien Offray de la Mettrie (c. 1709–1751; Figure 1–7) supported this notion in his work Traité du Vertige [Treaty of Vertigo], but stated that vertigo was physiological rather than a consequence of animal or humorous spirits. This idea of “visual vertigo” was further supported and refined by William Porterfield (c. 1696–1771) in the same year (1737). However, Porterfield affirmed that visual vertigo was specifically not associated with eye movements (i.e., nystagmus), but

Figure 1–7.  Julien Offray de la Mettrie (1709–1751).

rather occurred due to aberrant visual neural processing of images. This concept of “phantom” neural visual processing was similar to phantom leg syndrome, a concept that was familiar to Porterfield, whose leg was amputated in his youth. The suspected origin of “visual vertigo” was held for another 65 to 70 years. It was not until 1792 that Charles Wells suggested that the sensation of vertigo was actually due to eye movement that could easily be elicited following head (body) rotation. In his

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Essays upon Single Vision with Two Eyes: Together with Experiments and Observations on Several Other Subjects in Optics, Wells published what is now known to be the first account detailing the association between vertigo and eye movement (i.e., nystagmus of vestibular origin). In this report, Wells was the first to describe both the fast and the slow phase of eye movement during nystagmus. Although Charles Wells did not specify what internal organs were responsible for the production of this “nystagmus,” with the use of after-images, Wells was the first to provide irrefutable evidence systematically linking the pattern of eye movements to the direction of perceived vertigo (Wade, 2003). Most notably, Charles Wells published this essay in 1792, which was two years prior to the publication of Erasmus Darwin’s first edition of Zoonomia; or, The Laws of Organic Life (Vol. I). However, in their publication, Erasmus and Robert Darwin detailed the characteristics of vertigo and continued to support Porterfield’s earlier, and erroneous, notion that “visual vertigo” was specifically not associated with eye movements. Unfortunately, Wells’s association with eye movement and post-rotational vertigo as a landmark discovery in vestibular science went largely unnoticed — so much so that Charles Wells himself would essentially drift into historical oblivion for this discovery.1

The Erasmus Wells Debate One hundred and thirty-one years after Thomas Willis first introduced the concept of “visual vertigo,” and a little more than two centuries since Aristotle first introduced the five senses, the notion that there could be a sixth sense, one of motion perception, was brought to scientific light. But who was rightfully due the scientific discovery? Although Charles Wells’s sophisticated experiments on post-rotational vertigo and nystagmus were seemingly irrefutable, they were also essentially unknown, and ostensibly almost deliberately unrecognized. This was likely due to the fact that Erasmus Darwin’s world-renowned publication of Zoonomia was essentially medical and philosophical law at the time. Additionally, since the majority of scientific writings were in the German language, Erasmus Darwin clearly had the advantage, as Zoonomia was translated into German, while Charles Wells’s Essays upon Single Vision with Two Eyes was only published in English (Wade, 2003). Moreover, his essay appeared in vision 1

literature, a far cry from that of neurology, or “vestibular” research (if such a medical classification had existed then). It was also unclear whether Wells’s work was poorly represented in the German translation of Zoonomia or Erasmus Darwin himself did not fully understand Wells’s work, or both. Or perhaps it was because the word “vertigo” was not even in the title of Wells’s essay. The topic of vertigo was, in fact, one of the “Several Other Subjects in Optics” that was addressed in the title of Wells’s 144-page essay, buried between pages 85 and 105. Several sources have suggested that Charles Wells also struggled against his own exasperation. Despite his kindness and warmth of heart he was easily offended (Wade & Tatler, 2005). As such, Wells was at times irascible, even describing himself as “naturally irritable” in his own memoir (Wade, 2003). Whether or not these traits projected Wells as an obstinate and indignant person, it is clear that such qualities would have undoubtedly affected his reputation within the scientific community. In this regard, one could easily detect such indignation in two rejoinders Wells published in The Gentleman’s Magazine in September and October of 1794, only three or four months after the first volume of Zoonomia was published. Wells’s quick dispute of Darwin’s comments on visual vertigo was, if nothing else, highly detailed and concise. In each letter, Wells provided a rather pointed rebuttal that articulated a clear and concise scientific counter argument to each of Darwin’s apparent logical statements supporting “visual vertigo.” Among Wells’s points was the notion that vertigo could occur in complete darkness, that is, in the absence of any visual processing (Wade, 2003). However, it was Wells’s use of optical after-images that provided the indisputable scientific evidence supporting a physiologic link between eye movements and vertigo, thus finally putting to rest the notion of “visual vertigo.” Though Wells did not provide a theory as to the origin of the production of these eye movements (i.e., “vestibular” nystagmus), his work did lay the scientific foundation for others to begin considering this question. The Gentleman’s Magazine Refutes Wells’s two responses to Darwin’s theory of visual vertigo in Zoonomia were highly publicized at the time, as The Gentleman’s Magazine was well regarded. However, the magazine was not widely read by scientists outside of Britain (Wade & Tatler, 2005). Regardless of

 he phrase “drift into historical oblivion” is a play on words, respectfully evoking the title of Nicholas Wade’s book Destined for Distinguished T Oblivion (see the Epilogue).



1.  An Historical Perspective of the Perception of Vertigo, Dizziness, and Vestibular Medicine

the magazine’s limited readership, Wells’s rejoinders in The Gentleman’s Magazine had gained both scientific attention and popularity. As such, Erasmus Darwin briefly acknowledged Wells’s alternative theories on vertigo and nystagmus in his third edition of Zoonomia, which was published in 1801 (i.e., almost 10 years following the initial publication of Wells’s Essays upon Single Vision with Two Eyes. Unfortunately, Darwin’s position on visual vertigo changed little in the third edition. It was not until Darwin’s final fourth edition of Zoonomia that Erasmus and Robert Darwin would finally acknowledge, although begrudgingly, Charles Wells’s scientific contributions linking eye movements (nystagmus) to the perception of vertigo (Wade, 2003). Amazingly, however, they continued to support the theory of visual vertigo, thus continuing to dismiss Wells’s conclusions. Most notably, it was Wells’s second letter to The Gentleman’s Magazine, detailing the post-rotation nystagmus response that possibly offered the best evidence to suggest his work was the first foundational work on vestibular research.2 Specifically, it was Wells’s succinct description of the involuntary post-rotational nystagmus in his second retort, which detailed the apparent motion of the environment after cessation of rotation (Wade, 2003). The apparent rotation of the environment was dependent not only on the direction of subject rotation, but also on the direction of involuntary eye movement. Furthermore, the direction of the rotation of the environment switched directions in accordance with the change in the direction of head rotation (Wade, 2003). Finally, Wells also detailed the suppression of nystagmus with concentrated vision (i.e., vestibulo-ocular reflex [VOR] suppression), as well as the perception of vertigo and documentation of after-image eye movement in darkness. Collectively, Wells’s observations on vertigo and nystagmus are the first and foremost definitions of what we now know today to be the properties of clinical vestibular nystagmus. However, despite Wells’s scientific evidence supporting the association between vertigo and eye movements, the use of rotation for the diagnosis of vertigo and investigation of vestibular function would continue to remain absent in neurology clinics for over a century. In fact, it would take another 100 years until Róbert Bárány (c. 1876–1936) applied these “rotational” properties clinically. It is interesting that the published feud between Wells and Darwin in The Gentleman’s Magazine may 2 

have been the primary reason for the eventual crediting of Charles Wells’s work on vertigo and nystagmus. The detailed responses by Wells allowed for the public expansion of his theories and the devolution of “visual vertigo.”

Bridging the Gap: The Physiologic Link Between the Vestibular System and Vertigo The notion of linking head rotation to nystagmus (and vertigo) was a novel finding at the time, and suggesting that the semicircular canals were the origin for this nystagmus might have been the most logical step in the scientific process. However at the turn of the eighteenth century, an erroneous notion still persisted. There was a continued belief by many that the “Cretan Labyrinthos,” as Aelius Galen (c. 129–200/216 ad; Figure 1–8) had elegantly named the vestibular labyrinth, was responsible for auditory localization. After all, the anatomy of the labyrinth easily supported the contention that the semicircular canals were aligned for optimal sound localization (and amplification as Du Verney had suggested in 1683; Figure 1–9). Unfortunately, at the time of Wells and Darwin, the scientific bridge between the vestibular labyrinth, head rotation, nystagmus, and vertigo had yet to be made, and

Figure 1–8.  Aelius Galen (129–200/216).

 espite Wells’s work in vestibular research, it is often Jan Evangelista Purkyneˇ (c. 1787–1869) and Jean Pierre Flourens (c. 1794–1867) who D are frequently credited with and subsequently often referred to as the “Fathers of Vestibular Science”— but more to come on this later.

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Figure 1–9.  Joseph Guichard Du Verney (1648–1730).

because of this, it was unclear whether even Wells’s work actually had any direct impact on the work of two well-known vestibular scientists (Purkyneˇ and Flourens), who made these final connections.

Figure 1–10.  Jan Evangelista Purkyne ˇ (1787–1869).

Purkyne ˇ and Flourens Jan Evangelista Purkyneˇ (Figure 1–10) and Jean Pierre Flourens (Figure 1–11) were two world-renowned physician scientists, both performing work in vertigo and motion perception. Purkyneˇ in particular was highly regarded and extremely well known, as one merely had to address a letter to “Purkyneˇ, Europe” and it would be delivered successfully (Baloh, 2002). Along with other scientists at the time, such as Ernst Josef Mach (c. 1838–1916), Josef Breuer (c. 1842–1925), and Alexander Crum-Brown (c. 1838–1922), the discovery of the link between the vestibular system, vertigo, and eye movements advanced quickly. Unfortunately for Wells, neither Purkyneˇ nor Flourens spoke fluent English (Wade, 2003). As such, neither one ever referenced Wells’s work on vertigo and nystagmus. Most of the vestibular research at the turn of the century came from either Germany or France, with German often being the language of choice. Darwin’s Zoonomia was widely cited and available in German, which was familiar to both Purkyneˇ and Flourens (evidenced by the fact that

Figure 1–11.  Jean Pierre Flourens (1794–1867).

they both often cited Zoonomia) (Wade & Tatler, 2005). Both scientists continued to disregard Wells’s evidence on post-rotational vertigo and nystagmus, and



1.  An Historical Perspective of the Perception of Vertigo, Dizziness, and Vestibular Medicine

continued to promote their own beliefs.3 For example, Purkyneˇ continued to promote the idea that vertigo occurred in response to the independent rotation of the cerebellum. Moreover, it was likely Erasmus Darwin’s work on rotation (not Wells’s work) that may have swayed Purkyneˇ to abandon this idea and move toward accepting a link between the vestibular system and vertigo. In fact, on more than one occasion Purkyneˇ assigned sole credit to Darwin for his investigation of vertigo and the physiologic background of this phenomenon (Wade, 2003). This notion further supported Purkyneˇ’s apparent unfamiliarity with Wells’s work on vertigo and nystagmus. This was reinforced by the fact that Purkyneˇ himself is often credited with being the first to make the association between eye movements and rotation (Wade, 2003). In fact, most of the work related to vertigo and its physiologic and subjective bases often begins with citing Purkyneˇ and Flourens’s work, which is clearly evident in Coleman Griffith’s highly regarded, well-known, and often-cited historical perspective An Historical Survey of Vestibular Equilibration, published in 1922. Griffith begins his historical survey with Purkyneˇ and Flourens’ work on vestibular physiology, which may explain why most literature often cites Purkyneˇ and Flourens as the “Fathers of Vestibular Science.”

. . . And Then There Were Six The characterization of the original Aristotelian five senses went unchallenged for nearly two thousand years. It was Charles Wells’s 1792 treatise that provided the first indisputable evidence that supported the link between the patterns of eye movements in relation to the direction of post-rotary vertigo. However, two decades would linger on this evidential theory, until scientific discovery would take another giant leap forward. Scientific evidence would soon be provided by Purkyneˇ and Flourens in the early nineteenth century that would significantly propel forward Wells’s evidence. Interestingly, Purkyneˇ and Flourens would provide this evidence independently from one another, as both were actually unknown to one another during this time (Bárány 1916, Laureate Lecture). At the turn of the nineteenth century, both physicianscientists independently published their reports on 3

vertigo and rotation, as well as semicircular canal function. Purkyneˇ’s early publication in 1820, Beiträge zur näheren Kenntniß des Schwindels aus heautognostischen Daten, continued to expand on the symptomatic link between the vertiginous behavior of objects in the visual field and rotation (Griffith, 1922). However, it was Flourens’ landmark work published in 1824, Recherches expérimentales sur les propriétés et les fonctions du système nerveux dans les animaux vertébrés, that linked definitively discrete physiologic disturbances in the visual system when the semicircular canals of pigeons were stimulated. Flourens would publish three more landmark articles from 1824 through 1842 on the physiologic link between the visual system and the semicircular canals: (1) Experiences sur les canaux semicirculaires de l’oreille dans les oiseaux (1830), (2) Experiences sur les canaux semicirculaires de l’oreille dans les mammifères (1830), and (3) Recherches expérimentales sur les propriétés et les fonctions du système nerveux dans les animaux vertébrés (1842) (this 1842 report having the same title as his initial publication in 1824) (Griffith, 1922). It was Purkyneˇ ’s and Flourens’ experiments and writings from 1820 through 1842 that provided the scientific evidence that confirmed the physiologic link between the vestibular system and vertigo. In particular, Flourens’ work in 1824 all but singlehandedly transformed the long-held belief, that the vestibular system was responsible for sound localization, into the more scientifically accepted belief that the vestibular system was actually responsible for motion perception (and vertigo, when aberrantly stimulated). It was Flourens’ research involving the extirpation of semicircular canals in pigeons which provided the irrefutable evidence for the vestibular system’s role in the perception of motion, thus heralding the elusive sixth sense. In the words of Róbert Bárány during his Nobel Prize acceptance speech (Bárány, 1916, Laureate Lecture): Flourens thought that it would be possible to get an insight into the function of the semi-circular canal apparatus by destroying it. In fact, these experiments which were undertaken with pigeons, rabbits and other animals produced quite remarkable, constant and previously unknown disturbances. For instance, if the horizontal semi-circular canal was destroyed in a pigeon, it went on turning horizontally in a circle.

While neither Purkyneˇ nor Flourens ever referenced Wells’s work on vertigo and nystagmus, it remains curious that both scientists continued to neglect Wells’s contributions to vertigo and nystagmus, even after he was briefly acknowledged by Erasmus Darwin in the third edition of Zoonomia in 1801 (Wade & Tatler, 2005), which was 23 years prior to their landmark manuscript identifying the physiologic link between vertigo, nystagmus, and the vestibular system.

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If a vertical semi-circular canal was destroyed, the pigeon turned somersaults. Flourens has described the phenomena extremely well. But he did not give an explanation. In particular, he did not have the faintest idea that the animals were suffering from vertigo. You can see from this how easily one can pass by within an inch of the truth.

The concept of a sixth sense struggled for nearly two thousand years after Aristotle first described the five principle human senses. Therefore, it was not surprising that the concept was not accepted universally by scientists at the time. This skepticism included Jan Evangelista Purkyneˇ, who continued to remain somewhat hesitant in acknowledging all the available scientific evidence at the time (Wade, 2003), largely because his work continued to focus on the symptomatology of the vertiginous response, rather than the neural physiology.

Rotation in the Early Nineteenth Century and Discoveries of Vestibular Physiology . . . and Never the Two Disciplines Shall Meet A majority of the work investigating vertigo and rotation in the first quarter of the nineteenth century was, interestingly, not focused on that of scientific exploration of dizziness but rather the clinical treatment for the mentally insane. Despite the growing interest in the use of rotation and the written accounts supporting the “new” theory physiologically linking eye movements and vertigo, the use of rotation in the early nineteenth century was most commonly found in psychiatric asylums. Secondary to Erasmus Darwin’s publication of Zoonomia, the application of rotation quickly became a prominent therapeutic technique during the early nineteenth century for psychiatric disorders. In 1801, Erasmus Darwin introduced his “rotating couch” (Wade, 2003) as a means of inducing intentionally provoked vertigo and subsequent slumber in psychiatric patients. The idea of “medicinal slumber” was well accepted at the time and motivated many in the field of mental health care to prescribe such medically induced slumber for the treatment of psychiatric disorders in the early 1800s (Cohen & Raphan, 2004). Well-known psychiatrists Joseph Mason Cox, of Fishponds Private Lunatic Asylum, and William Saunders Hallaran (c. 1765–1825), a physician superintendent at the County

and City of Cork Lunatic Asylum, even developed their own “circulating swings,” for which they are probably best remembered. The success of “Hallaran’s Circulating Swing” in 1818 (Breathnach, 2010) was adopted by many at the time and, in particular, by Anton Ludwig Ernst Horn (c. 1774–1848), of the Charité-Hospital in Berlin, Germany. Horn eventually developed his own, ceiling-suspended, 13-foot rotating bed, which was capable of spinning 120 revolutions per minute (Belofsky, 2013) and producing up to four or five times the force of gravity (Harsch, 2006). Horn’s “psychiatric centrifuge” was also well accepted and widely used between 1814 and 1818 for the treatment of mental disorders. He reported success for the use of his “psychiatric centrifuge” in patients with hysteria (Harsch, 2006). Medicinal slumber continued through the late nineteenth century, including use of a human centrifuge in 1898 by Dr. F. R. von Wenusch to investigate the therapeutic potential of acceleration (White, 1964). However, the transition of using rotation for the treatment of psychiatric disease to the diagnosis of vertigo and dizziness would not occur until the vestibular system’s role was firmly redefined, both physiologically and clinically, from that of audition to one of motion perception.

From Rotation of the Mentally Ill to Vestibular Physiology Discoveries Despite the absence in the use of rotation for the clinical diagnosis and treatment of vertigo and dizziness throughout the 1800s, there were significant research advancements being made in the scientific understanding of vestibular physiology in the later quarter of the nineteenth century. Most notably, Ernst Josef Mach (Figure 1–12), Alexander Crum-Brown (Figure 1–13), and Josef Breuer (Figure 1–14) proposed the “hydrodynamic theory of semicircular canal function” between 1874 and 1875. Ernst Josef Mach published Grundlinien der Lehre von den Bewegungsempfindungen in 1875, Crum-Brown published On the Sense of Rotation and the Anatomy and Physiology of the Semicircular Canals of the Internal Ear in 1874, and most noteworthy, Josef Breuer published “Über die Funktion der Bogengänge des Ohrlabyrinthes” in 1874 and “Beiträge zur Lehre vom statischen Sinne” in 1875. Although all were instrumental in the development of the hydrodynamic theory, Josef Breuer’s role was particularly significant in its development (Baloh, 2017). In fact, Josef Breuer would be one of the most prolific vestibular physiologists in the latter quarter of the nineteenth century, publishing



1.  An Historical Perspective of the Perception of Vertigo, Dizziness, and Vestibular Medicine

Figure 1–12.  Ernst Josef Mach (1838–1916).

more than 200 articles on the topic of vestibular physiology in his lifetime (Baloh, 2017). The introduction of the hydrodynamic theory of semicircular canal function was staggering at the time. It was a great leap forward in the understanding of vestibular physiology, and the theory still remains prominent to this day. It is interesting that Mach, Breuer, and Crum-Brown independently arrived at similar conclusions but from different perspectives. The independent research from each scientist was truly brilliant, and eloquently recounted by Róbert Bárány during his 1914 Nobel Prize acceptance speech. It is also worth noting that, during the time of these discoveries, Alexander Crum-Brown also devised methods for measuring thresholds for detecting body movements on a rotating stool. He determined that the thresholds were lowest when the head was positioned so that one of the semicircular canals was in the plane of rotation, a precursor to Ewald’s laws of semicircular canal function. During this time period, Ernst Josef Mach also published scientific reports investigating the nature of otolith responses as well as the first reports indicating that the semicircular canals responded to acceleration, not velocity (Cohen & Raphan, 2004). Between 1874 and 1875, Ernst Mach constructed a rotational chair that was mounted in a rotatable frame and examined the perception of the visual vertical during static tilt as well as the visual aftereffects of body rotation. Mach performed such studies after observing the vertical

Figure 1–13.  Alexander Crum Brown (1838–1922).

Figure 1–14.  Josef Breuer (1842–1925).

tilting of telegraph poles when rounding an inappropriately banked curve on a train (Cohen & Raphan, 2004). For his work on subjective visual vertical, some consider Ernst Mach the “Father of Otolith Function Testing.” Despite this otological notoriety, Ernst Josef Mach, being an Austrian physicist and philosopher, is probably better known for Mach’s principle, which was a precursor to Einstein’s Theory of General Relativity.

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Róbert Bárány and the Early Twentieth Century Toward the later part of the nineteenth century and the early part of the twentieth century, the use of Horn’s “psychiatric centrifuge” for medicinal treatment finally gave way to more scientific evidence supporting the use of rotation as a clinical method for investigating vestibular function and dizziness. Nearly a century after the well-accepted and routine use of patient rotation for the treatment of psychiatric disorders, Róbert Bárány (Figure 1–15) introduced the application of patient rotation in 1907 as a means for the clinical assessment of the vestibular system. Bárány developed the first vestibular rotational chair that was universally adopted in otolaryngology clinics at the time. For this reason, modern-day rotational chairs are sometimes referred to as “Bárány chairs.” Despite the introduction of the Bárány chair into many neurology clinics, the use of rotation in the clinical diagnosis and treatment of vestibular and balance disorders was slow. In fact, in the beginning of the twentieth century, there was almost no advancement of rotational research. This was likely due to one of the most significant discoveries in clinical vestibular physiology. In 1906, Róbert Bárány published his most renowned paper, “Untersuchungen ueber den vom Vestibularapparat des Ohres reflektorisch ausgelösten rhythmischen Nystagmus und seine Begleiterscheinungen” [Investigations of Rhythmic Nystagmus and

Figure 1–15. Róbert Bárány (1876–1936).

Its Accompanying Manifestations Arising from the Vestibular Apparatus of the Ear] (Nylen, 1965). In this manuscript, Bárány would describe the alternating nystagmus response that occurred following administration of sterile water to the external ear canal. Earlier Bárány and others (e.g., Gustav Alexander, Heinrich Neumann von Héthárs) had observed such a nystagmus response consequent to ether being used as a sterile wash over the labyrinths during otologic surgery. Although this response was regularly observed during labyrinthine surgical procedures, Bárány made the crucial “bench-to-bedside” link that forever changed the clinical assessment of vestibular function. In short, Bárány had taken a “simple” surgical observation and conceived the caloric test, a simple bedside measure that could be used to evaluate each vestibular system independently. For this landmark work, Bárány would be awarded the Nobel Prize in Physiology and Medicine in 1914. In fact, no other Nobel Prize has been awarded in the field of vestibular medicine (noting that George von Békésy received the Nobel Prize in Physiology and Medicine in 1961 for his work in the field of hearing science on the cochlear traveling wave). Unfortunately, the life of Róbert Bárány and his receiving the Nobel Prize were not necessarily a cause for celebration.

Nobel Laureate Róbert Bárány in a Time of Controversy Upon the announcement of Bárány’s Nobel Prize, Róbert Bárány was a few thousand miles away being held as a prisoner of war in a Russian camp. Bárány’s notoriety as a world-renowned otologist followed him as a prisoner of war, such that he found himself not only treating otologic and neurotologic disease among his fellow POWs, but also treating the Russian commanders and their immediate family members. News of Bárány winning the Nobel Prize would eventually make its way across the Russian Steppe to where Bárány had been serving his time as a POW. Bárány’s controversial release from the Russian POW camp was negotiated by Prince Carl of Sweden, after which Bárány traveled to Sweden and received his Nobel Prize in 1916. Upon Bárány’s arrival in Stockholm, Sweden, he was lauded as any other Nobel Laureate. There, he delivered his Laureate lecture “Some New Methods for Functional Testing of the Vestibular Apparatus and the Cerebellum” to much pomp and circumstance. However, Bárány’s praise would be short-lived. After receiving his Nobel, Bárány returned to Vienna and was greeted with disdain and controversy by those



1.  An Historical Perspective of the Perception of Vertigo, Dizziness, and Vestibular Medicine

with whom he had practiced and refined his neurotology and surgical skills. These individuals included Heinrich Neumann von Héthárs, Alexander Spitzer, and Ádám Politzer (who many consider to be one of the fathers of modern otology4). Bárány even received a significant amount of criticism from his close friend Gustav Alexander, as well as from Ernst Mach, Josef Breuer, and Julius Eduard Hetzig (Baloh, 2017). There seemed to remain a persistent and pestering question that lingered in Vienna regarding the “misdirected” awarding of the Nobel to Bárány. Specifically questions remained as to whether or not Bárány commenced his Nobel Laureate work on the bedside caloric stimulation of the labyrinth after he had witnessed Alexander Spitzer, Julius Hetzig, and Josef Breuer’s demonstration of labyrinthine nystagmus in experimental animals, and after he had previously observed the labyrinthine nystagmus response while ether was washed over the labyrinth during neurotologic surgery with Heinrich Neumann. Subsequently, formal “charges” were brought to the Vienna Medical Faculty Academic Senate claiming that (1) Bárány did not discover the caloric reaction, but rather this credit should go to Alexander Spitzer, Julius Hetzig, and Josef Breuer, (2) Bárány omitted the fact that he obtained the idea for the change in nystagmus direction with cold and warm water from Heinrich Neumann, and (3) Bárány did not give proper credit to earlier investigators in his writings, specifically failing to cite Alexander’s previous work outlining otologic surgery at the time (some of which were even coauthored with Bárány; Baloh 2017). To these charges, the Academic Senate responded by stating: Dr. Bárány did not act scientifically correct, which was his duty as a faculty member, scientist and writer. His behavior demonstrates eminent carelessness in terms of the intellectual property of others. . . . His failure cannot be attributed to a lack of skill or training; in contrast, it is evident that Dr. Bárány represents a person of outstanding capabilities, diligence, and training. The errors, failures, and one-sided descriptions in his articles and lectures can only be explained by his addiction to enlarge his own merit at the expense of others. (Baloh, 2002)

Expectedly, Bárány was bitterly disappointed by his reception in Vienna and took the opportunity to accept a position to develop a new otolaryngology

4 

clinic in Uppsala, Sweden. During this period, the same accusations were brought against Bárány to the Medical Faculty of the Karolinska Institute in Stockholm, Sweden, the institute responsible for awarding the Nobel Prize. The Karolinska Institute concluded that Dr. Bárány did act scientifically correct. Hitzig and Breuer’s work was purely experimental and . . . Bárány should be given priority for discovery of the caloric reaction. Regarding Neumann’s suggestion to Bárány during an operation to test the effect of cold and warm water on the caloric reaction, the Faculty concluded that Bárány had already reported on his findings regarding the change in direction of the caloric reaction several months earlier in an article at an Academy meeting. (Baloh, 2002)

Letters in support of Bárány were sent to the Karolinska Institute, most notably by Bárány’s longtime good friend, Rafeal Lorente de Nó (who would later be recognized for detailing the VOR pathway in his 1933 landmark paper “Vestibulo-Ocular Reflex Arc”). Although he was pleased with the outcome, Bárány’s life was never the same. In spite of being a Nobel Laureate, Bárány lived a very quiet, almost lonely, existence (Baloh, 2017). He enjoyed music and playing the piano. Bárány’s life in his last few years would be marred by a series of strokes from malignant hypertension, leaving him with partial paralysis (Baloh, 2017). Bárány died on April 8, 1936, two weeks before an international meeting to celebrate his sixtieth birthday. He would later be commemorated numerous times over, culminating in the establishment of the International Bárány Society (founded in 1960 by Charles Skinner Hallpike and Carl O. Nylen), through which the Bárány Medal is awarded to an individual whose distinguished contributions to neurotology and vestibular medicine are preeminent in the field.

Moving Forward in the Wake of History With the exception of the more nascent vestibular sensory-evoked potentials (VSEPs) and vestibular evoked myogenic potentials (VEMPs), vestibular tests of today have largely rested on the principle foundations of the vestibular ocular reflex arc, head rotation,

Not to slight Guichard Joseph Du Verney, who was perhaps the very first otologist (Traynor, 2015).

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and caloric stimulation. These are, in fact, the very same principles that had their humble beginnings in the late 1700s. Although some may debate how much has really changed, there is no doubt that significant advancements have been made in vestibular assessment. The current state of vestibular science is poised to enter a new renaissance of clinical discovery. There is evidence for future testing protocols that could favorably expand and even redefine vestibular outcome measures, from vestibular threshold perception protocols to neurological vestibular evoked potentials, to unprecedented complex stimuli delivery systems. Together with a vast array of physiological and genetic understanding, new research using highly advanced devices, methods, and stimuli will undoubtedly expand our understanding of vestibular function and dysfunction. Throughout the entire historical perspective of vestibular medicine, since the days of Charles Wells, Jean Pierre Flourens, Ernst Mach, Josef Breuer, and Robert Bárány, one thing has remained a fundamental truth: A thorough understanding of vestibular anatomy and physiology is essential to the understanding and advancement of vestibular science. We must remember that it was not complex and ultra-sophisticated devices that gave us Ewald’s laws and the “hydrodynamic theory of semicircular canal function,” but rather it was the result of an excellent marriage of thought between the understanding of stimuli and physiologic outcomes. No one knows for certain what the future of vestibular research may bring; however, one thing has always remained certain since the time of the great Greek poet Homer (c. 750 bc): “I know not what the future holds, but I know who holds the future.”

Epilogue The summation of historical events is, if nothing else, very labor intensive. Piecing together historical facts and moments in time can be tricky. Thankfully, there are bodies of work from individuals that have significantly contributed to ease this challenge. Although many sources have contributed to the events portrayed in this chapter, there are some bodies of work that have proven extremely helpful, which I would like to highlight and acknowledge here. This chapter could not have been possible without the literary works from Nicholas Wade and Benjamin Tatler, specifically for their publications of “Destined for Distinguished Oblivion: The Scientific Writings of William Charles Wells” (Wade, 2003) and “The Moving Tablet of the Eye: The Origins of Modern Eye Movement Research” (Wade & Tatler, 2005). I especially wanted to highlight these two works, for much of the synopsis of Charles Wells and Erasmus Darwin relied on these authors’ tireless research of the historical events that surrounded Wells’s and Darwin’s scientific lives. In addition to these two sources, the historical events of Róbert Bárány were exceptionally summarized by Dr. Robert Baloh in two articles as well as a text published in 2017, Vertigo: Five Physician Scientists and the Quest for a Cure. Credit and praise for these sources are immeasurably acknowledged here, and all of these sources would certainly have my strong recommendation for anyone looking for an excellent read. Figure 1–16 provides a historical timeline of sentinel vestibular events.



1.  An Historical Perspective of the Perception of Vertigo, Dizziness, and Vestibular Medicine

Thomas Willis (1621-1675 )

Aristotle (384 - 322)

Erasmus Darwin J.E. Purkyně (1731 – 1802) (1787 – 1869)

William Porterfield (1696 - 1771 )

Joseph Guichard Julien Offray s Du Verney de la Mettrie Antonio Scarpa Charles Wells (1648 – 1730) (1709-1751) (1752 - 1832) (1757 - 1817))

Aelius Galen (129 – 200/216)

J.P. Flourens (1784 - 1867)

E. Mach (1838 – 1916)

Róbert Bárány (1836 -1936)

J. Breuer A. Brown (1842 - 1925) (1838 – 1922)

1794

1796

1820-1824 J. Flourens and J. Purkyně independently provided evidence supporting a scientific physiologic link between the vestibular system, nystagmus, and motion detection, thus the vestibular sixth-sense is scientifically confirmed.

1789

E. Darwin publishes first edition of “Zoonomia; or, The Laws of Organic Life (vol I)” supporting visual vertigo

1737

C Wells publishes “Essays upon Single Vision with Two Eyes: Together with Experiments and Observations on Several Other Subjects in Optics” - first associativeevidence linking nystagmus and head rotation.

1683

A. Scarpa publishes Anatomicæ disquisitiones de auditu et olfactu, which contains renowned lithograph plate engraving of the inner ear showing extraordinary detailed anatomy of the inner ear & vestibular labyrinth.

1661

J. de la Mettrie publishes “Traité du vertige,” which modified Thomas Willis’s hypothesis that the origin of vertigo was actually one of physiologic visual errors. W. Porterfield supports & refines physiologic origin to be one of ‘visual vertigo’ (abnormal visual CNS processing).

129-200/216

J.G. Du Verney publishes “Traite de L’Organe de L’Ouie” suggesting the semicircular canals act as ‘trumpets’ to amplify sound from different directions.

0 B.C.

460-322

1874-1875

1906 R. Bárány publishes ‘Untersuchungen ueber den vom Vestibularapparat des Ohres reflektorisch ausgelösten rhythmischen Nystagmus und seine Begleiterscheinungen’ (discovery of the caloric test).

E. Mach, J. Breuer, & A. Crum-Brown independently publish on the “hydrodynamic theory of semicircular canal function.”

T. Willis publishes “De Anima Brutorum quae hominis vitals ac sentitiva exercitationes duae (The Beasts and the Man’s Life: 2 Exercises).” Claims vertigo is a result of animal spirits in the CNS.

A. Galen identifies the ‘Cretan Labyrinthos’named after the labyrinths of Crete, Greece.

Aristotle provides first written account of vertiginous-type symptoms. Publishes the Aristotelian five senses.

0 A.D.

Figure 1–16.  Historical timeline of sentinel vestibular events from the time of Aristotle through Róbert Bárány.

References Baloh, R. W. (2002). Robert Bárány and the controversy surrounding his discovery of the caloric reaction. Neurology, 58, 1094–1099. Baloh, R. W. (2017). Vertigo: Five physician scientists and the quest for a cure. New York, NY: Oxford University Press. Bárány, R. (1906). Untersuchungen über den vom vestibularapparat des ohres reflektorisch ausgelösten rhythmischen nystagmus und seine begleitererscheinungen. Monatschr Ohrenheilk, 40, 193–297. Bárány, R. (1907). Physiologie und pathologie des bogengangsapparates [Physiology and pathology of the semicircular canal]. Wien, Deuticke. Bárány, R. (1916). Some new methods for functional testing of the vestibular apparatus and the cerebellum. Robert Bárány — Nobel Lecture. NobelPrize.org. Nobel Media AB 2019. Retrieved from https://www.nobelprize.org/prizes/med​ icine/1914/barany/lecture/

Belofsky, N. (2013). Strange medicine: A shocking history of real medical practices through the ages. New York, NY: TarcherPerigee/Penguin. Breuer, J. (1874). Über die funktion der bogengänge des ohrlabyrinthes. Med. Jahrb, S., 72. Breuer, J. (1875). Beiträge zur lehre vom statischen sinne. Med. Jahrb, S. 87. Bracha, A., & Tan, S. Y. (2015). Robert Bárány (1876–1936): The Nobel Prize–winning prisoner of war. Singapore Medical Journal, 56(1), 5–6. Breathnach, C. S. (2010). Hallaran’s circulating swing. History of Psychiatry, 21(81 Pt. 1), 79–84. Cohen, B., & Raphan, T. (2004). The physiology of the vestibuloocular reflex (VOR). In F. M. Highstein, R. R. Fay, & A. N. Popper (Eds.), The vestibular system (pp. 235–285). New York, NY: Springer. Crum-Brown, A. (1874). On the sense of rotation and the anatomy and physiology of the semicircular canals of the internal ear. Journal of Anatomy and Physiology, 8(Pt. 2), 327–331.

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Darwin, E. (1794). Zoonomia; or, the laws of organic life (Vol. I). London, UK. Darwin, E. (1796). Zoonomia; or, the laws of organic life (Vol. II). London, UK. Flourens, P. (1824). Recherches expérimentales sur les propriétés et les functions du système nerveux dans les animaux vertébrés. Paris, France: Crevot. Flourens, P. (1842). Recherches expérimentales sur les propriétés et les functions du système nerveux dans les animaux vertébrés (2nd ed.). Paris, France: Crevot. Griffith, C. R. (1922). An historical survey of vestibular equilibration. Urbana, IL: University of Illinois Press. Harsch, V. (2006). Centrifuge “therapy” for psychiatric patients in Germany in the early 1800s. Aviation, Space, and Environmental Medicine, 77, 157–160. Lorente de Nó, R. (1933). Vestibulo-ocular reflex arc. Archives of Neurology and Psychiatry, 30(2), 245–291. Mach, E. (1875). Grundlinien der lehre von den bewegungsempfindungen. Leipzig, Germany. Nobel Lectures Including Presentation of Speeches and Laureates’ Biographies. Physiology or Medicine. 1901–1921. (1967). Bárány lecture, (1916). Published for the Nobel Foundation in 1967 (pp. 500–511). New York, NY: Elsevier. Nylen, C. O. (1965). Robert Barany. Archive of Otolaryngology, 82, 316–319. Purkyneˇ, J. E. (1820). Beiträge zur näheren kenntniß des schwindels aus heautognostischen daten. Medizin Jahrbuch Kaiser-könig öester Staates, 6, 79–125. Ross, W. D. (Ed.). (1927). The works of Aristotle, Volume 7. Oxford: Clarendon. In N. J. Wade, (2003). Destined for dis-

tinguished oblivion: The scientific vision of William Charles Wells (1757–1817). New York, NY: Springer. Traynor, R. (2015). International giants in otology: Guichard Joseph Duverney. Retrieved from https://hearinghealthmatters.org/hearinginternational/2015/internationalgiants-in-otology-guichard-joseph-duverney/ Wade, N. (2000). William Charles Wells (1757–1817) and vestibular research before Purkinje and Flourens. Journal of Vestibular Research, 10(3), 127–137. Wade, N. J. (2003). Destined for distinguished oblivion: The scientific vision of William Charles Wells (1757–1817). New York, NY: Springer. Wade, N. (2010). The Darwins and Wells: From revolution to evolution. Journal of the History of Neuroscience, 19, 85–104. Wade, N., & Tatler, B. (2005). The moving tablet of the eye: The origins of modern eye movement research. New York, NY: Oxford University Press. Wells, W. C. (1792). An essay upon single vision with two eyes: Together with experiments and observations on several other subjects in optics. William Charles Wells, M.D. London, UK: Printed for T. Cadell, in the Strand. Wells, W. C. (1794). Reply to Darwin on vision. Gentleman’s Magazine, 64, 794–797. Wells, W. C. (1794). Reply to Darwin on vision. Gentleman’s Magazine, 64, 905–907. White, W. J. (1964). A history of the centrifuge in aerospace medicine. Santa Monica, CA: Douglas Aircraft Company, Biotechnology Branch. William Charles Wells (1757–1817) South Carolinian Troy. (1969). Journal of the American Medical Association, 209(1), 106–107.

2 Ontogeny of the Vestibular System and Balance Timothy A. Jones and Sherri M. Jones

Introduction and Background

Detailed knowledge regarding the development of vestibular and auditory function comes largely from the study of animals. Much of the information presented below is based on studies using chick or mouse models, and the corresponding developmental ages in the human are given in weeks post fertilization based on the work of a number of investigators, including Bredberg (1968), Anniko (1983a), Dechesne (1992), Pujol, Lavigne-Rebillard, and Lenoir (1998), Jeffery and Spoor (2004), Sans and Dechesne (1985), and Sulik and Cotanche (2004). Much, if not all, of the postnatal developmental changes observed in mammalian models occur prior to birth in the human. We will indicate human ages estimated or found to correspond to those of animal models, when possible. During the first week of human development following fertilization, the zygote undergoes cleavage to form a blastocyst which then attaches to the uterine wall (i.e., endometrium). By the end of the second week the blastocyst is fully implanted within the endometrium and has formed the bilaminar embryonic disk (Figures 2–1A and D). The laminae are termed epiblast and hypoblast. The cells of the epiblast will give rise to all the cells of the adult. Cells of the hypoblast will form extra-embryonic structures. The basic anatomical axes and planes illustrated are already established by this stage prior to morphogenesis, which is initiated during gastrulation (week 3). The orientation of axes and planes shown are standard conventions and will be referenced throughout the chapter. Morphogenesis begins with gastrulation, which is a process of epiblast cellular proliferation and migration

In the human, embryonic development begins at fertilization of the ovum and lasts until the end of the eighth week after fertilization. The fetal period then extends from the ninth week until birth (36 to 40 weeks after fertilization). There are a number of major events occurring during weeks 3 and 4 of embryonic development that are critical for normal formation of the head and neck, including the ear. This period includes the appearance of the cranial placodes and development of the pharyngeal apparatus. Disturbances in these and other important early processes, as may be produced by genetic variation or exposure to physiological stressors, teratogens, or other factors, can lead to serious head and neck developmental abnormalities, including deafness and vestibular dysgenesis. Our purpose here is to present the normal ontogeny of vestibular sensors. Detailed consideration of the ontogeny of the auditory system as well as the consequences of genetic variation on vestibular and auditory development is available elsewhere (Jones & Jones, 2011). Considered here are developmental events common to both modalities during the early formation of the inner ear and important differences in developmental programs where appropriate. We begin during embryonic development and in particular emphasize the appearance of the first outward structural sign of the emerging inner ear, the otic placode. The chapter concludes with vestibular functional maturation and subsequent acquisition of postural control and balance. 15

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D A

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Figure 2–1.  Anatomical axes and planes in the developing embryo. A. Isolated 3-dimensional bilaminar embryonic disk with connecting stalk. B. Intersecting planes: transverse, median (also called sagittal plane) and horizontal.The transverse or lateral plane contains the left-right (LR) and dorsal-ventral (DV) axes.The medial plane contains the anterior-posterior (AP) and dorsal-ventral axes.The horizontal plane contains the anterior-posterior and left-right axes. C. Anatomical directions in the adult human, embryo, and one amphibian species. D. Schematic representation of an isolated bilaminar embryonic disk as seen from the dorsal view. Anterior-posterior and left-right axes are shown as dashed lines. From Genetics, Embryology, and Development of Auditory and Vestibular Systems (2011) (p. 98) by Sherri M. Jones and Timothy A. Jones.

to produce three distinct germ layers: the ectoderm, mesoderm, and endoderm. All tissues develop from these three germ layers. With the induction of the neural plate, progression of neurulation, and formation of the neural tube, a systematic regional segmentation emerges, which distinguishes the forebrain (prosencephalon), midbrain (mesencephalon), and hindbrain (rhomencephalon) of the incipient brain. The hindbrain is further segmented into seven neuromeres (rhombomeres), where the cells of each neuromere

acquire specific identities such that the cells of each neuromere have unique characteristics and collectively respond to external signals in a manner that differs from neighboring segments. During this period (week 3), cranial placodes develop from ectodermal regions very near their respective neuromeres. Olfactory, visual, and auditory sensory organs as well as cranial sensory ganglia develop from their respective placodes. The inner ear develops from the otic placode (Figure 2–2).



2. Ontogeny of the Vestibular System and Balance

hindbrain

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Figure 2–2.  Formation of the otic vesicle (OV) from the otic placode (OP) over a period from approximately 3 to 4 weeks in the human embryo (follow arrows: 21–23 to 28–35 days post fertilization. [E8.5 to just beyond E10.5 in mouse]). d = days post fertilization. ED = endolymphatic duct; EN = endoderm; CC = central canal; CD = cochlear duct; D = dorsal; L = lateral; Mesoderm = mesenchyme presumptive mesoderm; NP = neural plate; NT = neural tube; OC = otic cup; OP = otic placode; OV = otic vesicle; r5-r6 = rhombomeres 5 and 6; SAG = statoacoustic ganglion; SE = surface ectoderm (epidermis); V = ventral. From Genetics, Embryology, and Development of Auditory and Vestibular Systems (2011) (p. 158) by Sherri M. Jones and Timothy A. Jones.

Formation of the Otic Placode and Otic Vesicle The inner ear is formed from primordial ectodermal cells near neuromeres (rhombomeres) 5 and 6 in the embryonic hindbrain. These cells form a flat, thickened patch of ectoderm called the otic placode during week 3

(see Figure 2–2). The otic placode appears morphologically as the first step in the formation of the inner ear. A variety of genetic signals define a region of tissue committed to form the otic placode, and subsequent molecular signaling leads to the separation of the otic placode from epidermal tissue (reviewed by Ohyama, Groves, & Martin [2007]). According to Groves (2005), the cells ultimately forming the placode are not simply

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gathered from adjacent cells, but rather it appears likely that the cells migrate from a wide area and somehow collect to form the placode. Cells of the otic placode give rise to the otic vesicle (also called the otocyst) at about week 4 (day 26), from which sensory, nonsensory, and most neural cells of the inner ear will be derived (see Figure 2–2). The otic vesicle, however, does not give rise to olivocochlear and vestibular efferent fibers or to autonomic innervation of blood vessels. Shortly after forming, the otic placode begins to bend and fold inward, producing a shallow dimple. This invagination of ectoderm continues until a deep pit is formed, which is called the otic pit or otic cup (see Figure 2–2). The dorsal edge of the otic tissue remains in close approximation to the hindbrain/ neural plate during this process. This association favors molecular signaling and formation of asymmetric molecular signal fields. Ultimately, the otic cup closes to form the otic vesicle. Closure of the otic cup and the proximal neural groove (thus forming the neural tube locally) occurs at about the same time during week 4. During and after its formation, the otic vesicle is influenced by signals from the hindbrain as well as the mesenchyme surrounding the otic vesicle (known as the periotic mesenchyme or mesoderm) that becomes the bony labyrinth of the inner ear. Several important signaling molecules play a dominant role in establishing the dorsal-ventral morphological axis within the otocyst. The dorsal-ventral boundary of the otic vesicle (a line midway between the bottom and top of the otic vesicle) distinguishes the dorsal vestibular sensors from the ventral cochlear sensors. Molecular signals are thought to form gradients of influence along the dorsal-ventral extent of otic tissue (Schneider-Maunoury & Pujades, 2007). Tissue elements at any given position experience a unique combination of signal levels and each combination of signals has the potential to favor one program of development or another. Molecular signals within the otocyst and in the surrounding regions are also responsible for the order and layout of structures along the anteroposterior and mediolateral dimensions of the otic vesicle.

Delamination and Formation of the Statoacoustic Ganglion Under the influence of specific proteins, proneural cells (neuroblasts, i.e., cells that will become afferent neurons) detach from and leave the epithelium of the otic cup and vesicle and then migrate medially and ventrally into the mesenchyme, ultimately to form

the statoacoustic ganglion (Figures 2–2 and 2–3). This process is called delamination; it begins in epithelial regions of the presumptive utricle and cristae as early as week 4 (22 to 28 days) and represents the beginning of neurogenesis. The epithelial neuroblasts divide and ultimately differentiate into auditory and vestibular neurons. Delamination expands to include prosensory regions (i.e., regions containing cells that will become sensory hair cells) within or adjacent to the sacculus and eventually the cochlea. Delamination continues through periods as late as week 9. We will consider the formation of the statoacoustic ganglion in more detail later in the chapter.

Formation of Prosensory Patches For warm-blooded vertebrates, there are six or seven sensory patches in the mature inner ear (utricle, saccule, cochlea, three cristae, and the macula lagena in birds). This list does not include the very small sensory patch called the crista neglecta, about which little is known (Montandon, Gacek, & Kimura, 1970). The sensory epithelia form in close association with the nonsensory components (i.e., cristae with canals, maculae with vestibule, and cochlea with cochlear duct). There is evidence that molecular signals from the sensory patches guide the surrounding nonsensory structures in morphogenesis (reviewed in Bok, Chang, & Wu, 2007). Before such cooperative signaling can occur, the proneural and prosensory cells must be specified and distinguished from the surrounding epithelium. These precursor “neurosensory” cells (cells that in the future may take on a neural or sensory cell fate) are specified early in the development of the otocyst. A neurosensory domain (i.e., region of cells that will become hair cells or neurons) can be identified at late week 4 with the expression of genes that may be viewed as markers for cells destined to become neurons or sensory cells (Bok et al., 2007; Morsli, Choo, Ryan, Johnson, & Wu, 1998). Inactivation of these genes or of corresponding pathways interferes with the formation of the statoacoustic ganglion and sensory organs. Those cells destined to become neural cells will soon delaminate (as described above) while the remaining cells will become the sensory epithelia.

Sensory Patches At late week 4, certain regions of the otic vesicle (regions A, B, and C of Figure 2–3) express specific

E

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Figure 2–3. Lateral views of locations for important markers of prosensory and sensory domains during development. Regions forming the most dorsal sensory epithelia (cristae of semicircular canals) are distinguished early by the expression of particular genes (labels A and B), whereas the more ventral regions are marked with a different combination of signals (labeled C). The ventral prosensory domains elaborate the sensory epithelia of the utricular macula (um), saccular macula (sm) and cochlear duct (cd) in that order. ac = anterior crista. hc = horizontal (lateral) crista. pc = posterior crista. Schematics are based on data from the mouse. Corresponding ages in human are given (weeks post fertilization). Adapted from Bok, Chang, and Wu, 2007 with permission from International Journal of Developmental Biology, 51, 526.

cd ED

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genes that outline the neurosensory domain, including presumptive cristae, maculae, and cochlear prosensory fields as well as the proneural fields where neuroblasts delaminate. The dorsal fields (A and B of Figure 2–3) are distinguished from ventral prosensory regions (C of Figure 2–3) by being marked with different combinations of gene signals. The patterns mark and distinguish which domains become cristae and which become macular and cochlear sensors. The pattern of expression for one gene (Otx1) highlights the region of the presumptive lateral (horizontal) canal, and in its absence (Otx1-/-) the lateral canal fails to form (Morsli et al., 1999). Anteroventral regions of the otocyst form in sequence: first the utricle, then the saccule, and finally the cochlea. As noted above, neuroblasts delaminate from this region and migrate anteriorly to form the statoacoustic ganglion over the period from week 4 to week 9. Initially, there is no distinction between presumptive macular and cochlear regions (see Figure 2–3, week 4); however, development proceeds from dorsal to ventral revealing first the more dorsal utricular maculae (see Figure 2–3, weeks 5 to 6) and then, later, the saccular macula and cochlea (see Figure 2–3, weeks 9 to 10). By week 5, the utricle is clearly segregated and (by late week 5) the saccule is easily recognized, but a clear segregation from cochlear fields is evident only after week 6 (Morsli et al., 1998). Segregation of these macular and cochlear sensory patches requires signals from nonsensory regions of the otic vesicle after week 4 (Nichols et al., 2008). In the absence of such signaling, the utricle, saccule, and cochlea form a combined malformed single mosaic sensory epithelium. The progressive segregation of sensory epithelia also appears to be linked to the simultaneous delamination process as cells migrate from the prosensory regions to become neurons of the statoacoustic ganglion (Fritzsch et al., 2002).

Formation of the Cochlea and Zone of Non-Proliferation The emerging cochlear duct can be seen initially as a lengthening of the ventral pole of the otocyst beginning at about week 5 in humans (see Figure 2–3). The duct continues to extend first ventromedially, then it turns abruptly, anteriorly forming a curved hook by late week 5 (Morsli et al., 1998). This represents initiation of the cochlear coil, and by the sixth week a full half turn is achieved (see Figure 2–3). The cochlea will continue to elongate and increase the number of coils (~2.5 turns in the human adult).

At the early stages of cochlea formation (e.g., weeks 5 to 6), the cochlear duct (Figures 2–3 and 2–4B) houses a thick (four to five cells thick) undifferentiated epithelium that forms a ridge or sheet extending from the base to apex. This ridge of cells contains prosensory cells that have segregated ventrally from the sacculus. The ridge contains the presumptive organ of Corti. All cochlear hair cells and supporting cells will arise from this epithelial ridge. Elongation and coiling of the cochlea continues with the leading edge of extension represented at the apical tip. Beginning at about late week 5, a central strip of the apical epithelial ridge begins to exit the cell cycle and terminate mitosis (Figure 2–4) (Chen, Johnson, Zoghbi, & Segil, 2002; Chen & Segil, 1999; Lee, Liu, & Segil, 2006). Over a period of about a week in humans (late week 5 to week 6), a wave of terminal mitosis sweeps along a central strip of the epithelial ridge from the cochlear apex to base. This is followed shortly afterward by a wave of cells exiting the cell cycle, which also moves along the central strip from the cochlear apex to base forming a cellular zone of nonproliferation (ZNP) along the epithelial ridge (see Figure 2–4) (Chen et al., 2002; Chen & Segil, 1999; Lee et al., 2006). These postmitotic cells form the undifferentiated prosensory domain of the organ of Corti, and its formation is presumably completed before weeks 7 to 8 in humans (Chen et al., 2002; Chen & Segil, 1999; Lee et al., 2006; Ruben, 1967). By approximately week 8, the cochlear coil has reached 1.5 turns and the ZNP is in place (Chen & Segil, 1999). The region of the initial ventromedial cochlear extension in the otocyst continues to elongate during the coiling process, thus (importantly) increasing the distance between the saccular macula and the first turn of the cochlea (Morsli et al., 1998). Elongation of the cochlear epithelium after weeks 7 to 8 must be accomplished without ZNP cell division, since prosensory cells in the ZNP have exited the cell cycle. Completion of the adult number of coils (~2.5 turns) is not accomplished until weeks 9 to 10 (Chen & Segil, 1999; Morsli et al., 1998; Sher, 1971; Suli & Cotanche, 2004). The cochlea continues to elongate in the human from 20 mm to 35 mm between 10 and 16 weeks (Bredberg, 1968; Sulik & Cotanche, 2004). Coiling and elongation of the ZNP is thought to be accomplished largely through the process of convergent extension. For this reason, the cochlea is subject to abnormal morphogenesis (short, thickened organ of Corti) when alterations in planar cell polarity (PCP) signaling are present (Jones & Chen, 2007; Kelley & Chen, 2007; McKenzie, Krupin, & Kelley, 2004; Montcouquiol et al., 2003; Wang et al., 2005; Wang, Guo, & Nathans,



2. Ontogeny of the Vestibular System and Balance

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Radial neurites Figure 2–4.  A. Formation of the zone of non-proliferation (ZNP, marked gray) in the cochlear duct at four periods of development, based on studies in the mouse model (e.g., Chen et al., 2002, Lee et al., 2006). Corresponding estimated ages for the human are shown. The ZNP appears first in the apex and then sweeps towards the base over the next week (48 hours in mouse). The formation of ZNP is completed by approximately week 6 (E14 mouse, Chen et al., 2002, Lee et al., 2006), however, the cochlea continues to elongate and coil until weeks 9 to 10 (P0, mouse). During this latter period of elongation, the sensory epithelium thins and narrows. B. Schematic of the cochlear duct circa week 6 (E14 mouse). According to Lim and Rueda (1992), the greater epithelial ridge (GER) incorporates the region of inner hair cells, whereas the lesser epithelial ridge (LER) incorporates the region where outer hair cells will form. Together they form the floor of the early cochlear duct, also called the epithelial ridge. The zone of non-proliferation identifies the epithelial region of prospective inner and outer hair cells. Kolliker’s organ (KO) has been defined a number of ways. Here, Kolliker’s organ includes only that portion of the GER that does not include prospective sensory hair cells. RIHC = region of inner hair cells. ROHC = region of outer hair cells. From Genetics, Embryology, and Development of Auditory and Vestibular Systems (2011) (pp. 164, 166) by Sherri M. Jones and Timothy A. Jones.

2006). Mutations in, or knock outs of, core PCP genes (or related signaling pathways) prevent elongation and result in a shortened cochlea. The extent to which

vestibular sensors depend on the convergent extension process is not clear. However, like the cochlea, the vestibular epithelia start out as a layered partition of

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four to five epithelial cells and at maturity are reduced to an apical layer of sensory cells supported by one or two non-sensory cells (Dechesne, 1992). Whether the thinning process involves convergent extension has not been clarified (to our knowledge).

Hair Cell Differentiation Before differentiation can begin, vestibular and auditory prosensory epithelial cells must complete the last (or terminal) cell division. This is often referred to as terminal mitosis and is an event noted above in the formation of the cochlear ZNP. The postmitotic prosensory epithelial cells appear structurally like any other cells in the epithelium. There are no superficial structural distinctions and no obvious evidence of axial polarization. Prosensory cells must initiate differentiation before such outward distinctions will appear. Vestibular afferent and efferent neurons are present in sensory regions at about week 6. Prosensory cells demonstrate ongoing mitosis at this time. Within vestibular epithelia there are temporal and spatial gradients over the course of mitosis. In general, central regions (apex of cristae and striolar regions of maculae) initiate and reach peak levels of mitosis well before peripheral regions (base cristae, edges of maculae). Terminal mitosis occurs in a similar order (Mbiene & Sans, 1986; Sans & Chat, 1982). Although these general trends may hold, for any given vestibular region there is a more or less continual eruption of new immature stereociliary bundles until late fetal periods, thus suggesting that some cells do not complete terminal cell division until very late. Differentiation of prosensory cells of the cristae, maculae, and cochlea all require the induction of the gene atonal homolog 1 (Atoh1) (also known as mouse atonal homolog 1, Math1; Bermingham et al., 1999). Prosensory cells exit the cell cycle and ultimately must express Atoh1 before differentiating into hair cells. Atoh1 expression and differentiation of hair cells begin in the cristae and maculae well before similar levels are expressed in the cochlea (Bermingham et al., 1999; Chen et al., 2002; Lanford, Shailam, Norton, Gridley, & Kelley, 2000; Woods, Montcouquiol, & Kelley, 2004). Atoh1 expression is presumably present throughout the sensory epithelium by weeks 8 to 10 and then is downregulated during later fetal periods (Driver et al., 2013; Lanford et al., 2000; Shailam et al., 1999). During differentiation of the sensory epithelium, a remarkable pattern of hair cells and supporting cells emerges. Our understanding of the molecular signals

orchestrating these events is more detailed for the cochlea than vestibular sensors, but in either case, there are many more questions to answer. One feature of both auditory and vestibular epithelia suggests a common organizing mechanism. The presence of orderly patterned mosaics of hair cells and supporting cells in all inner ear sensory epithelia implies a role for Notchmediated lateral inhibition (Lanford et al., 1999, 2000). In particular, all epithelia are arranged such that every hair cell is isolated from other hair cells by a ring of supporting cells or their processes. Lateral inhibition is one strategy that produces a “center on, surround off” pattern, where “on” refers to a hair cell and “off” to a non-sensory supporting cell. In due course across the entire postmitotic sensory epithelium, a molecular scheme can be postulated to produce a mosaic of patches, where each patch is composed of a hair cell surrounded by supporting cells. This scheme is simplistic and incomplete, but it provides a basis for us to begin to understand how such mosaics can be shaped by molecular signaling and how the remarkable structures of the vestibular system and cochlea may be formed. Prior to differentiation, prosensory cells appear as homogeneous epithelial cells interconnected to each other by gap junctions (Dechesne, 1992; Ginzberg & Gilula, 1979). Gap junctions are subsequently lost only in cells committed to a hair cell fate. This occurs during the earliest period of hair cell differentiation (Bryant, Forge, & Richardson, 2005; Forge, Souter, & DenmanJohnson, 1997). Thus, one of the earliest events of hair cell differentiation includes the isolation of hair cells from surrounding supporting cells by eliminating direct electrochemical coupling between them.

Vestibular Stereociliary Bundles The traditional definitive structural sign of hair cell differentiation is the elaboration of microvilli and formation of stereociliary bundles. Using scanning electron microscopy, vestibular hair cells can be definitively identified by about week 8 in the cristae with the appearance of stereociliary bundles (Bryant et al., 2005; Dechesne, 1992; Denman-Johnson & Forge, 1999; Mbiene & Sans, 1986). In contrast, the first morphological evidence of cochlear stereocilia begins to emerge between weeks 10 and 12 (Anniko, 1983b; Lim & Anniko, 1985; Pujol et al., 1998; Sulik & Cotanche, 2004). The earliest hair cells appear with microvilli or stereocilia encircling a single kinocilium in the center of the cell (Figure 2–5). The first sign of intrinsic hair cell

Developing Vestibular Sensory Epithelium

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Maturation and refinement continues Figure 2–5. Development of vestibular stereociliary bundles. Estimated human ages in weeks post fertilization are shown. The earliest stages of development are similar for both auditory and vestibular hair cells although vestibular hair bundles begin appearing much earlier than cochlear bundles. Later developmental stages for auditory hair bundles are very different than those for vestibular bundles. Stereociliary bundles for vestibular epithelia are mature by weeks 20 to 23 (Dechesne, 1992). KC = kinocilium; S = stereocilia; HC = hair cell; BB = basal body; LPR = line of polarity reversal; CP = cuticular plate. From Genetics, Embryology, and Development of Auditory and Vestibular Systems (2011) (p. 174) by Sherri M. Jones and Timothy A. Jones. 23

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Balance Function Assessment and Management

polarization begins almost immediately with a movement of the kinocilium toward the lateral edge of the cell, thus taking an eccentric position in each hair cell. The direction of the movement reflects the emergence of the preferred direction of stimulation for each hair cell and hence the incipient morphological polarization vector (MPV). Preventing the formation of the primary cilium (kinocilium) prevents proper planar orientation of outer hair cells (OHCs; Jones, Roper, et al., 2008). Disruption of PCP signaling pathways has similar effects. In Looptail mouse mutants, auditory and vestibular hair cells are disoriented, indicating a role for PCP signaling in establishing vestibular hair cell orientation (Jones & Chen, 2007; Montcouquiol et al., 2003, 2006; Rida & Chen, 2009). There are also a number of important structures that serve to mechanically couple individual stereocilia together as well as link the stereocilia to the kinocilium mechanically. There is of course the protein linkage to hair cell transduction channels called “tip links” that are critical to sensory transduction. Cadherin 23 (Cdh23) and protocadherin 15 (Pcdh15) make up the tip links (Kazmierczak et al., 2007). Given the complex architecture of the stereociliary bundle (see Chapter 4), much more remains to be learned about its molecular and functional development. Like the cochlea, each vestibular hair cell is surrounded by supporting cells. However, there is an additional layer of organization in the vestibular system. In the cochlea, the direction of polarization for the hair bundle is the same for all hair cells with respect to the axis of the cochlea (all point laterally from the central axis). In vestibular maculae, hair bundle orientation is a function of the particular sensory organ examined. Intrinsic vestibular hair cell polarization is marked by the cells’ MPV. In each crista, MPVs of hair cells are oriented in the same direction. However, in the maculae, MPV orientation depends on the position of the hair cell on the epithelial surface. As noted in Chapter 4 that MPVs of hair cells are arranged systematically over the surface of the macular epithelium, and in the adult both maculae show a line coursing through the middle regions of the epithelium (striolar regions), where MPV directions abruptly reverse. Across this line of polarity reversal, MPVs point in opposite directions. These MPV patterns arise during development and are thought to depend critically both on PCP signaling pathways and on intrinsic cell polarity. Stereociliary bundles are not readily identified in vestibular hair cells before week 7, but as noted above they do begin to appear earlier than auditory hair cells (Bryant et al., 2005; Dechesne, 1992; Denman-Johnson & Forge, 1999; Forge et al., 1997; Mbiene, Favre, & Sans, 1984; Mbiene & Sans, 1986). Similar to the cochlea, the

hair bundle is generally not polarized with its first appearance on a newly formed vestibular hair cell. The kinocilium is centrally located and surrounded by emerging stereocilia (see Figure 2–5). Although outward signs of polarization may not be apparent at this time, intracellular changes have already begun that clearly indicate proteins are being organized asymmetrically in the cell. The progressive development of selected features of vestibular hair cell bundles over the period of 7 to 15 weeks is illustrated in Figure 2–5. Morphological polarization occurs rapidly as the kinocilium assumes an eccentric position on the apical surface of hair cells. By week 8, signs of morphological polarization are seen in large numbers of cells (see Figure 2–5). Moreover, already at this stage there is evidence of a planar organization of MPVs. MPV angles shift systematically as a function of position over the macular surface. A clear line of MPV reversal, however, is not seen. Thus, like auditory hair cells, planar organization of vestibular MPVs does not precisely match the mature organization initially. Reorientation of incipient MPVs is required. This happens early in rodents. The striolar line of MPV reversal is sharp and clearly established several days before birth in the mouse (Denman-Johnson & Forge, 1999) and likely by weeks 10 to 12 in the human. The cuticular plate is first apparent in some macular hair cells using electron microscopy at about this time (week 10), although traces of the cuticular plate are seen earlier using specific immunological markers (Nishida et al., 1998). Once bundles appear in vestibular hair cells, development of the normal staircase form and maturation occurs rapidly (see Figure 2–5). By weeks 11 to 12, typical staircase shapes and numerous lateral and tip stereocilia links can be found (Anniko, 1983a; Forge et al., 1997; Mbiene & Sans, 1986). Bundle height increases progressively in the mouse embryo, reaching mature heights only after birth (Denman-Johnson & Forge, 1999). In the human, bundle height increases dramatically between weeks 10 and 11, and the bundles have achieved adult size by approximately week 15 (Dechesne, 1992). Functional transduction channels make their appearance in the tips of stereocilia (in mice) several days before birth (Géléoc & Holt, 2003) and are estimated to appear by approximately week 12 for the human. Nascent hair cells continue to appear at the vestibular epithelial surface. Discrete samples in time give the impression of successive waves of new immature bundles. Hair bundles at various stages of development continue to mature, and the overlying otoconial membrane continues to elaborate until relatively mature hair bundles dominate the surface during weeks 11 to 12 (Dechesne, 1992; Denman-Johnson & Forge, 1999).



2. Ontogeny of the Vestibular System and Balance

Innervation of the Vestibular End Organs There are three types of innervation to the inner ear. First, vestibular receptors communicate information about head motion to the brain via primary sensory afferent neurons having cell bodies in the peripheral statoacoustic ganglion. The statoacoustic ganglion neurons arise from within the otocyst during development as noted above. Second, the brain can also modify peripheral sensory receptors by adjusting activity in efferent neurons that have cell bodies in the brainstem and axon terminals on the inner ear hair cell sensors or on primary afferent terminals. Efferent neurons arise from rhombomere 4 during development (see below). Third, blood vessels of the inner ear are under the control of sympathetic neurons. These autonomic neurons originate from neural crest cells during development.

Development of Afferent Innervation The statoacoustic ganglion and its neural projections form over the period from weeks 4 to 9 as progenitor cells delaminate from the anteroventral wall of the otocyst. By week 7, vestibular and cochlear anlagen can be distinguished histologically as pars superior and pars inferior of the statoacoustic ganglion, respectively. Although distinguishable, these two portions remain as a contiguous collection of cells until about week 9, when they actually separate physically into the spiral and vestibular ganglia (Sher, 1971; Sulik & Cotanche, 2004). The geniculate ganglion (seventh or facial cranial nerve) separates completely from the vestibular ganglion finally on P1 in mouse. Most sensory neurons are born between weeks 4 and 8. During week 6, fibers from the statoacoustic ganglion can be seen entering the rostrolateral wall and projecting well into the epithelium near the luminal surface of the otocyst (Dechesne, 1992; Sher, 1971; Van de Water, 1984). Efferent neurites arrive at about the same time (Bruce, Kingsley, Nichols, & Fritzsch, 1997). The presence of auditory and vestibular afferents in epithelia is thought to slightly precede the arrival of efferent terminals, and efferent neurites appear to follow afferent tracts during their growth (Bruce et al., 1997). Neurotrophins regulate primary afferent innervation density. Neurotrophins are proteins secreted by target tissues that serve to prevent the natural cell death of path-finding neurons (Davies, 1996; LeviMontalcini, 1987; Levi-Montalcini & Angeletti, 1968; Lewin & Barde, 1996). Hypothetically, the amount of

neurotrophin present ultimately determines the number of neural cells that survive to innervate target cells. This ability to determine whether developing neurons survive is known as a neurotrophic effect. Elevated amounts of neurotrophin can cause excessive growth of neurites, whereas reduced levels of neurotrophin decrease neurite outgrowth and decrease survival of cells. The absence of neurotrophins can result in the loss of innervation entirely. Neurotrophins also have neurotropic effects, that is, they may serve to guide neurites along their growth paths (Fekete & Camparo, 2007; Fritzsch, Silas-Santiago, Bianchi, & Farinas, 1997; Levi-Montalcini, 1987). The elaboration of afferent neurites appears to occur simultaneously with the delamination process in the otocyst. Two processes underlying afferent innervation of sensors have been emphasized (Fekete & Camparo, 2007; Fritzsch et al., 1997). In one model, neuroblasts send neurites back into sensory epithelia after delaminating and migrating out of the otocyst. This model requires a major guidance signal to aid neurites in their pathfinding. In the second model, the dendritic terminal endings of afferent neurites remain in the region of the original site of delamination, whereas the cell bodies migrate (translocate) to the mesenchyme rostromedial to the otocyst. This leaves a ready-made dendritic path to target sensory regions. In this case, even though neurites are initially in the proximity of target sensory regions, they must still grow extensively and find their specific final sensory destinations. This second model provides an early-formed path for arriving efferent neurites to follow on their way to the vestibular epithelium. There is evidence for both models, and it is conceivable that both models operate to some extent depending on the sensory organ involved. The importance of each model may depend on the class in question (e.g., aves versus mammalia). The molecular cues operating to guide neurite growth are not clear in the inner ear, although several candidates have been entertained (Fekete & Camparo, 2007; Fritzsch et al., 1997; Pauley, Matei, Beisel, & Fritzsch, 2005). The candidates include neurotrophins that may be involved in both guidance and survival of primary afferent dendrites. The neurotrophins’ brain-derived neurotrophic factor (BDNF) and neurotrophin-3 (NT-3) are required for proper innervation patterns and maintenance of all inner ear ganglion cells. In the absence of BDNF and NT-3, all ganglion cells die before birth (Ernfors, Van de Water, Loring, & Jaenisch, 1995; Liebl, Tessarollo, Palko, & Parada, 1997; Silos-Santiago, Fagan, Garber, Fritzsch, & Barbacid, 1997). Statoacoustic ganglion neurons must also form central projections. Neurites of the central axon must

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Balance Function Assessment and Management

grow and terminate on cells within the vestibular nuclei of the brainstem and cerebellum. Guidance mechanisms for axons projecting to the central nervous system (CNS) are independent of those responsible for peripheral afferent terminations (Pauley et al., 2005). The signals guiding central afferent projections are unknown. By week 7, peripheral afferent projections extend to all presumptive vestibular sensory epithelia (cristae and maculae) as well as to the wall of the cochlear duct (Dechesne, 1992; Sher, 1971). Terminals for vestibular afferent neurons at this stage are immature, and the final differentiation and refinement of these projections take place over a prolonged period. In the mouse, final refinements in vestibular dendrites are made during postnatal periods. In the human, final refinements occur during the last trimester. Vestibular afferent neurite terminals are present in the undifferentiated prosensory epithelium of the otocyst (see above). Specialized synaptic contacts have been reported for the mouse vestibular epithelium as early as five days before birth (e.g., E15; Mbiene, Favre, & Sans, 1988). The earliest vestibular synaptic contacts form on postmitotic prosensory cells before, or coincident with, the onset of hair cell differentiation. Development of primary afferents in the human parallels events characterized in other mammals. Unmyelinated vestibular primary afferents in humans arrive in the undifferentiated epithelium during weeks 6 to 7 (Dechesne, 1992; Desmadryl, Dechesne, & Raymond, 1992). Apical tight junctions are present in nascent hair cells and prosensory epithelia in the human during this early period. Afferent neurites form numerous synaptic contacts on hair cells, displaying emerging kinocilia by week 8. By 14 to 15 weeks, most hair bundles are relatively mature, with only a few immature bundles appearing on the surface (Dechesne, 1992). Thus, given an early presence, it is likely that the earliest primary afferent contacts are made with immature “nonpolarized” hair cells. Through collateralization, contacts may be made with a mixture of nonpolarized and polarized hair cells. Descriptions of the surface of the vestibular epithelium at 8 to 10 weeks suggest that, at any given time, despite a clearly established striolar boundary, there are typically several hair cell developmental stages coexisting in the same vicinity. Moreover, this developmental mosaic is generalized across the macula (Denman-Johnson & Forge, 1999). Hair cells with immature bundles appear between relatively more mature hair cells, forming a complex mosaic of hair cell stages. It is reasonable to imagine that a sensory unit, defined as one primary afferent and all hair cells it innervates, also incorporates a mosaic of hair cell

polarization stages and directions at this stage. Thus, nascent sensory units are likely composed of hair cells that do not have a uniform hair bundle polarization status. Indeed, it would appear that hair cells at this stage may take on a wide range of immature features, including hair cells with varying and just-emerging polarization vectors, particularly those innervating regions of the line of polarity reversal. It is important to note that by week 10 in the human (Dechesne, 1992) and during the period from E14 to E16 in the mouse, otoconial growth begins and calcification rates are at their highest levels (Lim, 1984; Nakahara & Bevelander, 1979; Salamat, Ross, & Peacor, 1980; Veenhof, 1969). Presumably, stimulus-dependent developmental processes in macular organs could only become effective during and after this period of otoconial formation. Although initial contacts may form early (weeks 6 to 7), they may not be functional synaptic contacts, as most of the differentiation of vestibular neural dendrites occurs relatively late, from week 11 to week 23 (Dechesne et al., 1994; Rüsch, Lysakowski, & Eatock, 1998; Van de Water, Anniko, & Wersall, 1977). Similarly, the final maturation of vestibular hair cells (particularly membrane conductances), especially type I hair cells, occurs during the first and second postnatal weeks for mice (weeks 23+ for humans) (Dechesne, 1992). By week 8, primary afferent dendrites penetrate the basal lamina of the sensory epithelium and send a single process passing through lower layers to the superficial apical layer, where they branch to produce several undifferentiated collaterals (Desmadryl et al., 1992). The terminals are initially restricted in their extent and density, but by week 12 they begin to ramify considerably, covering distances of 30 to 50 microns. At week 8, clear evidence of synaptic contacts between afferents and hair cells is present. Synaptic bodies and coated vesicles can be recognized in hair cell synaptic regions at 8 to 10 weeks (Dechesne, 1992). At these early stages the afferent terminals are still immature. Soon thereafter (week 12), the first evidence of incomplete calyces as well as bouton terminals can be seen (Dechesne, 1992; Dechesne et al., 1994; Rüsch, Lysakowski et al., 1998; Van De Water et al., 1977). During weeks 12 to 13, some maturation is observed, and incomplete calyces, boutons, and type I and type II hair cells can be distinguished but are not mature. Numerous tethered dense core vesicles associated with wellformed synaptic ribbons can be identified between weeks 13 and 15 in the human (Dechesne, 1992). By approximately week 20, all three dendritic types are present (calyx only, bouton only, dimorphs) and are distributed in their normal proportions over the crista. Although most features of the mature cristae are pres-



2. Ontogeny of the Vestibular System and Balance

ent, fine structure and function of the vestibular system in general continues to mature over several weeks after birth in the mouse. Development of these late features is discussed in more detail below.

>12). It is likely that efferent contacts are made on the progenitors of type I hair cells prior to calyx formation (Favre & Sans, 1978). However, what role, if any, these terminals play in the differentiation and maturation of the type I hair cell is unknown. In his pioneering work, Van De Water (1976) concluded that there was no influence of innervation on cytodifferentiation in explanted otocysts. Inasmuch as there was no ultrastructural evaluation of the explants, it may be worth re-examining this issue.

Development of Efferent Innervation The first efferent axons arrive in the prosensory regions of the otocyst at about week 6 (E12 in mouse; Fritzsch & Nichols, 1993; Pujol et al., 1998). These neural processes have origins (cell bodies) in rhombomere 4 of the hindbrain (future brainstem; see Simmons, Duncan, Craponde Caprona, & Fritzsch, 2011 for review) and appear in the otocyst before hair cell differentiation (Bruce, Kingsley, Nichols, & Fritzsch, 1997). Initially, vestibular efferent cell bodies form a single nucleus on each side of the brainstem (medial to vestibular nuclei, lateral to cranial nerve motor nucleus VI). Both ipsilateral and contralateral cell bodies give rise to early projections to each end organ. On either side of the cochlear and vestibular ganglia, efferent fibers tend to grow along the afferent tracts, and their appearance in time follows that of afferent projections (Bruce et al., 1997; Bruce, Christensen, & Warr, 2000). In the absence of afferent projections, efferent neurites do not reach the end organs (Ma, Anderson, & Fritzsch, 2000). Efferents travel in the vestibular nerve until they reach the vestibulocochlear anastomosis, at which point cochlear efferents segregate from vestibular efferents and enter the spiral ganglion, initiating the intraganglionic spiral bundle (IGSB) by weeks 8 to 9. The IGSB follows the spiral ganglion through the course of the cochlear coil. There is some evidence that the earliest arrivals in the cochlea are medial olivocochlear fibers with cell body origins distinct from vestibular efferents (reviewed by Simmons, 2002). As noted, vestibular efferents reach prosensory regions of the otocyst by weeks 6 to 7, presumably having followed projections of postmitotic delaminating vestibular ganglion cells. Ultimately, efferent neurites follow afferent projections in the inferior and superior vestibular nerves to reach their respective end organs. Little is known about the nature of terminal contacts made by efferents during these very early embryonic periods. It is likely that early efferent arrivals contact precursors to both type I and type II hair cells directly. Ultimately, efferents undergo extensive branching in all end organs and form bouton type axosomatic endings on type II hair cells and at later stages form axodendritic endings on calyx dendrites innervating type I vestibular hair cells. Axodendritic efferent contacts appear relatively late, since calyces begin forming late (week

Late Development and Maturation of Vestibular Sensors Although still immature, the human can hear and respond to head movement at birth. Therefore, a functional inner ear emerges in the human fetus and, for this reason, the human is considered to be precocial. In contrast, many nonhuman mammals (e.g., mice, rats, cats, dogs, ferrets; Curthoys, 1983; Heywood et al., 1976; Rüsch, Lysakowski et al., 1998; Van Cleave & Shall, 2006) are relatively unresponsive to head movement and are deaf at birth and thus are considered altricial (or altricous). Vestibular function in these neonatal, non­human mammals matures during subsequent weeks. In order to perceive head motion, the forces associated with head movement must reach the vestibular sensory apparatus, hair cells must transduce the mechanical stimulus into membrane currents and release neurotransmitter, and postsynaptic vestibular ganglion neurons must respond to the neurotransmitter and transmit discharges to the CNS. Once in the CNS, the signals must be processed and relayed via the brainstem nuclei and thalamus to vestibular sensory regions of the cortex (e.g., Lopez & Blanke, 2011; Shiroyama et al., 1999), where perception can take place. We focus here on the emergence of peripheral vestibular function, which covers adequate stimulation, stimulus transduction, and encoding of information in the primary afferents of the vestibular nerve. More details about the mature central vestibular system are briefly summarized in Chapter 4.

Adequate Stimulation The vestibular system is an example of a special sense that relies on elaborate ancillary structures to preferentially select, from among numerous potential environmental stimuli, only a few particular mechanical events that serve as adequate stimuli. For example,

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both vestibular and auditory hair cells are mechanoreceptors responding to displacement of the hair bundle along the axis of polarization. However, the most effective stimulus causing such shearing motion naturally is considerably different for the two sensors. In the vestibular system, normal head motion is effective in stimulating vestibular hair cells but not cochlear hair cells. Low levels of airborne sound effectively stimulate cochlear but not vestibular hair cells. Special structures are largely responsible for these functional attributes, rather than substantial differences in the receptors themselves (although there are significant differences to be sure). In the vestibular system, there are dense otoconia that are packed into the otoconial membrane lying immediately over the stereociliary bundles in the maculae (utricle and saccule, see Chapter 4). These dense otoconial crystals, being fixed in the otoconial matrix, introduce a shearing force on macular hair cell bundles when placed under a linear acceleration field. Such a field occurs in association with head movement or in the presence of gravity, thus leading to the displacement of the otoconial membrane and stimulation of macular sensors. Without dense otoconia, macular hair cells are not stimulated (Jones, Erway, Bergstrom, Schimenti, & Jones, 1999; Jones, Jones, & Hoffman, 2008). Stimulation of ampullary organs depends on the semicircular canals and the inherent inertia of the endolymphatic fluids within the membranous labyrinth (see Chapter 4). During head rotation, pressure gradients develop across the cupula within the canal lumen due to the inertia of endolymphatic fluid. These pressure gradients distort the cupula and produce shearing forces at the surface of the sensory epithelium where hair cell bundles are displaced and hair cells are activated or inhibited. Without the canals and their fluidfilled patent lumens, the ampullae would be insensitive to head rotation.

Development of Vestibular Function In mammals, movements of the mother or the fetus could serve as natural stimuli before birth. However, the actual time of onset for vestibular function (i.e., an adequate stimulus producing an appropriate neural response) during development in mammals and birds has not been determined. Nonetheless, we can estimate an earliest age based on known requirements for a functioning vestibular apparatus. In mice, the otoconial membrane and otoconia form early in the embryo (from E14 to E16) and continue to elaborate at

least until birth (Anniko, 1983a; Lim 1984; Nakahara & Bevelander, 1979; Salamat, Ross, & Peacor, 1980; Veenhof, 1969). In the human this occurs in the fetus by week 10 (Dechesne, 1992). The semicircular canals form even earlier, initially as epithelial tubes (semicircular ducts, beginning about E12.5 in the mouse; Lim & Anniko, 1985; Sher, 1971). The ducts generally are well formed and patent by about week 7 in the human (E15.5 in mouse). Between weeks 6 and 7, the crosssectional shape of the ducts enlarges from a slit-like form to a much wider oval and the three ampullae are present by week 7. The cristae emerge during this same period. The incipient cupula forms a thin membrane extending from the crista to the ampullar roof (Anniko, 1983a; Lim & Anniko, 1985). In the human, the cupula is present by week 8 (Dechesne, 1992). By the tenth to twelfth weeks, the crista and cupula are well formed and semicircular ducts have the characteristic circular cross section (Lim & Anniko, 1985). Thus it is conceivable that natural stimulation of ampullar and macular sensors could begin at 9 to 12 weeks in the human (Dechesne, 1992).

Transduction Channels and Associated Membrane Currents Although delivery of an adequate stimulus to the vestibular epithelium may be possible in the fetal human and mouse, it is reasonable to question whether vestibular receptors are capable of responding to natural stimulation prior to birth. Hair cell transduction channels are believed to be located in the tips of stereocilia (Beurg et al., 2009; Hudspeth, 1982). The opening and closing of transduction channels are thought to be controlled by protein tip links tethered to adjacent stereocilia (Hudspeth, 1985; Pickles, Comis, & Osborne, 1984; Xu et al., 2009). When such transduction channels become functional in the human is not known. However, we can gain insight on the probable timing of functional onset from studies in other mammals. Functional transduction channels appear first in vestibular hair cells. In the mouse, they appear suddenly over a period of approximately 24 hours between E16 and E17 (Géléoc & Holt, 2003), which corresponds to about week 12 in the human. Tip links may appear one or two days earlier than transduction channels in the mouse (Denman-Johnson & Forge, 1999; Nayak, Ratnayaka, Goodyear, & Richardson, 2007). This timing parallels that of the appearance of otoconia in the maculae (Anniko, 1983a; Lim, 1984; Nakahara & Bevelander, 1979; Salamat et al., 1980; Veenhof, 1969) and the canal



2. Ontogeny of the Vestibular System and Balance

apparatus for the ampullae noted above. Thus in the mammalian fetus, natural mechanical stimuli likely do reach vestibular hair cell receptors as they acquire the ability to transduce them into receptor potentials.

responses to simulated transduction currents at the earliest stages are slow and follow stimulus current profiles poorly. With the upregulation of particular genes and the acquisition of new membrane conductances, the hair cell’s ability to follow stimuli improves. In the bird, mature-like vestibular hair cell membrane responses and a full complement of ion channels are present just before hatching (Masetto et al., 2000), whereas in the altricial mammal the mature configurations of channels and more mature responses emerge in the late embryo and neonate (E18 to P4; Géléoc, Risner, & Holt, 2004; Masetto et al., 2000; Rüsch & Eatock, 1996; Rüsch, Lysakowski, & Eatock, 1998). Figure 2–6 illustrates how a vestibular hair cell receptor response to a depolarizing current step changes with the acquisition of new basolateral hair cell channels during development. The imposed depolarizing current is used to simulate depolarizing transduction currents. A relatively mature response (bottom trace) does not appear until the gK,L channels are present. The voltage response of the hair cell is the resulting receptor potential, which modulates transmitter release from the hair cell. Note the changes in the shape of the receptor potential as new ion channels are added at different ages of development. Although it is not known, one would anticipate (based on studies in animals) that mature hair cell responses to stimulation would be present prior to birth after 20 weeks in the human. A number of studies have examined the temporal sequence of channel acquisition in animals (Eatock & Rüsch, 1997; Géléoc et al., 2004; Géléoc & Holt 2003; Hurley et al., 2006; Li, Meredith, & Rennie, 2010; Masetto et al., 2003; Rüsch, Lysakowski, et al., 1998; Sokolowski et al., 1993). We have tabulated the sequence of acquisition of several membrane ion channels for the chick and mouse (Table 2–1) based on the work of several laboratories (i.e., Géléoc et al., 2004; Masetto et al., 2000; Rüsch, Lysakowski, et al., 1998). One striking difference to be noted regarding the acquisition sequence in vestibular hair cells versus that for auditory hair cells is the fact that there are no descriptions of Ca2+-based hair cell action potentials (spikes) during vestibular development. Although the reason for this has not been explored, one might speculate that the early appearance of the fast IKA and IK(Ca) (BK) channels in vestibular hair cells may prevent the development of hair cell spiking. In the cochlea, BK channels appear late in the maturation of inner hair cells (IHCs), and prior to their appearance, the IHCs generate spontaneous Ca2+-based action potentials. This spontaneous action potential activity is thought to be critical for the refinement of peripheral and central auditory neural

Hair Cell Response to Transduction Currents The appropriate hair cell response to an adequate stimulus requires more than just transduction channels. The vestibular hair cell response to transduction currents (i.e., the sensory receptor potential) depends on the nature of ionic channels located within basolateral portions of the hair cell membrane. When gated open, these basolateral ion channels permit the movement of particular ions across the membrane, thus contributing to current flow. Collectively, the ability to conduct currents (i.e., the property of conductance, symbolized as “g”) depends on the number of channels open for each type of channel. Each channel type is named according to the dominant ion species it conducts. Currents associated with particular channels are often designated with an “I” and a subscript indicating the specific ion channel (e.g., potassium current, IK). Conductance associated with the current IK for example is designated as gK. There are a variety of voltage-gated channels that are important in shaping the receptor potential. These include K+, Na+, and Ca2+ channels (Eatock & Hurley, 2003). These currents determine the resultant hair cell receptor potential and in turn the characteristics of neurotransmitter release and transmission from hair cell to primary afferent. Thus, they determine the very nature of the transfer of information about head motion and ambient sound to the primary afferent and ultimately to the brain. The mature hair cell receptor potential reproduces the shape of an applied depolarizing current. Thus, the mature receptor potential normally follows the input signal reliably so that the gating of channels at the basolateral surface and the release of neurotransmitter is synchronized to the stimulus input. Based on work in animals, we know that the first hair cells born are not equipped with the adult complement of basolateral membrane ion channels. Undifferentiated otocyst cells and new hair cells (weeks 7 to 8) have few if any voltage-gated K+ membrane channels (Correia, Rennie, & Koo, 2001; Eatock & Hurley, 2003; Sokolowski, Stahl, & Fuchs, 1993). Specific channels appear at different developmental stages in hair cells and each channel can impart different characteristics to the hair cells’ response to transduction currents. Early hair cell

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Stimulus:

Depolarizing Current

pA

Responses: Early

mV mV mV

Late

mV

1. 2. 3. 4.

gKv at E10–E12 +gKA at E14 -gKA at E14 +gK,L at E18

Figure 2–6. The effects of acquiring selected K+ channels on the hair cell receptor response. Top tracing shows the hypothetical step depolarizing current applied. This depolarization simulates transduction currents (levels reflected in picoamps, pA). The four traces below the stimulus, (traces 1–4), are schematic representations of the receptor potential response. During development, the shape of the receptor potential changes with the addition or removal of each channel. The first response tracing represents a young age where the hair cell has acquired only the early delayed rectifier, gKv (trace 1). Additional channels appear successively over time (e.g., gKA, gK(Ca) and gK,L traces 2 and 4). Traces 2 and 3 illustrate the kind of change in membrane response produced by electrically inactivating gKA (-gKA) before presenting the stimulus (trace 3). Corresponding ages in the chick embryo are shown to the right of traces. Note how ultimately the response follows the step depolarizing currents closely as the cell acquires gK,L (trace 4) and matures. Hair cell membrane voltage responses (mV) are schematic representations of data reported by Masetto et al. (2000) and Chen and Eatock (2000) with permission. From Genetics, Embryology, and Development of Auditory and Vestibular Systems (2011) (p. 216) by Sherri M. Jones and Timothy A. Jones.

circuits during development (e.g., Jones & Jones, 2011). Cochlear IHC spiking disappears as BK channels are upregulated during development just before the onset of hearing (Brandt et al., 2007; Fuchs & Sokolowski, 1990; Kros et al., 1998; Marcotti et al., 2003a; Schweizer et al., 2009).

Behavioral Response to Head Motion In the precocial chicken, there is no question that the vestibular system is virtually mature at hatch inasmuch

as hatchlings quickly learn to walk bipedally within minutes to hours. In the human, it also is likely that the peripheral vestibular system is mature at birth. However, it will be at least a year before any walking is done. Considerable maturation is required in central motor control circuitry as well as in the skeletomotor system itself. To evaluate the development of vestibular responses to head motion, it is useful to study the behavior of altricial mammals (rats, cats, mice, gerbils, etc.). In such animals, during a span of 2 or 3 weeks, the vestibular apparatus goes from nonfunctional to functionally mature and this occurs with observable behaviors. When a mature animal lying face up is



2. Ontogeny of the Vestibular System and Balance

Table 2–1.  Age of Appearance for Various Currents Recorded from Vestibular Hair Cells or Primary Afferent Neurons in the Chick and Mouse*

tory eye movements are mature at 6 to 10 months of age (e.g., Cioni, Favilla, Ghelarducci, & La Noce, 1984; Cyr, Brookhouser, Valente, & Grossman, 1985; VienerWacher, Toupet, & Narcy, 1996), although other aspects continue to mature up to late childhood or adolescence (e.g., Cyr et al., 1985; Herman, Maulucci, & Stuyck, 1982; Valente, 2007; Viener-Wacher et al., 1996). Studies of standing balance function generally demonstrate continued maturation of balance into late childhood and adolescence (e.g., Casselbrant et al., 2010; Charpiot, Tringali, Ionescu, Vital-Durand, & Ferber-Viart, 2010; Hirabayashi & Iwasaki 1995; Valente, 2007). It is likely that behavioral maturation in the human is due to central myelination and circuit refinements after birth. Recent work in this area is summarized at the end of this section.

Current

Chick

Mouse

IKv

E10

E14

ICa

E10

E15–birth**

IKA

E12

?

IK(Ca)

E14

P12–P23***

Ih

E16

P3

IK,L

E17

E18

IKir

E19

E15

*The appearance and distribution of different ion channels throughout development contribute to the developing hair cell’s response to stimulation, release of neurotransmitter, and developing neural discharge patterns. Information from Masetto et al. (2000) and Géléoc et al. (2004) unless otherwise noted. Chicken: equivalent days of incubation (E) are given based on Hamburger and Hamilton (1951) staging. Mouse: embryonic (E) days of gestation are equivalent to days post conception (dpc, Kaufman, 1992). Days postnatal are designated with a “P” where P0 is the day of birth or hatch. “?” = not reported. **Expression in vestibular primary afferents beginning at E15 and decreasing by birth. Changes in the density of the different ICa types (L, P/Q, N, R, T) also occurred from E15 to birth (Chambard, Chabbert, Sans, & Desmadryl, 1999). ***Based on expression of BK channels in the rat (Schweizer, Savin, Luu, Sultemeier, & Hoffman, 2009), which first appear at P12 and diminish by P23.

dropped from a reasonable height onto a soft sponge base, it will turn quickly to right itself and land on its feet. This is the air-righting reflex and it can be used to assess the combined maturity of the vestibular and motor control systems. This reflex is absent at birth in rats when the vestibular system is still immature. It appears first between 9 and 14 days after birth (e.g., Hard & Larsson, 1975; Laouris, Kalli-Laouri, & Schwartze, 1990). In contrast, reflex compensation to maintain gaze during rotation on a turntable appears as early as 3 days after birth in the rat (Parrad & Cottereau, 1977). Thus, despite immature peripheral receptors (noted above), it is clear that some behavioral responses can be elicited in the neonatal rodent. Of course behavioral testing alone leaves open the question of whether the behavioral immaturities reflect the functional status of peripheral or central components or both. Human studies evaluating eye movements in response to rotational stimuli suggest that some aspects of compensa-

Primary Afferent Function When recording normal mature individual vestibular primary afferent neurons in the absence of head movement, the neurons are not silent but rather discharge spontaneously and continuously (Figure 2–7). This is true for afferent neurons innervating both ampullar (semicircular canal) and macular (otoconial gravity receptors) epithelia. Discharge rate (action potentials/ sec, also called spikes/sec) remains relatively constant unless the head is moved thus stimulating or inhibiting hair cells and neurons innervating them. At first thought, in the absence of head movement one might suppose that such tonic activity is due to the constant stimulation of gravity receptors (utricle and saccule) by the ever-present gravitation field of Earth. However, tonic spontaneous vestibular afferent discharge is present in animals that have no otoconia and thus animals that cannot sense gravity (Jones, Jones, et al., 2008). Continuous (tonic) activity arising from the vestibular sensors normally provides a profound influence on CNS circuitry throughout most of the neuraxis including brainstem, hypothalamic, and limbic systems (e.g., Balaban, 2002; Porter & Balaban, 1997; Balaban & Porter, 1998; Yates, 1996; Yates & Miller, 1998). These afferent signals assert a powerful influence on descending skeletomotor and autonomic systems and provide input for compensatory eye movements, perceptual tracking of position, and orientation in space. Tonic vestibular activity constantly adjusts alpha and gamma motor neuron outflow, thus controlling background antigravity muscle tone and posture under an imposing gravitational force field. Therefore, spontaneous as well as sensory-induced tonic activity arising

31

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Balance Function Assessment and Management

A.

Adult

Irregular Discharge Adult

CVm*: 0.462 82.0spikes/s

Regular Discharge Adult

CVm*: 0.033 75.5spikes/s 0.2s

B.

0

P7 Neonate

4

8

12

16

20

24

Time (s) Figure 2–7. Spontaneous discharge activity of vestibular primary afferent neurons in mice. A. Adult mice: Each voltage spike represents an individual action potential. No stimulus is presented. These cells were chosen for illustration because they have similar high discharge rates. Two types of activity patterns are recognized. Irregular discharge (top tracing) is characterized by irregular spacing between spikes, and a high CV. A regular spike discharge pattern tends to show regular spacing between spikes and a low CV. Modified from Jones, Jones, et al. (2008). B. Spontaneous spike train of primary afferent neuron recorded from the superior vestibular nerve in the neonatal mouse at P7 (corresponding human age: 10 to 12 weeks). Note the time scale difference in B. This record was made over a period of approximately 24 seconds. Each vertical “spike” represents the onset time of the neural spike discharge during this portion of the recording. Discharge rate is slow and an irregular firing pattern (with high CV) typical for neonatal vestibular neurons is apparent. Unpublished data. CVm* = indicates that CV values were normalized for spontaneous rate based on mouse data. From Genetics, Embryology, and Development of Auditory and Vestibular Systems (2011) (p. 219) by Sherri M. Jones and Timothy A. Jones.

from vestibular sensors plays an important role in nervous system function. Spontaneous vestibular discharge patterns are of two types in mammals and birds: regular and irregular. Just how regular or irregular the neural discharge is depends in part on the nature of the dendritic synaptic termination and on the nature of the membrane channels resident in the neuron (Eatock, Xue, & Kalluri, 2008; Iwasaki, Chihara, Komuta, Ito, & Sahara,

2008; Kalluri, Xue, & Eatock, 2010). The regularity can vary widely and this variety can be quantified using a single number called the coefficient of variation (CV = standard deviation/mean spike interval). The value of the CV normally varies between 0 and 1. The CV approaches 1.0 as the discharge pattern becomes more irregular (more stochastic, to be precise), whereas the CV approaches 0.0 as the discharge becomes more regular. Figure 2–7 illustrates the discharge patterns of reg-



2. Ontogeny of the Vestibular System and Balance

ular and irregular vestibular afferents in mature (Figure 2–7A) and developing (Figure 2–7B, P7 neonate) mice. Discharge rates in mature mice range from less than 10 to over 140 spikes/sec, with most between 55 and 110 spikes/sec (e.g., Jones, Jones, et al., 2008). The recordings of Figure 2–7B were made in vivo from primary afferent neurons of the superior vestibular nerve (Jones & Jones, 2011). The discharge pattern of the neonate reflects a relatively low discharge rate (~8 spikes/sec) with irregular discharge timing (CV = 0.66). Recording the activity patterns of individual vestibular primary afferent neurons in intact animals (i.e., in vivo) is challenging. Some investigators have instead explored the use of vestibular explant preparations. In this case, the labyrinth with the ganglia are removed and maintained in a physiological solution. Vestibular primary afferents recorded in a mouse inner ear explant preparation are also spontaneously active (Desmadryl, Raymond, & Sans, 1986). Afferent discharge patterns in explants have been measured on different postnatal days. Mean spontaneous discharge rates were low initially (day of birth, P0: 5 to 10 spikes/sec) and all neurons displayed irregular activity. Remarkably, regular discharge patterns were found at P1 and older. Beginning between P6 and P8, discharge rates increase dramatically (>80 spikes/sec), and the proportion of regular fibers increase as well. In a similar preparation in the chicken, Galicia, Cotes, and Galindo (2010) reported irregular spontaneous discharge rates on the order of 40 spikes/sec and CVs above 1.0 in recordings as early as five days before birth (E15). Many of the patterns found in the in vitro preparation were similar to those reported for in vivo studies (discussed below). In vitro studies provide many practical advantages while at the same time raising the question of whether neurons behave the same when studied in their natural environment, that is, in vivo. Spontaneous discharge patterns of horizontal canal neurons have also been recorded in vivo in the neonatal rat from age P1 to P20 (Curthoys, 1983). Discharge rates were low at the youngest ages (40% UVH >60% UVH >80% UVH Overall

50% 64% 68% 77% 49%

73% 72% 71% 70%

Dizziness

35%

92%

258

Canal paresis

90%

53%

Guidetti, Monzani, & Civiero (2002)

273

Confirmed peripheral weakness

Initial visit

74%

Could not calculate

Iwasaki, Ito, Abbey, & Murofushi (2004)

132

Dizziness

Six months of recovery

66

Could not calculate

56%

71%

Totals

2219

17

117

UVH >20%

175

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Balance Function Assessment and Management

increasing peripheral vestibular system loss the sensitivity of the HSN test increases, there is no agreed on criterion of how much loss is needed to observe a positive head-shake test. When utilizing the head-shake as a screening tool for unilateral vestibular dysfunction, the presence of HSN is a good indicator that the patient should be referred for quantitative testing. The absence of HSN but a case history positive for dizziness would also warrant a referral for a complete balance function assessment. However, the head-shake test in isolation appears to be a poor predictor of low and moderate levels of vestibular hypofunction. The body of research (see Table 9–3) suggests that the head-shake test, therefore, should be used in conjunction with other bedside tests or formal balance function testing. A modification of the head-shake test (head-shaking tilt suppression) has been proposed by Zuma e Maia et al. to assist with differentiating UVH from central pathology (Zuma e Maia, Cal, D’Albora, Carmona, & Schubert, 2017). Tilting the head down after the head-shake test suppressed the induced angular slow phase velocity by more than 50% in individuals with peripheral vestibular lesions. Individuals with central vestibular lesions, however, had very little ability to suppress the HSN. In patients with UVH, tilting the head down suppresses the HSN via influence of the otolith organs. In patients with central pathology, there is impairment of the otolith mediation on the VS system. The VEDGE task force determined that the HSN test was Reasonable to Recommend at this time for patients with acute (zero to six weeks) and chronic (greater than six weeks) vestibular disorders (Scherer et al., 2014). The head-shake test was Reasonable to Recommend at this time for patients with peripheral or central dysfunction. The low sensitivity (22.5% reported by Vicini, Casani, and Ghilardi [1989]) precluded a higher recommendation for use in diagnosing central vestibular dysfunction. Considering the findings of the head-shake test in conjunction with those of the HIT might be helpful during the bedside assessment. The task force gave an Unable to Recommend at this time rating for use of the head-shake test in individuals with BPPV.

Dynamic Visual Acuity Test–(Non-Instrumented) Introduction Head movements may evoke dizziness or visual blurring in patients with either unilateral or bilateral

vestibular hypofunction. This perception of objects “bouncing” or “blurring” when the head is moving has been termed oscillopsia, meaning “oscillating vision” (Brickner, 1936). It can often be attributed to a defect in the VOR. One of the primary functions of the VOR is to keep the retina (fovea) stable on an object of interest when the head is moving. When the vestibular labyrinths sense head movement, they produce (by way of the VOR) equal and opposite compensatory eye movements that keep the eyes steady. This vestibular-driven reflexive process allows the observer to retain visual acuity with head movement and is known as dynamic visual acuity (DVA) (Miller & Ludvigh, 1962). The VOR is extremely precise and requires only a few degrees of error per second between the retina and the target to significantly degrade visual acuity and result in oscillopsia (Westheimer & McKee, 1975). Barber (1984) suggested that an examiner may be able to identify an underlying vestibular disorder if DVA was abnormal. The “oscillopsia test” was his initial description of a method to quantify the performance of a patient’s DVA. This very simple test permitted the quantification of a patient’s visual acuity with and without oscillation of the head. The premise was that if there was damage to the VOR, then a patient’s visual acuity would be poorer with head movement than without. Throughout the years there have been many variations on the original oscillopsia test, or as it is often termed, DVA test. For the purposes of this chapter it is referred to as DVA.

Technique It is suggested that commercially available computerized DVA systems greatly increase the sensitivity of the test to vestibular dysfunction (Herdman, Tusa, Blatt, Suzuki, Venuto, & Roberts, 1998). However, as these systems are not available in all settings, a standard protocol that can be performed in most clinics is described. The patient should perform the following test with best corrected vision (i.e., while wearing glasses or contacts). First, position an Early Treatment Diabetic Retinopathy Study (ETDRS) eye chart at a prescribed distance (typically 2.44 to 4 m). The threshold is defined as the lowest line read without error. Gently grasp the patient below the malar eminences and over the parietal region and oscillate the head at a frequency of 2 Hz and less than 20 degrees of arc displacement in the yaw plane (Figure 9–2). The direction of line reading should be alternated to control for memorization and the examiner must be careful not to pause when the direction of head rotation is changed.



9.  Bedside Assessment of the Vestibular System

A

B Figure 9–2.  A. An image illustrating correct hand placement for a patient being tested during the dynamic visual acuity test. B. View from the patient’s perspective while dynamic visual acuity is being assessed.

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Balance Function Assessment and Management

Results Normal Result A drop in best-corrected vision of no more than two lines from baseline acuity with head rotation is obtained. Abnormal Result A drop in best-corrected vision of three or more lines from baseline acuity with head rotation is obtained.

Mechanism When the head is moved, the orbit of the eye moves as well. The VOR provides a precisely calculated neural input to contract or relax the appropriate oculomotor muscles to adjust the eye in the orbit to retain the visual target of interest on the fovea so that clear vision can be maintained. Oscillation of the head left and right during the DVA test stimulates the lateral SCCs. The hair cells in the lateral SCCs provide information regarding rotational acceleration of the head in the yaw plane. When the head is turned toward the right in the yaw plane, there is an increase in neural firing rate in the vestibular nerves on the right side and a slow deviation of the eye in the opposite direction. Simultaneously, there is a corresponding decrease in firing rate in the afferent nerves on the left side. This asymmetry in firing rates between the corresponding lateral SCCs is proportionate to the acceleration of the head. The vestibular end organs transduce this acceleration into a neural code that the central vestibular system uses to adjust the oculomotor muscles and move the eye in the opposite direction of the head movement to retain the visual target on the fovea for clear vision. For the VOR to generate an appropriate compensatory eye movement, gain (the ratio of slow phase eye velocity to head velocity) and phase (the temporal difference of slow phase eye velocity to head velocity) must be accurate. When a vestibular end organ loses sensory cells, the frequency response of the peripheral system is reduced. Take, for example, the case where one vestibular end organ has been severely impaired and a large number of sensory hair cells in the lateral SCCs are damaged. With a quick head movement in the yaw plane, fewer sensory cells respond in the damaged ear than in a healthy ear for the same frequency. The leading ear will produce less neural activity, which is insufficient to drive the compensatory slow-phase eye velocity. This

would result in a head:eye movement ratio less than 1:1 and the eye would drift off target. This would result in the eye moving to some degree with the head instead of the normal compensatory eye deviation (via the VOR) away from the direction of rotation of the head. The ultimate result would be a reduction in visual acuity due to the slippage of the target from the fovea. This relationship between the VOR and DVA enables the clinician to make inferences regarding the status of the vestibular system. For head movements at frequencies above 2 Hz, or those that are associated with normal everyday movements, even a small amount of retinal slippage during head movement can be an indication of vestibular dysfunction. The effect of oscillopsia is most often encountered in patients with bilateral vestibular system hypofunction due to ototoxicity, bilateral end-organ disease (e.g., bilateral Ménière’s disease), or aging (Longridge & Mallinson, 1984). Patients with poorly compensated or severe UVH can also have impaired dynamic visual acuity.

Test Performance Results of investigations describing the ability of the DVA test to differentiate between normal individuals and those with vestibular disorders are mixed. When the complete body of literature describing the use of the DVA test to identify and quantify vestibular deficits is examined, it becomes apparent that there are many factors that can explain the differences in specificity and sensitivity found between studies. Several groups have described a positive relationship between peripheral vestibular dysfunction and DVA performance (Demer, Honrubia, & Baloh, 1994; Herdman et al., 1998; Longridge & Mallinson, 1984, 1987a, 1987b). In one of the first series of studies, Longridge and Mallinson (1984, 1987a, 1987b) described a customized eye chart called the dynamic illegible E (DIE) to assist in the detection of vestibular hypofunction. The authors designed a chart using only the “E” from the Snellen chart oriented in different directions. This was to control for the fact that some of the letters in the standard Snellen chart are more readily identifiable than others. Each orientation was referred to as an optotype. Using the DIE test procedure, the patient indicates the direction of the optotype in each column with the head still. This procedure was then repeated while the patient’s head was oscillated back and forth at a frequency of 1 Hz. The examiner recorded any change in visual acuity during the dynamic phase of the test.



Using the DIE test, Longridge and Mallinson (1984) reported the ability of the DVA test to screen for aminoglycoside vestibulotoxicity. A group of 8 subjects with documented aminoglycoside toxicity were selected to perform the DIE test. Six of these subjects were unable to identify any of the optotypes from the DIE test with head movement. One patient had normal caloric responses and was able to perform the DIE test with abnormal results, and one patient was unable to be tested due to osteomyelitis. Interestingly, when blood serum was monitored during therapy, none of this group had toxic levels. According to the authors, these results provided evidence that the DIE test was an appropriate screening tool for aminoglycoside vestibulotoxicity. Longridge and Mallinson (1987a, 1987b) provided further support for use of the clinical DVA test in the prediction of vestibular dysfunction. This investigation evaluated the relationship between DIE test performance and the magnitude of caloric reduction. The authors recruited 244 patients with abnormal caloric tests to undergo DIE testing. Multiple regression testing revealed a significant correlation between visual acuity during head movement and degree of caloric reduction. Specifically, the greater the degree of caloric reduction, the poorer the DIE test score. Demer et al. (1994) used a computerized paradigm to measure DVA performance. The authors compared a group of 13 normal subjects with 2 patients presenting with complete bilateral vestibular system weakness. The 2 subjects with vestibular dysfunction demonstrated reduced DVA performance compared with the normal group. The authors suggested that DVA testing during imposed head motion is a quantitative and clinically feasible measure of oscillopsia that reflects functionally significant abnormalities in the VOR. Herdman et al. (1998) presented data describing DVA performance in patients with bilateral and unilateral vestibular deficits using a computerized system. DVA test performance was found to be significantly different when scores obtained from patients with unilateral and bilateral vestibular loss were compared with those of their normal counterparts. Furthermore, in the UVH group, there was a significant difference in DVA performance for head movements toward the affected side, compared with the unaffected side. When the authors examined the sensitivity and specificity of the test for age-matched normal controls compared with the patient groups, the computerized DVA test was shown to have a sensitivity of 94.5% and specificity of 95.2%. However, evidence from other studies fails to support the reported relationship between DVA test per-

9.  Bedside Assessment of the Vestibular System

formance and vestibular dysfunction. Burgio, Blakely, and Myers (1992) found a poor relationship between vestibular dysfunction and DVA performance. This study evaluated 115 patients referred to a dizziness clinic and compared them with 17 control subjects. The experimental group consisted of 25 patients with unilateral caloric weakness (25% to 100%), 10 with a bilateral weakness (total slow phase velocity of 0 to 21 deg/s), and 80 with normal ENGs who had complaints of dizziness. The investigators found that the DVA test was highly specific (100%) but had poor sensitivity. Their results suggested that the DVA test did not detect vestibular loss or subjective dizziness in more than 50% of the cases with significant unilateral impairment. The inconsistency in findings among the various studies above is due to several factors. First, differences in methodology when performing the DVA test exist between the aforementioned studies. Computerized DVA testing systems require that the head move at or above a critical acceleration of the head prior to exposure to visual stimuli. This prevents the subject from reading the optotypes when the head is slowed to change direction. Herdman et al. (1998) employed such a system and reported high sensitivity for DVA testing. A second source of variability is the frequency of head movement during the test. The pursuit system has been shown to contribute to gaze stabilization at lower frequencies. Lee, Dumford, and Crowley (1997) assessed DVA performance from 27 normal patients using voluntary head rotation at frequencies ranging from 0.7 to 4 Hz. The authors found that there was a natural decrement in visual acuity with increasing frequency of horizontal head movement. The authors suggested that the ocular motor system becomes an ineffective system for ocular stabilization at frequencies above 2 Hz and that the VOR functions as the primary control system for visual stabilization during lower frequencies associated with ambulation. According to their results, to obtain an accurate measure of how well the VOR is compensating for head movement, the head should be oscillated no slower than 2 Hz. Many of the studies described previously were performed with head oscillations at frequencies below 2 Hz (Barber, 1984; Longridge & Mallinson, 1984, 1987a, 1987b). In patients with UVH, the ability to read the optotype is improved when oscillating the head toward the intact or better end organ. In paradigms where performance is not measured for each half-cycle, this may result in spuriously good DVA performance. This variable can be controlled by computerized DVA systems, where left and right head movement performance can

179

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be assessed separately, thereby increasing the sensitivity of the test to unilateral end organ dysfunction. A fourth source of interstudy variability is the method used to calculate the DVA score. The two common methods are the traditional Snellen distance 20/ XX system (i.e., 20/20, 20/100, etc.) and the LogMAR scale. Computerized DVA systems typically use the measurement parameter “logarithm of the minimum angle of resolution” or LogMAR. The LogMAR scale is a conversion method that transforms the geometric sequence of a traditional Snellen chart to a linear scale. The LogMar scale describes performance as visual acuity loss. Specifically, vision loss is represented by a positive score, whereas better visual acuity is represented by a negative score. Many of the earlier studies discussed above have described DVA performance by indicating how many lines of the Snellen chart visual acuity dropped with head movement. This interpretation of lines lost is only accurate when all steps between lines are equal, which is not the case in the Snellen chart. For this reason, use of an ETDRS eye chart is recommended. A fifth variable to consider in assessing the sensitivity of DVA is the degree of vestibular system compensation patients with UVH have attained. Herdman, Schubert, Das, and Tusa (2003) reported the effect of vestibular exercises on the recovery of DVA in patients with UVH. The sample consisted of 21 patients with UVH who were culled from an ambulatory referral center. Of this total, 13 of the patients performed vestibular exercises designed to increase VOR gain, whereas 8 of the patients performed placebo exercises. Subjects in the treatment group receiving vestibular exercises showed a significant improvement in DVA performance, whereas those performing the placebo exercises did not. In contrast, Longridge and Mallinson (1987a, 1987b) used the conventional DVA test to explore the relationship between DVA performance and central nervous system compensation. The factors of age, degree of caloric impairment, and time from onset of disease process were compared with scores from the DIE test. The investigators found no correlation between DIE test performance and central vestibular system compensation. The clinical utility of the DVA test appears to be influenced somewhat by technique and experience of the examiner. The non-instrumented DVA test using an ETDRS eye chart can be extremely useful in predicting severe vestibular dysfunction. Specifically, the clinical utility has been proven when the examiner suspects bilateral vestibular dysfunction from aminoglycoside vestibulotoxicity or a severe unilateral lesion (Burgio et al., 1992; Demer et al., 1994; Longridge & Mallinson,

1984). However, computerized DVA systems, although superior, are not always available in all balance clinics. They allow the examiner to document central nervous system compensation after rehabilitation, predict the side of the lesion in unilateral involvement, and grossly quantify the severity of bilateral vestibular hypofunction. As part of the National Institutes of Health Toolbox for the Assessment of Neurological and Behavioral Function, a computerized DVA test was developed that is valid, easy to administer, time- and cost-efficient (Rine et al., 2012, 2013). Regardless of the system used, it is important that whenever the results from the DVA test are abnormal, a full balance function workup should be recommended. When results are determined to be normal, the referral should be made based on a thorough case history. The VEDGE task force determined that the noninstrumented DVA test was Reasonable to Recommend at this time for patients with acute (zero to six weeks) and chronic (greater than six weeks) vestibular disorders (Scherer et al., 2014). Serial testing may be useful to gauge the degree of rehabilitation effectiveness (central compensation). The non-instrumented DVA test was Reasonable to Recommend at this time for patients with peripheral or central dysfunction, and may be useful during the bedside assessment to corroborate HIT and HSN findings.

Valsalva-Induced Nystagmus Introduction The self-induced change of middle ear and intracranial pressure commonly known as the Valsalva maneuver (VM) is capable of inducing eye movements in patients with craniocervical junction abnormalities and disorders affecting the inner ear. These anomalies may include Arnold–Chiari malformation, perilymphatic fistula, superior canal dehiscence, and other anomalies that involve the oval window, round window, saccule, or ossicles. The VM is named in honor of one of its early proponents, Antonio Mario Valsalva (1666– 1723), although documentation of the technique exists from the sixteenth century and earlier as a treatment for deafness and method for removing foreign bodies from the ear canal (Lustig & Jackler, 1999). Hennebert first described eye movements induced by changes in middle ear pressure in the early twentieth century. This phenomenon is now known as Hennebert’s sign and describes a conjugate eye movement away from the affected ear with positive pressure applied to the



external auditory meatus. A movement toward the affected ear is expected with applied negative pressure. The presence of such a movement allows the examiner to deduce the presence of an anomalous connection between the inner ear and the external environment (Goebel, 2001).

Technique Two variants of the VM should be performed by the patient: one designed to increase air pressure in the sinuses and middle ear, the other designed to increase venous pressure in the cranium. In both cases, the subject should wear Frenzel or VNG goggles to prevent VOR suppression and to permit the observation and documentation of eye movements (Zee & Fletcher, 1996). The patient also should be instructed to report any sensations of dizziness or vertigo induced by the test procedure, including blurred vision, oscillopsia, or diplopia (Brandt & Strupp, 2005). Eye movements should be observed during and immediately following pressurization and relaxation for both tests. The positive air pressure variant is performed by increasing barometric pressure in the sinuses, middle ear, and pharynx. Patients should be instructed to take a deep breath, pinch the nose, and close the mouth tightly, then blow as if equalizing the pressure of the ears when descending from altitude on an airplane. The patient should maintain the pressure for 10 to 15 s. The result is an increase in middle ear pressure (Walker & Zee, 2000). Following recovery from any elicited responses, the patient should strain against a closed glottis and lips for a similar duration, as if pressurizing the lungs to help stabilize the trunk while lifting a heavy weight. This variant serves to raise the intracranial pressure by inducing increases in central venous pressure (Walker & Zee, 2000). Either or both techniques may induce nystagmus in patients with the anomalies described above, and both should be included in the bedside test battery.

Results Normal Results Although Hennebert’s sign has been reported in normal subjects, the VM should not elicit sensations of dizziness or vertigo in the great majority of patients. The examiner, therefore, should be careful to distinguish between a shift of the eyes (positive Hennebert’s sign) and nystagmus. No elicited conjugate eye movements should be observed under Frenzel or VNG goggles.

9.  Bedside Assessment of the Vestibular System

Abnormal Results Increased middle ear or intracranial pressure as a result of either variant of the VM will elicit a conjugate movement of the eyes toward the contralesional ear in the cases of lateral and anterior canal involvement. If the patient maintains increased intracranial pressure, a corrective saccade toward the ipsilateral ear will be observed. Thus, nystagmus will “beat” toward the affected ear. The direction of the fast phase of nystagmus may provide information regarding the site of lesion. Horizontal nystagmus indicates involvement of the lateral semicircular canal and will beat toward the affected ear. Torsional and down-beating vertical nystagmus indicates a site of lesion in the anterior canal, whereas torsional and up-beating vertical nystagmus suggests involvement of the posterior canal (Davies, 2004). The direction of torsion provides information regarding the laterality of the lesion; the fast phase of the torsional nystagmus will beat in a clockwise direction for lesions of the left ear and a counterclockwise direction for lesions of the right ear.

Mechanism Increased pressure in the middle ear acts on abnormal connections between the labyrinth and the external environment to induce a pressure gradient within the cochlea. These abnormalities may exist as a hypermobility of the oval and round window membranes, defects of the bony structures surrounding the lateral aspect of the membranous labyrinth such as erosion due to cholesteatoma or chronic otitis media leading to dehiscence or fistula of the posterior or lateral canal, or defects of the floor of the middle cranial fossa leading to superior canal dehiscence (Brandt & Strupp, 2005; Goebel, 2001). The increased pressure within the affected labyrinth simulates movement of the head as it stimulates neural firing by displacing the cupula of the semicircular canal. The increased neural discharge rate drives the VOR such that a compensatory eye movement away from the affected ear is generated (Hennebert’s sign). In the case of straining against a closed glottis, increased pressure within the middle fossa is generated through changes in central venous pressure. Increasing and maintaining pressure within the thoracic cavity decreases venous return through the jugular vein, thereby raising intracranial pressure (Minor et al., 2001). An abnormal connection between the middle fossa and the vestibular labyrinth such as occurs in the case of superior canal dehiscence will induce a pressure

181

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change in the affected canal and elicit down-beating, torsional nystagmus beating toward the affected ear. Conversely, a dehiscence of the posterior canal will elicit up-beating and torsional nystagmus with the fast phase oriented toward the affected ear (Brantberg, Bagger-Sjoback, Mathiesen, Witt, & Pansell, 2006).

Test Performance A review of the literature suggests that the Valsalva test is useful in screening for the presence of canal dehiscence and perilymphatic fistula. The phenomenon, however, has also been reported in the presence of several other disorders, including cholesteatoma. Brantberg, Greitz, and Pansell (2004) reported a case of superior canal dehiscence where abnormal bone development in the middle cranial fossa was not the cause of the dehiscence. The patient exhibited pressureinduced vertigo despite the location of the dehiscence close to the common crus. Similarly, Tilikete, KrolakSalmon, Tuy, and Vighetto (2004) reported the case of a subject with bilateral superior canal dehiscence. In this case, both Valsalva-induced vertigo and Tullio’s sign could be elicited, with upward and counterclockwise torsional beating nystagmus. Halmagyi et al. (2003) described a patient who underwent three stapedectomy surgeries despite the audiometric finding of conductive hearing loss with preserved ipsilateral and contralateral acoustic reflexes, symptoms of superior canal dehiscence. The patient reported hypersensitivity to bone-conducted sounds (Tullio’s phenomenon) and exhibited a vestibular evoked myogenic potential (VEMP) at abnormally soft sound intensities and Valsalva-induced vertigo. Rambold, Heide, Sprenger, Haendler, and Helmchen (2001) reported the case of a patient who experienced VM-elicited contralateral horizontal nystagmus with the diagnosis of perilymphatic fistula. The patient also exhibited pulse synchronous oscillations of the eyes. Several studies have been conducted investigating the sensitivity of the Valsalva test. Reported sensitivity has varied. Hillman, Kertesz, Hadley, and Shelton (2006) reported vertigo evoked by VM in only 12 of 27 (44%) subjects with superior canal dehiscence. Of the 12 subjects, 8 could elicit nystagmus during Valsalva or simulated heavy lifting, corresponding to a sensitivity of 29%. Minor (2000) reported Valsalva-induced nystagmus in 10 of 17 subjects (i.e., a sensitivity of 58%) subsequently identified with superior canal dehiscence. In a later study the VM showed 82% sensitivity in a cohort of 28 patients previously diagnosed with supe-

rior canal dehiscence (Minor et al., 2001). Symptoms could be evoked in some of these patients by pressing on the tragus of the ear. The authors noted that nystagmus could continue for several beats after the release of pressure. Cremer, Minor, Carey, and Della Santina (2000) reported that 8 of 11 subjects with superior canal dehiscence exhibited nystagmus following VM (i.e., 73% sensitivity). Brantberg et al. (2001) reported that 8 of 8 (100%) subjects with superior canal dehiscence experienced pressure-induced vertigo. The subjects reported that the vertigo worsened during periods of upper respiratory infection. The presence of a positive Valsalva test, therefore, should be considered evidence of an abnormal connection between the middle ear and the inner ear, or the intracranial space and the middle ear.

Modified Clinical Test of Sensory Interaction on Balance Introduction There are three main systems that contribute to balance and postural control. We use our visual system to orient ourselves to things we know to be vertical in our world such as door frames, windows, corners of rooms, etc. We use input from the somatosensory system (information from joint receptions and Golgi tendon organs) to give us information about the support surface. Lastly, we use information from the vestibular system to gain awareness of spatial orientation relative to gravity. The Modified Clinical Test of Sensory Interaction on Balance (mCTSIB) is a bedside test of postural control under various sensory conditions. The mCTSIB is a modification of the Clinical Test of Sensory Interaction on Balance (CTSIB) that originally used six sensory conditions, including a visual conflict dome to introduce visual conflict (Cohen, Blatchly, & Gombash, 1993). The mCTSIB retains conditions 1 (eyes open, firm surface), 2 (eyes closed, firm surface), 4 (eyes open, foam surface), and 5 (eyes closed, foam surface) from the original CTSIB (Figure 9–3). This test gives the examiner insight into an individual’s ability to maintain postural control during four different sensory conditions. It cannot be used to diagnose a vestibular disorder; however, in the last condition with vision removed (eyes closed) and inaccurate somatosensory input (foam surface), the only system giving accurate sensory input is the vestibular system. Individuals with impairments in vestibular function tend to have difficulty with the eyes closed,



9.  Bedside Assessment of the Vestibular System

A

B

C

D

Figure 9–3.  A. Condition 1— Eyes open on a firm surface B. Condition 2 — Eyes closed on a firm surface C. Condition 3 — Eye open on a foam surface D. Condition 4 — Eyes closed on a foam surface.

foam surface condition. However, it must be noted that there are many other reasons that an individual may experience difficulty in that, or any of the other, condi-

tions. If an individual has deficits of postural control during any of the mCTSIB conditions, a more in-depth balance assessment is warranted.

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Technique Patients are asked to stand with their arms at their sides in the following four test conditions: (1) firm surface with eyes open, (2) firm surface with eyes closed, (3) compliant surface (foam) with eyes open, and (4) compliant surface (foam) with eyes closed. The foam should be of sufficient density and thickness to support the individual’s bodyweight. Each position is timed for 30 s. If patients are unable to maintain the position for 30 s, they are provided two additional attempts, and the times for the three trials are averaged. The position of the feet (feet together versus feet apart) and footwear do not influence the scores (Whitney & Wrisley, 2004; Wrisley & Whitney, 2004). A total score is calculated by adding the times (or average times if more than one trial is required) for the four test positions together.

Results Normal Results Normative data for the CTSIB has been published in 69 healthy adults aged 20 to 70 years (El-Kashlan, Shepard, Asher, Smith-Wheelock, & Telian, 1998). Cohen et al. (1993) also presented data for a group of neurologically asymptomatic adults for the CTSIB. While a maximum score on the CTSIB is 180 (30 s for each of six test conditions), only four of the test conditions are performed for the mCTSIB. Normal subjects should be able to maintain the four test positions for approximately 30 seconds, with a score close to 120. Abnormal Results An inability to maintain the four test positions for approximately 30 seconds is considered to be abnormal.

Mechanism The medial and lateral vestibulospinal and reticulospinal tracts are important components of the vestibular contribution to postural control. The medial vestibulospinal tract originates in the medial vestibular nucleus and contributes fibers to the medial longitudinal fasciculus. The lateral vestibulospinal tract originates in the lateral vestibular nucleus and carries vestibular and cerebellar information to the lower motor neurons. The lateral vestibular nucleus receives afferent information from the eighth nerve, as well as efferent information from the vermis and fastigial nuclei in the cerebellum. Descending projections from the fastigial nuclei

to the vestibular nuclei and reticular formation influence axial and proximal motor control (Zhang, Wang, & Zhu, 2016). The reticulospinal tract originates from the reticular formation and influences muscle tone. It also facilitates or inhibits volitional movement (pyramidal system) and myotatic reflexes. Myotatic reflexes contribute to postural control by maintaining joint stiffness. Volitional movement contributes to postural control through the execution of learned, purposeful movements. These purposeful movements can prevent or counteract a loss of balance.

Test Performance The mCTSIB is correlated with condition 2 (firm surface with eyes closed; r = 0.48), condition 4 (swayreferenced surface with eyes open; r = 0.30), and condition 5 (sway-referenced surface with eyes closed; r = 0.51) on the Sensory Organization Test (SOT) (Wrisley & Whitney, 2004). Weber and Cass (1993) found that the mCTSIB condition 4 (standing on a compliant surface [foam] with eyes closed) had a sensitivity of 95% and a specificity of 90% in comparison to the SOT in patients with complaints of dizziness and imbalance. Individuals with posterior canal BPPV demonstrated greater sway velocity when standing on foam with eyes open or eyes closed during the instrumented mCTSIB (Zhou et al., 2015). No postural deficits were observed in individuals with horizontal canal BPPV compared with healthy controls (Zhou et al., 2015). In patients with unilateral vestibulopathy, correlations between the conditions on the CTSIB and the SOT composite score ranged from −0.23 to −0.65 (Park et al., 2013). Park et al. (2013) found the resulting sensitivity was 42% and the specificity was 68% for the mCTSIB to correctly identify individuals with unilateral vestibulopathy from healthy controls. The VEDGE task force determined that the mCTSIB was Reasonable to Recommend at this time for patients with acute (zero to six weeks) and chronic (greater than six weeks) vestibular disorders. The mCTSIB was Reasonable to Recommend at this time for patients with peripheral or central dysfunction and in individuals with BPPV.

Summary The results of bedside tests of vestibular function such as those described in this chapter are commonly considered to be well-established criteria for the appropri-



9.  Bedside Assessment of the Vestibular System

ate referral of patients for diagnostic testing. However, a review of published literature regarding the tests in question do have conflicting results. Rather, the tests may be most appropriately used as a screening to alert the examiner that additional testing is warranted or to inform the examiner of specific functional impairments experienced by the patient. Although the tests reviewed in this chapter tend to exhibit high specificity, their attendant low sensitivity renders them relatively unsuitable for diagnostic purposes in clinical use. As such, these informal assessment tools should not be considered to be substitutes for electrophysiologic testing, imaging studies, or other diagnostic testing. If bedside tests are included in the screening and referral process, new or improved versions and combinations of the tests must be developed, investigated, and proven by clinician scientists. Without such developments, it is likely that reliance on bedside tests of vestibular function may lead to missed diagnoses or inappropriate referrals for testing and follow-up care.

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Wilson, W. R., & Kim, J. W. (1981). Study of ventilation testing with electronystagmography. Annals of Otology Rhinology and Laryngology, 90(1 Pt. 1), 56–59. Wrisley, D., & Whitney, S. (2004). The effect of foot position on the modified clinical test of sensory interaction and balance. Archives of Physical Medicine and Rehabilitation, 85(2), 335–338. Zee, D. S., & Fletcher, W. A. (1996). Bedside examination. In R. W. Baloh & C. M. Halmagyi (Eds.), Disorders of the vestibular system (pp. 178–190). New York, NY: Oxford University Press. Zhang, X.-Y., Wang, J.-J., & Zhu, J.-N. (2016). Cerebellar fastigial nucleus: From anatomic construction to physiological functions. Cerebellum & Ataxias, 3(1), 1–10. Zhou, R., Liu, B., Zhang, S., Liu, D., Liu, J., Leng, Y., & Kong, W. (2015). The balance function of the patients with benign paroxysmal positional vertigo during standing. Journal of Clinical Otorhinolaryngology, Head, and Neck Surgery, 29(22), 1966–1969. Zuma e Maia, F. C., Cal, R., D’Albora, R., Carmona, S., & Schubert, M. C. (2017). Head-shaking tilt suppression: A clinical test to discern central from peripheral causes of vertigo. Journal of Neurology, 264(6), 1264–1270.

10 Eye Movement Recording and Ocular Motility Testing Neil T. Shepard, Michael C. Schubert, and Scott D. Z. Eggers

Introduction Provided is a discussion of the technical aspects of eye movement recording techniques, the routine clinical evaluation of the ocular motor systems involved with gaze stability, saccade production, smooth pursuit tracking, and the optokinetic system. In addition are the interpretations for each of these tests and how they can be used in routine clinical investigations of the dizzy patient, principally for the purpose of site-oflesion determination. To better understand the interpretation of these tests and how they can be used to localize lesions to the central nervous system (CNS), the reader is referred to Chapter 3 and other sources (Leigh & Zee, 2006) for a review of the neurologic pathways involved in each of the ocular motor tasks listed above. In a review of that nature, you find overlaps in the neural pathways especially between gaze stability to an eccentric target and saccade production, gaze stability to a primary target and smooth pursuit, smooth pursuit and optokinetic activity. Therefore, although the tests for ocular motor functioning can be used to indicate CNS involvement and, in some cases, suggest differential lesions within the CNS, specific site-of-lesion determination clearly is not always possible. In many cases, both brainstem and cerebellar structures may be implicated, and further differentiation with physiologic testing alone is not possible with routine clinical techniques. There are, however, other combinations of results that are highly suggestive of specific regions of the brainstem or cerebellum involved in abnormal ocular motor control.

Using specific patient examples of abnormal eye movements, the following discussion attempts to delineate the global CNS indicators from those with more specific site-of-lesion implications. But first we need to discuss briefly the task of recording eye movement.

Eye Movement Recording Techniques The measurement of the vestibulo-ocular reflex (VOR) and ocular motility requires the use of sophisticated methods to transform the movements of the eyes into signals that can be digitized, processed, and analyzed. There are at least three methods for accomplishing this. The methods include electro-oculography (EOG) (electronystagmography [ENG]), infrared videonystagmography (VNG) (i.e., video-oculography [VOG]) techniques and scleral search coil techniques. In this chapter we will constrain the discussion of eye movement recording techniques to those used in contemporary vestibular system assessment clinics. Those techniques include ENG and VNG.

Electro-Oculography/ Electronystagmography Origin of the Corneoretinal Potential and Electrode Use The electrical transducer of the visual system is the retina, which also serves as the source of the corneoretinal

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potential (CRP). The CRP is a bioelectrical signal that is measured during EOG, which is the recording technique used in ENG. The eyeball has a dipolar orientation like a “battery,” with the cornea being positively polarized and the retina negatively polarized. This standing potential is propagated through the eye by volume conduction, where it is capable of being recorded with conventional surface electrodes. As the cornea is positively charged and the retina is negatively charged, two electrodes placed at the outer canthus of each eye and routed into a differential amplifier should “see” neither a positive nor a negative charge with the eyes in primary position (Figure 10–1A). If the eyes move conjugately to the right, the electrode at the right outer canthus should record a positive charge (i.e., as the positive pole of the right eye is pointed toward it) and the electrode at the left outer canthus should record a less positive charge (i.e., as less of that cornea is pointing toward that electrode) (Figure 10–1B). A leftward conjugate eye movement of similar magnitude results in the left electrode recording positive charge and the right electrode with a less positive charge (Figure 10–1C). The convention in EOG recordings is for upward trace deflections to represent rightward and upward eye deviations, and for downward trace deflections to represent leftward or downward eye deviations.

A

B

Assuming the examiner observes a full, conjugate range of movement of the eyes during informal testing, most clinicians record EOG using a “bitemporal” electrode array (Figure 10–2). It must be stated that for bitemporal recordings, electrical activity for the two eyes is “averaged.” This means that disconjugate movements of the eyes will be missed and underscores the importance for the clinician to examine informally the movements of the eyes to detect gross or subtle ocular motility disorders such as disconjugate eye movements before electrodes are placed on the face or goggles are placed over the eyes. An alternative to the bitemporal electrode placement is the monocular technique (Figure 10–3). The monocular recording technique permits the recording of eye position for each eye separately. The electrode pairs are routed to a differential amplifier that literally subtracts the electrical signal recorded by the inverting electrode input from the electrical signal recorded by the non-inverting electrode input (see Figures 10–2A through 10–2E). In doing this, electrical activity that is unrelated to the CRP (i.e., unwanted electrical interference) that is common to both the inverting and non-inverting electrodes (e.g., stray 60-Hz electrical signals, EKG interference) will be subtracted out (and eliminated), a technique referred to as common mode rejection (CMR). This should result in a reduction in the noisiness of the EOG recordings.

C

Figure 10–1. The corneoretinal potential (CRP). The cornea is positively charged and the retinal is negatively charged. A. When the eye is in midline position a pair of electrodes placed on either side of the eye will see neither a positive nor a negative voltage. B. When the eye turns to the right, a positive electrical potential is generated. C. When the eye turns to the left, a negative electrical potential is generated.

A

B

C Figure 10–2.  Bitemporal electrode montage and the connections to a two-channel differential amplifier (i.e., two channels permit the recording of horizontal and vertical eye deviations). A. The horizontal and vertical amplifier outputs to a printer when the eyes are at primary (central) gaze (i.e., there is no pen deflection). B. The horizontal and vertical amplifier outputs to a printer for a rightward eye deviation. Notice that a rightward eye movement results in an upward pen deflection in the horizontal channel (a leftward eye deviation would result in a downward pen deflection). C. The horizontal and vertical amplifier outputs to a printer for an upward eye deviation. Notice that an upward eye deviation results in an upward pen deflection in the vertical channel (a downward eye movement would result in a downward pen deflection).  continues

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D

E Figure 10–2.  continued   D. The horizontal and vertical amplifier outputs to a printer for an oblique eye deviation (i.e., an up/right eye movement). Notice that the eye movement is represented by deflections in both the horizontal and vertical channels. E. The horizontal and vertical amplifier outputs to a printer for a torsional eye movement. Notice that as the eye is rotating about its anterior/posterior axis there is neither a deviation in the horizontal nor in the vertical channels. This figure was adapted from An Introduction to ENG, by C. W. Stockwell, 2004. Schaumburg, IL: GN Otometrics.

The electrical signals resulting from conjugate horizontal eye deviations are approximately 20 µV per 1 degree of eye deviation in normal subjects with normal retinal function. These eye signals must be amplified by a factor of approximately 10,000 for the eye signals to be within an amplitude range that can be digitized and processed by most computerized data acquisition and processing systems. It should be noted as shown in Figure 10–2E, torsional movements of the eye without distinct horizontal or vertical movements result in tracings without any deviation, since there is no movement of the dipole laterally or vertically. Figures 10–1 through 10–3 are shown with a strip chart recorder and pins for illustration. Currently, most systems on the market illustrate the traces on to a computer monitor screen.

Infrared Video Recording Techniques Although scleral search coils are still considered the gold standard for eye movement recordings, infrared video tracking systems have rapidly become the stateof-the-art technique for recording eye movements. A method for creating a vision-denied condition is the final component of the hardware. Video tracking systems make use of pupil localization technology and the reflective properties of the corneal surface to calculate pupil position and angle of gaze. Implementation of the system varies between manufacturers, but most make use of a goggle-type headpiece to illuminate the eyes that contains infrared diodes, dichroic glass “mirrors” that reflect the image of the eyes into a single camera or a pair of cameras that record the image of the eye.



10.  Eye Movement Recording and Ocular Motility Testing

Figure 10–3.  Electrode locations and four-channel amplifier connections for a monocular montage.

A headband holds the assembly over the eyes (Figures 10–4 and 10–5). This setup fixes the camera in place relative to the head, ensuring that changes in observed pupil position are caused solely by eye movements rather than a combination of head and eye movements. The use of the dichroic glass allows the patient to follow the visual targets during ocular motility testing) but will reflect the eye image(s) into the left and right eye cameras. Last, there are controls on the goggles that permit the image of the eye to be raised, lowered, converged, diverged, or focused.

Technique and Interpretations of Ocular Motility Testing In the evaluation of the dizzy patient, the eyes provide the most direct access to the evaluation of the peripheral vestibular system. However, the pathways from the labyrinthine structures involve significant neurologic substrate in the brainstem and cerebellum with controlling influence from higher centers in the midbrain and cerebral cortex. Therefore, correct interpretation of eye movements relative to the periphery rely on normal function of the central pathways. Also, symptoms of dizziness can result from lesions in the central

Figure 10–4. Model wearing a monocular, video eye movement recording system.The lens reflects the left eye image into a head-mounted video camera.

neural pathways or at the central nuclei. Secondary to these issues, it becomes important to use the eyes as our window into the CNS-controlling structures for eye

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Figure 10–5. Illustrated is the use of a set of binocular infrared video goggle system..

movements that function independently of the peripheral vestibular system. As one approaches the assessment of the ocular motor system functioning independently of the peripheral vestibular system (during head still examinations), four principal ocular control events are evaluated. These include the following: 1. Saccade testing — This is the ability to move the eyes in a rapid single movement to refixate a target of interest onto the fovea (the most sensitive part of the retina) for clear viewing. 2. Smooth pursuit tracking — This is the ability to track the movement of a target of interest maintaining the image on the fovea with smooth continuous eye movements, as opposed to tracking with the use of repeated saccades. 3. Gaze stability — This refers to the ability to maintain gaze stable without the generation of other eye movements (principally jerk nystagmus) while looking straight ahead (primary), left, right, up, and down. 4. Optokinetic nystagmus — This is the development of reflexive eye movements in the form of jerk nystagmus during the visualization of moving objects that fill 80% to 90% or greater of the visual field of view. Ostensibly, the purpose for the generation of the nystagmus is to assist clear visual viewing

when the head is in constant velocity motion, or the head is still and objects of interest are moving in a regular manner, or both are moving at constant velocities that are not equal, in which case the the vestibulo-ocular reflex is normally inhibited in order to maintain a clear visual view by preventing the eyes from counter-rotating off the visual scene.

Saccade Testing Technical Considerations To assess saccadic eye movement, targets need to be presented that require sudden rapid movements of the eyes. In the past, this has been accomplished with the use of fixed targets placed on a wall or screen such that when the patient was seated at a particular distance from the target plane, eye movements to each target from the center would require a 10- to 15-degree subtended arc movement of the eyes. This task was used for calibration of the system and for a cursory evaluation of volitional saccades. With the use of computerized systems, targets can now be presented via light bars or through video projection systems. More importantly, the task can be either that of presenting fixed position targets or targets that appear randomly in different positions in the horizontal or vertical planes. Also, it is



10.  Eye Movement Recording and Ocular Motility Testing

possible to present the targets at random time intervals together with the random location. Although fixed target location and timing are used for certain paradigms, producing volitional saccades (predictable targets), the use of random saccade testing is preferable in the overall evaluation to elicit reflexive saccades (ability to react when a target of interest suddenly appears at a new location). Targets fixed or random are usually presented within a ±30-degree range of subtended arc movement of the eye. Saccade testing, specifically the use of a broad bandpass filter of 10 to 100 Hz and a sampling rate of a minimum of 60 Hz with 100 Hz or higher, is now advised by the American National Standards Institute for ENG/VNG (ANSI, 2009). It is also with this task that individual eye evaluation is the preferred technique. This is secondary to the

need to recognize disorders involved with disconjugate eye movements such as intranuclear ophthalmoplegia (see case examples below). If using EOG for this task, additional electrodes may need to be placed near the medial canthus of each eye paired with those at the lateral canthus to obtain individual horizontal eye movements (refer to Figure 10–3 above). Parameters for Saccade Testing Analysis Refer to the bottom two panels of Figure 10–6 as each of the analysis parameters are defined: n Velocity — the plot on the left presents the

“main sequence plot.” This is a plot of the peak velocity of the eye movement during

Figure 10–6. Results of a normal random saccade test via individual eye video recordings on a 49-year-old female diagnosed with unilateral vestibular hypofunction secondary to vestibular neuronitis. The top two panels provide a sample of the traces showing the target in the dark line and the left and right recorded eye movements in the lighter line. The left eye is in the top panel with the right eye in the second panel. The third and fourth panels give the quantitative analysis for the saccade test. Each dot represents the analysis of a single saccade out of the total of 30 presented for the test. From the left to the right in both the third and fourth panels the plots are for velocity (main sequence plot), accuracy, and latency all as a function of the excursions of the eyes. The left eye analysis is in panel three with the right eye analysis in the fourth panel.

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the trajectory from the initial point of regard to the new eye location. Note that if the sampling rate is less than 100 Hz, the plot is more representative of the average velocity, not truly peak velocity. The eye velocities are plotted as a function of the excursion distance of the eye in degrees of subtended arc movement, not the movement of the target. n Accuracy — the center plot gives the percentage of the distance the eye moved in its first single movement relative to that of the target as a function of eye movement excursion. One hundred percent indicates that the eye moved the same distance as the target in a single major excursion. Values over 100% indicate an overshoot, whereas those under 100% show an undershoot. n Latency — the final plot to the right reflects the lapsed time in milliseconds from the initiation of the target movement to the initiation of the eye movement, again as a function of eye movement excursion. In each of the plots, the abnormal region is defined as two standard deviations below the mean in the main sequence plot, two standard deviations above and below the mean in the accuracy plot, and two standard deviations above the mean in the latency plot and shown by the stippled region. These plots are typically analyzed such that if 50% of the saccades sampled for any of the three parameters are within the normal range, the saccade test is considered normal. Agerelated normative data are not needed for routine clinical analysis of saccade testing by either fixed, random, or remembered paradigms (Hain, 1993; Leigh & Zee, 2006; Shepard & Telian, 1996). A sample of normative data for individual eye recordings (electro-oculography techniques) from 46 subjects of age 19 to 49, 15 of age 50 to 69, 8 from 70 to 79, and 7 from 80 to 88 is shown in Figure 10–7. In the figure the population responses with means and two standard deviation ranges are given for all three parameters discussed above. In the main sequence plot in Figure 10–7, abduction velocities are lower than adduction velocities. This is a finding that has been reported previously (Boghen, Troost, Daroff, Dell’Osso, & Birkett, 1974) again by the use of EOG recording techniques. In this work it was determined that a consistent relationship between the peak velocity and the size of the excursion of the saccade was present — the larger the excursion of the saccade, the higher the peak velocity up to about 500 degrees/

second. It was also demonstrated that the duration of the saccade also lengthened with the increase in excursion up to about 100 ms. This duration is shorter than that needed to obtain visual feedback, implying that adjustments in the speed of the saccade and the final destination of the eye movement cannot be adjusted while the saccadic eye movement is in progress. Comparisons with other eye movement recording techniques suggest that this may be unique to the use of EOG techniques, as use of scleral search coils and infrared reflections show the opposite (Leigh & Zee, 2006). In a direct comparison between VOG and search coils for saccade, smooth pursuit, and optokinetic nystagmus in both an artificial and human eye during roll plane rotation, the mean differences between the VOG and the search coil were 0.56, 0.78, and 0.18 degrees of rotation for the roll, pitch, and yaw (horizontal) planes, respectively (Imai et al., 2005). The implication from this is that normative data for saccade testing need to be those developed from the video recordings, but if EOG techniques are used, then the normative ranges for comparison should be those developed with the EOG technique. It has not been demonstrated, irrespective of the recording technique, that age-related normative ranges are needed for the clinical study of saccades.

Interpretation of Saccade Testing There are several protocols for testing saccadic activity. These are all well documented in the literature for ENG or VNG applications (Jacobson, Newman, & Kartush, 1993; Leigh & Zee, 2006; Shepard & Telian, 1996). Therefore, we concentrate our interpretation discussion on what has become the most common protocol used for routine clinical evaluation of saccadic eye movements, the random saccade paradigm. Recognize that, in general, the interpretation of a fixed saccade paradigm will be like that detailed below for the random saccade paradigm. As indicated above, the parameters used for analysis of a saccadic eye movement are the latency to onset after the presentation of a target at a new location, the accuracy with which that movement is made, and the peak velocity of the eye during the movement. The combined use of these three allows for possible suggestions of localization of involvement within the CNS based on the neurologic substrate responsible for the performance aspects of each of the three outcome parameters. Saccade testing abnormalities do not occur as a result of peripheral vestibular system lesions but



10.  Eye Movement Recording and Ocular Motility Testing

A Figure 10–7.  A. Shown are the individual eye data for a random saccade paradigm for the left eye of the 76 subjects with age distributions as given in the text. The graph on the top left gives latency to onset of saccade eye movements, the top right plots percent accuracy, and the bottom graph shows the peak velocity all as a function of the excursion of the eye.  continues

reflect CNS lesion sites (Tables 10–1 to 10–3). A detailed discussion of the current state of knowledge of the neural pathways responsible for saccade production is provided by Leigh and Zee (2006); only a brief summary of the salient aspects of that information is presented below. The neural substrate information is then used to develop the interpretation suggestions given for abnormalities related to saccade velocity, accuracy, and laten-

cies or combinations of these parameters in Tables 10–1, 10–2, and 10–3, respectively. For a horizontal or vertical reflexive saccade via the random saccade paradigm, the initiation of the movement results from the presentation of a target of interest in a new location. The horizontal reflexive eye movement that brings gaze to the new target is primarily engendered by excitatory burst neurons (EBNs) in

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B Figure 10–7.  continued  B. The right eye results for latency, accuracy, and velocity are given in the same orientation as in part A. From Practical Management of the Balance Disorder Patient, by Shepard, N. T., and Telian, S. A., 1996, pp. 100–103. Used with permission.

the paramedian pontine reticular formation (PPRF) in the caudal pons (van Gisbergen, Robinson, & Gielen, 1981). For vertical and torsional saccades, the excitatory burst neurons are part of the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF) in the rostral mesencephalon (King & Fuchs, 1979; Vilis, Hepp, Schwarz, & Henn, 1989). These premotor neurons initiate bursts of activity approximately 12 ms prior to the actual initiation of the eye movement. However, while the premotor neurons connect with cranial nerve nuclei

III and VI, the neural circuit also involves activity from inhibitory and omnipause neurons in the brainstem and midbrain areas in a complex network allowing for the activity of the EBN to initiate eye movements (see Chapter 3 in this text for a more detailed discussion) with velocities proportional to the neural firing rate (Leigh & Zee, 2006). There is a growing body of evidence that for both horizontal and vertical voluntary saccades, areas other than simply frontal eye fields of the frontal lobe and brainstem and midbrain circuits are



10.  Eye Movement Recording and Ocular Motility Testing

Table 10–1.  Abnormalities of Saccade Velocity • Slowing both eyes, all directions with full ocular range-of-motion Fatigue, medications, drowsiness PPRF for horizontal movements and RIMLF for vertical Cerebral hemispheres, superior colliculus, cerebellum Early in myasthenia gravis especially with repeated activity — glissades, initial fast movement and slowing as the target is approached (Leigh & Zee, 2006) • Slowing either eye, restricted directions For horizontal PPRF For vertical RIMLF For horizontal on adduction only (monocular or binocular) — MLF lesion on the side of the slowing (INO)

Table 10–2.  Abnormalities of Accuracy • Hypometria (undershoot) Fatigue, medications, drowsiness Bilateral — cerebellar dorsal vermis (Leigh & Zee, 2006) Unilateral — ipsilateral cerebellar/brainstem Visual acuity or visual field cuts Myasthenia gravis for large saccades Brainstem burst neuron providing too short of a burst Cerebral hemispheric — contralateral to the lesion more likely if the patient demonstrates neglect (Meienberg, Harrer, & Wehren, 1986) • Hypermetria (overshoot) Cerebellar Bilateral — cerebellar fastigial nucleus (Leigh & Zee, 2006)

Cranial nerves III, IV, VI, or muscle palsy • Abnormally fast Later in myasthenia gravis of ocular type (Leigh & Zee, 2006)

Table 10–3. Abnormalities of Latency • Both eyes in all directions

Calibration errors

Fatigue, medication, drowsiness

Restriction syndromes (see text for explanation)

Frontal eye fields, but likely for remembered or antisaccade tasks as opposed to reflexive random saccade paradigm

involved. These include the superior colliculus, cerebellum, various regions of the frontal lobe, the posterior parietal cortex, basal ganglia, and thalamus. A synthesis of this literature is provided by Leigh and Zee (2006). Primary control over the velocity of the saccadic movement is engendered by the PPRF in the pons. Yet not all saccadic slowing disorders are from the pons region of the brainstem. A useful generality is that global slowing (both eyes in both directions with full ocular range of motion) could involve either the PPRF or the riMLF (see Chapter 3 for complete discussion), yet higher centers such as the superior colliculus and cerebral hemispheres need to be considered. If the slowing is restricted to involve only one eye or a single direction, then slowing of abduction is most likely a sixth nerve palsy with monocular slowing of adduction, which would be most likely internuclear ophthalmoplegia (INO) with an ipsilateral medial longitudinal fasciculus (MLF) lesion (see Chapter 3 for a full discussion of the effects of lesions in these areas). See Table 10–1 for other considerations. In the performance of saccade testing, more so than during other portions of the ENG/VNG, individ-

Visual deficits — severe reductions in acuity, amblyopia (Ciuffreda, Kenyon, & Stark, 1978) • Both eyes for fixed saccade paradigms — learned or commanded tasks Basal ganglia as in Parkinson’s and other disorders of motor initiation where target location and timing of movement is regular (Lasker & Zee, 1997; Lasker, Zee, & Hain, 1987) • Abnormally short latency Highly unusual — most likely patient anticipating target movement, needs reinstruction • Superior colliculus and pathways to reticular formation in the brainstem (Leigh & Zee, 2006)

ual eye recordings should be made if at all possible. It is during saccade testing that disconjugate eye movements are accentuated. The hallmark eye movement disorder causing disconjugate movement is that of INO. In this disorder the adducting (moving toward the midline) eye is abnormally slow. Recognition of the condition immediately implies a lesion in the MLF on

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the side of the eye with the adduction slowing (Leigh & Zee, 2006). Additionally, when INO is bilateral, there is a presumptive diagnosis of multiple sclerosis until proven otherwise. Video 10–1 shows the eye movements of a 44-year-old male with multiple sclerosis. The eye movements were captured during VNG sac-

cade testing and illustrate bilateral INO. Figure 10–8 shows the recorded analysis for the eye movement in Video 10–1. Video 10–2 shows the eye movements of a 30-year-old male during random saccade testing, with Figure 10–9 illustrating the recorded analysis for Video 10–2. In this example, the eye movements and

Figure 10–8.  The recorded eye movement from individual eye recordings for the 44-year-old male in Video 10–1 who was subsequently diagnosed with multiple sclerosis. The column of results on the left is for the right eye with the right column representing the left eye. The top two panels indicate peak velocity; the middle two show accuracy, and the bottom two are for latency all as a function of the excursion of the eyes. The larger light color dots represent average performance for the parameter at the specific excursion with the small black dots the performance for individual saccades. The velocity panels clearly show, as seen in the video, slowing of each eye on adduction indicating bilateral INO. Additionally, abnormal slowing is noted for both eyes dominantly on movements to the right. note that analysis is done based on needing 50% of the individual saccades to be outside the normal range for a particular aspect of the study to be considered abnormal.

Figure 10–9. Saccade performance from the 30-year-old male in Video 10–2 demonstrating left-side INO and subsequently diagnosed with a left-side brainstem stroke. See legend for Figure 10–8 for details of the figure layout. Additionally, the top two panels show samples of the raw eye movement for five saccades. The lighter trace is the actual eye movements with the black trace the target movement. Right eye represented on the left and left eye on the right. In the velocity plot for the left eye significant slowing is noted for adduction. 201

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analysis are consistent with left-side unilateral INO. The patient was shown to have had an ischemic stroke on the left involving the left MLF pathway. Abnormally fast saccades typically occur as a result of the saccade being prematurely halted before reaching the target (restriction syndrome) (Leigh & Zee, 2006). This can occur as a result of disease process that reduces the range of motion of an eye (such as myasthenia gravis) or a mechanical restriction in range of motion (such as trauma or a mass lesion), making the saccade too fast for its actual recorded amplitude, though likely normal velocity for its larger intended amplitude (Leigh & Zee, 2006). During ENG or VNG testing, inaccurate calibration needs to be ruled out as a cause for apparent abnormally fast saccade performance. The cerebellum, specifically the dorsal vermis and fastigial nucleus regions, are major contributors to the accuracy with which saccades are performed (Leigh & Zee, 2006). Yet although overshoot dysmetria (hypermetria) is considered a strong indication of cerebellar involvement, the possibilities for involvement in the presences of hypometric (undershoot dysmetria) saccades are considerably broader (Leigh & Zee, 2006). Patients with severe visual acuity deficits, especially macular degeneration, may perform the saccades to targets by using multiple smaller saccades, because during a random saccade task the target direction is clear but placing the target on the fovea becomes difficult. Patients with visual field cuts that involve a full or partial hemisphere (hemianopia) will produce hypometric saccades. Here also combinations of brainstem and cerebellar lesion may result in mild to severe undershooting of the target (Leigh & Zee, 2006). Another aspect of saccade accuracy is related to the mentioned ocular lateralpulsion introduced in the section on gaze testing (a full discussion of the anatomy and examination findings is given in Chapter 3). This directional bias of saccades is most commonly ipsipulsion, with hypermetric saccades (overshoot) to the lesion side and hypometric saccades to the contralateral side (undershoot). The last attribute of a saccade is the length of time to initiation of the eye movement (latency) once a target of interest appears or a command is given to gaze at an already existing target within the visual field. Lesions in the PPRF or riMLF involving the burst neurons could cause delays in the initiation of the eye movement horizontally or vertically but this would represent an unusual situation. The process to initiate the burst neuron activity involves multiple other central areas that could result in delayed onset of burst neuron activity and ultimately in an increase in latency for the desired saccade. The involvement may be from visual acuity

problems, and amblyopia (Ciuffreda, Kenyon, & Stark, 1978) to visual eye fields in the frontal cortex (Leigh & Zee, 2006). Likely more with latency than either velocity or accuracy, the state of the patient regarding medication, drowsiness, and attention highly influences the results. It is with latency more so than with velocity or accuracy that the paradigm differences between fixed (volitional or commanded) saccades and the random paradigm reflexive saccades are seen. Basal ganglia involvement can cause increased latencies to fixed saccades yet show normal initiation timing with random saccades (Leigh & Zee, 2006). Once drugs, inattention, drowsiness, fatigue, and impaired visual acuity are ruled out, then any abnormality with saccade performance must be considered as a potential indicator of CNS or peripheral ocular motor involvement. It would not be reasonable to consider peripheral vestibular system involvement as a possible source for disruptions in any of the saccade parameters discussed above. When performing an antisaccade paradigm, the primary means for analysis during an ENG or VNG is percent error. This would be a ratio of the number of saccadic eye movements that were made in the direction of the target movement to the number made in the opposite direction (the desired response). With practice you should expect patients to be able to perform the antisaccade task with a percent of error near zero for an interval of 5 to 10 s. When overall performance from the start to the end of the task was investigated in a large number of young healthy male subjects, the percent error has been noted to be 23% with a large variance of 17% (Evdokimidis et al., 2002). If performance is such that correct sustained saccades cannot be obtained for 5 to 10 s, then involvement in the eye fields of the frontal cortex must be considered (Leigh & Zee, 2006).

Pursuit Tracking/Smooth Pursuit Tracking Technical Considerations General filter setting would be the same as for saccade testing with a low-pass filter at 100 Hz and a highpass filter, if used, at 3 to 10 Hz. Like saccade testing, a 60 Hz notch filter can be used as required. For pursuit tracking, the issue of the sampling rate of the video or electrode system is not as critical as in saccade testing given the much slower eye velocity being captured. Whereas many systems will provide for binocular individual eye recording, the simultaneous individual eye recording is not as clinically revealing as with saccade



10.  Eye Movement Recording and Ocular Motility Testing

evaluation. However, if this feature is available in the video systems, it can be of use, as usually a selection of either the right or the left eye can be used for analysis, thus allowing for optimization of the analysis if a poor recording was obtained for technical reasons for only one eye. What is critical with this evaluation is the use of age-sensitive normative data. Changes in performance of pursuit tracking can be seen starting in the third or fourth decades of life (Paige, 1994). Figure 10–10 shows the effects of age and the frequency of target presentation on the outcome parameter of pursuit velocity gain (discussed below). A full set of normative data for individual eye electrode recordings for all outcome parameters as a function of age is reprinted in Table 10–4 for reference (Shepard & Telian, 1996). The data given in Table 10–4 are from subjects ranging in age from 20 to 80 years with 8 to 10 normal subjects in each decade. These data are for horizontal smooth pursuit testing. Statistical analysis showed significant differences at the p = 0.05 level criteria for age grouping shown in the table. For all the smooth pursuit frequencies, the excursion of the target was a 17.5-degree peak (movement to either side of center). These data were developed using the EOG technique. The authors are not aware of pub-

lished normative data as a function of age developed using video recordings. It is the use of age-sensitive normative data that improves the overall performance of smooth pursuit testing, not by increasing sensitivity but by increasing the specificity of the test. Attention to the stimulus for smooth pursuit tracking by fixed velocity (ramp) or varying acceleration/ velocity (sinusoidal) target protocols (see below) can maximize performance. The greater brightness of the target and the large size of the target are both features that improve performance (Hutton & Tegally, 2005). Even if the visual field is filled with the stimulus, it is the central portion of the fovea that dominates the response (van den Berg & Collewijin, 1986; Van Die & Collewijin, 1986). For smooth pursuit tracking as well as for saccade testing, these are novel tasks for the patient. Even though the ocular motor tasks are used throughout an individual’s daily routines, they are not used in a focused and isolated manner as when testing. Therefore, to achieve maximum performance, the tasks may have to be repeated with coaching multiple times. It is important not to accept the first trial for saccades or pursuit tracking as adequate performance unless the first trial is either normal or explainable by age-related normative data. Parameters for Analysis

Figure 10–10. A modeling of smooth pursuit data acquired from normal volunteers as a function of age groupings (on the x-axis) and frequency of target movement (on the y-axis). The pursuit outcome parameter of velocity gain (see text for explanation) for the left eye is shown on the z-axis. The modeled data were developed using a negative exponential weighting function. From Practical Management of the Balance Disorder Patient by Shepard, N. T., and Telian, S. A. Copyright © 1996.

Here as with saccades, the specifics of the analysis are dependent on the manufacture of the equipment being used, unless the facility has the capability to develop its own computer sampling and analysis techniques. That said, there are three parameters more commonly seen with routine ENG/VNG analysis of smooth pursuit. These usually assume the use of a sinusoidal protocol (see discussion below). For this discussion, refer to Table 10–4 and Figure 10–11. Velocity gain is indirectly a measure of how sinusoidal the eye movement was in comparison to the target. The gain value is calculated by a ratio of peak eye velocity divided by peak target velocity. Figure 10–11 presents a plot of the overall combined velocity gain without regard to movement of the eye leftward or rightward. Other examples of velocity gain displays showing the individual gain for eye movements in each direction are provided with the discussion of interpretation given below. If the eye tracked the target in a perfect manner, the gain would be expected to be 1. As saccadic disruptions in the eye movement occur, this introduces discontinuities that reduce the sinusoidal behavior of the eye movement and result in gain values less than unity. The mathematical process to determine

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Table 10–4. Normative Data Age 20–49 Years 0.2

0.3

0.4

0.5

0.61

0.71

Gain L

0.82 0.42–1.22

0.84 0.64–1.04

0.82 0.62–1.02

0.83 0.63–1.03

0.72 0.32–1.12

0.71 0.37–0.95

Gain R

0.85 0.45–1.25

0.84 0.58–1.1

0.87 0.67–1.07

0.82 0.62–1.02

0.78 0.52–1.04

0.73 0.39–0.97

Phase

−0.36 6.36–5.64

−0.13 4.13–3.87

−0.25 4.25–3.75

−1.85 7.85–4.15

−2.36 8.36–3.64

−4.72 12.72–3.2

0.2

0.3

0.4

0.5

0.61

0.71

Gain L

0.86 0.56–1.16

0.82 0.60–1.04

0.82 0.58–1.06

0.78 0.50–1.06

0.69 0.39–0.99

0.61 0.27–0.95

Gain R

0.83 0.53–1.13

0.84 0.56–1.12

0.80 0.56–1.04

0.76 0.40–1.12

0.73 0.43–1.03

0.66 0.32–1.00

Phase

−0.4 6.40

−0.79 4.79–3.21

−0.89 4.89–3.11

−2.38 8.38–3.62

−5.06 13.06–2.9

−7.89 17.89–2.1

0.2

0.3

0.4

0.5

0.61

0.71

Gain L

0.90 0.68–1.12

0.82 0.60–1.04

0.75 0.45–1.05

0.7 0.34–1.06

0.63 0.27–0.99

0.48 0.08–0.88

Gain R

0.87 0.59–1.15

0.85 0.65–1.05

0.8 0.6–1.00

0.7 0.4–1.00

0.68 0.46–0.9

0.5 0.24–0.76

Phase

0.13 3.87–4.13

−0.01 3.81–3.79

−1.4 −6.8–4.0

−2.32 −10.3–5.7

−4.2 −11.4–3.0

−3.7 −12.7–5.3

0.2

0.3

0.4

0.5

0.61

0.71

Gain L

0.77 0.49–1.05

0.81 0.61–1.01

0.76 0.54–0.97

0.7 0.54–0.96

0.61 0.27–0.95

0.6 0.38–0.82

Gain R

0.83 0.57–1.09

0.8 0.5–1.1

0.71 0.39–1.03

0.61 0.31–0.91

0.63 0.29–0.97

0.6 0.23–0.87

Phase

−0.49 4.29–3.32

−2.64 −12–6.8

−2.3 −6.3–1.7

−4.07 −14.1–5.9

−7.8 −15.8–0.2

−8.9 −20.9–3.1

Age 50–69 Years

Age 70–79 Years

Age 80–89 Years

the actual gain is manufacturer specific. As noted in the leftmost plots in the second and third panels of Figure 10–11, the stippled region represents the age-related low range of normal (two standard deviations below the mean) for persons 49 years old. Asymmetry, shown in the middle plot of panels 2 and 3 in Figure 10–11, is simply the percentage dif-

ference for velocity gain for the right or left eye moving rightward and leftward. This provides a means to indicate asymmetric performance in smooth pursuit tracking for rightward versus leftward eye movements. Phase angle, the third parameter, provides a measure of how much the eye is lagging or leading the target. In general, given the instructions to follow or

10.  Eye Movement Recording and Ocular Motility Testing

Figure 10–11. Smooth pursuit analysis shown is from a 49-year-old female being evaluated for possible vestibular neuritis event. The top panel shows the left eye raw movement and the right raw eye trace, superimposed for each of the three frequencies tested; 0.2, 0.4, and 0.6 Hz. The testing was done using a video-recording system with the peak excursion of the target at 15° subtended arc. The second and third panels provide the analysis for velocity gain, asymmetry in velocity gain in percentage, and phase angle between the target movement and the eye movement in degrees each as a function of frequency of the target, as seen from left to right (refer to the text for an explanation of the parameters). The second panel is for the left eye whereas the third is for the right.

track the target, it is expected that the eyes will be in phase with the target or be minimally lagging behind. Patients who consistently lead the target do so with saccadic movements and usually do not understand the task requested of them. Sinusoidal Target This represents the most commonly used method for testing smooth pursuit tracking abilities. The target is presented via a light bar or projection system moving with a sinusoidal trajectory (see Video 10–3). The peak excursion of the target would be fixed between 15 and 20 degrees of subtended arc movement to either side of center. The excursion is maintained the same and the frequency of the target is varied between 0.2 and 0.6 Hz, thereby increasing the difficulty of the task. It is suggested that subtle abnormalities may be detected by increasing the task difficulty to evaluate the smooth pursuit system across its full physiologic range. However, in doing such and given the age effect on smooth pursuit, it is critical to have age-sensitive normative data to prevent false-positive identifications of pathology that actually represent degraded performance secondary to age alone. It is this paradigm that typically

uses some version of the three major analysis parameters in interpretation. Fixed-Velocity Pursuit For some patients the sinusoidal movements of a target produces nausea, which results in poor performance or inability to complete the task. An alternative is the fixed-velocity smooth pursuit task. In this paradigm the target can be presented moving left to right (or the reverse) at a speed of 20 to 40 deg/s. Each target traverses the light bar or is within the video projection field and a new target is presented at the same speed and in the same direction. After several samples, the direction is reversed at the same speed. The alternative to constant direction is to use a triangular waveform to produce the stimulus target movement. In this case the target moves left to right and then reverses back right to left. Be aware that, as the target makes a sudden stop and sudden change in direction, smooth pursuit performance will be less than perfect, as the smooth pursuit system does not handle abrupt changes without introducing a saccadic eye movement to track the target. To increase the sensitivity of the test to more subtle abnormalities, the speed is increased up to 40 deg/s.

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Speeds up to 70 deg/s are possible but the smooth pursuit tracking system’s performance is significantly poorer at these high speeds (Meyer, Lasker, & Robinson, 1985). As in the sinusoidal task, age-sensitive normative data for each of the speeds tested should be available for testing. The analysis in this situation is significantly simpler, as it is just the eye velocity divided by the target velocity that produces the gain value.

Interpretations of Smooth Pursuit Tracking The principal parameters for interpreting smooth pursuit tracking are paradigm specific. The most widely used protocol is the predictable sinusoidal or fixedvelocity target movement. For this type of paradigm, the velocity gain and phase of the eye movement with regard to the target are used for the sinusoidal target, with velocity gain as the main factor when using fixedvelocity stimuli. As with other ocular motor tasks, these parameters are highly susceptible to the state of the subject, but unlike gaze stability and saccades, smooth pursuit tracking is the task most sensitive to age. Data demonstrating the effects of age on various aspects of smooth pursuit are available in the literature (Paige, 1994; Spooner, Sakala, & Baloh, 1980; Zackon & Sharpe, 1987). The neurologic substrate (for a complete description, see the discussion in Chapter 3 of this volume) for the generation and sustaining of accurate smooth pursuit tracking starts with retinal stimulation and involves multiple areas of the cortex with projections through the pontine area of the brainstem to the cerebellum and onto the nuclei of the extraocular muscles. These pathways are suggested from both primate and human studies (Berman et al., 1999; Leigh & Zee, 2006). The complexity of the multiple pathways and the various contributions of the individual components make specific site-of-lesion identification within the pathways difficult at best, even when multiple protocols are used to investigate patient performance. No specific differentiation in lesion site has been determined when comparing reduced velocity gain for sustained target presentation at fixed velocity versus changing velocity stimuli of the sinusoidal target. Lesions could involve large cerebral infarcts, basal ganglia regions, pontine projection pathways to the cerebellum, and various areas of the cerebellum (Leigh & Zee, 2006). The principal region of the cerebellum involved in the production of smooth pursuit eye movements is that of the paraflocculus of the vestibulocerebellum (Rambold, Churchland, Selig, Jasmin, &

Lisberger, 2002). The dorsal vermis of the cerebellum is involved in the initial movement of pursuit during the onset of the task (open-loop period) but does not seem to participate in the steady-state aspects of the performance seen with fixed-velocity or sinusoidal (increasing acceleration) protocols (Takagi, Zee, & Tamargo, 2000). Therefore, although there are numerous other neurologic substrate contributions to various aspects of the performance of pursuit contingent on the specific task, the vestibulocerebellum is a common final pathway that is always involved in the production of the eye movements. Even though it is a significant oversimplification, an interpretive suggestion is that persistent abnormalities of pursuit using sustained target tasks may relate to lesions in the vestibulocerebellum (especially with coexisting gaze-evoked nystagmus) or the immediate projection pathways from the pontine nuclei of the brainstem. One must always be cognizant of the other pathway possibilities that could be involved in pursuit disruptions. The use of the phase parameter for sinusoidal target tasking is a measure of the temporal arrangement between target and eye movements. In general, at younger ages the phase angle should be close to zero for properly performed smooth pursuit. As we age or as the task becomes more difficult, by increasing the frequency of target movement the phase lag becomes more apparent. A leading phase is not usually taken as an indication of pathologic activity but rather as anticipatory behavior on the part of the patient. The leading could be anxiety regarding the testing situation or simply a lack of understanding the task. Most often this is corrected with reinstruction of the patient and repeating of the task. It is typical that reduction in gain will be seen with abnormal phase lag. However, when the phase lag is outside the normal range with velocity gain normal and reinstruction and repeated testing does not remove the abnormality, possible central system involvement should be considered but it would be less likely to involve the dorsolateral pontine nuclei or the vestibulocerebellum (Leigh & Zee, 2006). Pursuit disruptions can be bidirectional or unidirectional. When asymmetric gain is encountered, lesion sites can again range from the cortex to the pontine nuclei and vestibulocerebellum. In most cases, the pursuit abnormality is toward the lesion side due to a double decussation between the cortex and ocular motor nuclei. The magnitude of the gain disruption is usually greater for lesions in the lower system pathways versus lesion in the cortex (Leigh & Zee, 2006). Video 10–4 and Figure 10–12 demonstrate asymmetrical pursuit in a 20-year-old male with indications of cortex and

10.  Eye Movement Recording and Ocular Motility Testing

Figure 10–12. The top panel shows the target and the recorded eye movements for the right eye from a 20-year-old male following a severe closed head injury accident. The bottom panel gives the quantitative analysis for the eye movements shown in the top panel and Video 10–4. In the analysis the larger gray dots are the average performance over several cycles of the target movement with the small black dots the velocity gain for an individual cycle. All are shown as a function of frequency of target movement for a fixed target excursion of 20 degrees to each side of center. Note the significant asymmetry in performance for left versus right. See the text for discussion of the asymmetry.

subcortical involvement resulting from a closed head injury accident. The eye movements demonstrate classic saccadic disruptions to the attempt to move the eyes in a smooth manner when tracking the light bar target. This is referred to as “cog wheeling” pursuit. Note that the performance of the pursuit worsens for leftward movements yet improves for rightward movements as the frequency of the target increases. The analysis of his eye movement shown in Figure 10–12 brings up the question as to whether pursuit is interpreted as abnormal when performance at the lower frequencies is abnormal, yet as the difficulty of the task increases the performance returns to the normal region as shown for eye movement to the right in Figure 10–12. Could it be possible to have lesions in areas other than the cerebellum that may cause abnormalities at the lower

frequencies yet normal performance at the more rapid movements? It would take comparisons of fixed-velocity paradigms and the accelerating target paradigm (as used in this example) to suggest that situation (Leigh & Zee, 2006). However, in most situations, if the sinusoidal pursuit returns to a normal range as the frequency of the target for a fixed excursion is increased, the study is taken as normal, especially when the performance is symmetrical. Video 10–6 demonstrates pursuit abnormality that is strictly unidirectional with no abnormal performance to the right as a contrast with the example in Video 10–4. The quantitative analysis for this video is shown in Figure 10–13. The patient is a 33-year-old male with a closed head injury and diagnosed traumatic brain injury. Video 10–7 demonstrates abnormal pursuit that is

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Balance Function Assessment and Management

Figure 10–13.  Quantitative analysis for the eye movements shown in Video 10–6 from a 33-year-old male with diagnosed traumatic brain injury. See the legend for Figure 10–12 for an explanation of the symbols shown in the analysis panel. Note that this analysis shows strictly unidirectional pursuit disruption compared to the asymmetric pursuit performance in Figure 10–12, suggesting possible abnormalities in both directions of different magnitudes.

bidirectional and symmetric. This is from the 46-year-old female with diffuse brainstem and cerebellar involvement secondary to alcohol abuse. The quantitative analysis for her eye movements is given in Figure 10–14. There can be interactions between saccade performance and that of smooth pursuit that can give the appearance of unidirectional pursuit abnormalities that is a false positive. This is illustrated in Videos 10–8 and 10–9. These videos show random saccade performance (see Video 10–8) followed by smooth pursuit performance (see Video 10–9) in a 52-year-old female with multiple sclerosis. As can be seen in Video 10–8, the patient is displaying bilateral INO with significant slowing of each eye on adduction. Therefore, when viewing her performance for smooth pursuit, it would appear that as each eye adducts with the pursuit task, the eye is moving smoothly while the abducting eye has a saccadic appearance. The smooth movements of each eye on the pursuit task for adduction are a result of the effects of the INO causing saccades to not be produced, as is seen when abducting movement is made. It is the combination of the INO and the central system lesion to the pursuit neuro-substrate that gives the appearance of unidirectional pursuit abnormality.

tral brainstem/cerebellar lesions, whereas abnormalities in gaze stability can occur from either a central or peripheral vestibular system lesion. Criteria for differentiating between central and peripheral lesions are discussed below. Technical Considerations Filter settings and sampling rates would be the same as that for smooth pursuit tracking, and usually individual eye recordings would not be necessary. However, if one eye is observed with a visual occluding camera while the other has vision, a form of nystagmus known as latent nystagmus (jerk nystagmus that has its fast component away from the occluded eye) can result from an ocular misalignment, specifically that of congenital strabismus, most likely esotropia, (Dell’Osso, Ellenberger, Abel, & Flynn, 1983) and may not be representative of either a peripheral or a central lesion. Because of this, when using a video system with a single visual occluding camera, it is always best to check gaze stability with both eyes viewing the target prior to the formal recording of gaze stability. Parameters for Analysis

Gaze Stability Testing This evaluates a patient’s ability to maintain gaze on a target in primary position or eccentric positions (right, left, up, or down) in a steady manner without the production of eye movements, principally jerk nystagmus, or presence of saccadic intrusions. The sole purpose of saccade and pursuit testing is the identification of cen-

In the majority of abnormal gaze stability, the type of eye movement is that of jerk nystagmus. If the nystagmus is persistent in primary gaze, it is referred to as fixation present spontaneous, designating the direction of the beat, and one can give the average slow component velocity. When jerk nystagmus is noted in any of the eccentric positions, it is referred to as fixation present gaze-evoked nystagmus, again designating the

Figure 10–14.  Quantitative analysis for the eye movements from the 46-year-old female shown in Video 10–7. Shown are the sample recordings for both the right eye in the upper panel and the left eye in the lower panel. The quantitative analysis for each eye is shown below the eye tracings. See text for further information and Figure 10–12 legend for explanation of the symbols on the figure. 209

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Balance Function Assessment and Management

direction of the fast component. A specific nomenclature is used when nystagmus is horizontal and direction fixed. Designation as to fixation present or fixation removed is made along with an indication as to the direction of the nystagmus beat. Next, it is indicated whether the nystagmus was present when gazing only in the direction of the fast component (first degree), in the direction of the fast component and in primary (second degree), or in the direction of the beat, primary, and while gazing away from the beat of the nystagmus (third degree). Last, it is indicated whether the nystagmus followed Alexander’s law (see Chapter 3 for a full explanation) — if it follows Alexander’s law, the nystagmus will increase in its briskness (slow component velocity) as the gaze is directed further in the direction of the fast component of the nystagmus). For example, the phrase “third degree, left-beating gaze evoked nystagmus with fixation present following Alexander’s law” implies a left-beating nystagmus that is present with fixation when the individual is looking at a target to the right, primary, and left, and the nystagmus increases in intensity as the gaze is shifted toward the direction of the fast component, to the left. In all other situations, when nystagmus changes direction or another nonjerk nystagmus eye movement is noted, a verbal description of those movements is required. Although these are descriptive techniques instead of quantitative analysis as used for saccades and smooth pursuit, they are adequate for the analysis of gaze-stability testing, as the primary focus is the presence or absence of abnormal eye movements. This is especially true when one encounters saccadic intrusions, although some minor analysis of the eye movement recording may be needed to distinguish between certain forms of saccadic intrusions (see discussion below). Protocol Gaze stability testing is usually performed first with fixation present using a target in the primary position. The target is then moved 25 to 30 degrees (this would be considered the minimum subtended arc movement to elicit gaze-evoked nystagmus) to the right, left, up, or down. If the subtended arc movement exceeds 30 degrees laterally or up, the possibility of physiologic endpoint nystagmus is increased. However, physiologic endpoint nystagmus is not persistent when fixation is present, decaying to stable eye movement typically within seconds (Leigh & Zee, 2006). Between each of the eccentric gaze positions, it is important to return to the primary position to observe for rebound nystagmus (a jerk nystagmus that beats in the direction of the last movement of the eyes). Each of the positions

(primary, eccentric, and primary for rebound) should be held for at least 10 s to observe for nystagmus. Avoid prolonged eccentric gaze (>1 min) as that can produce a rebound nystagmus in normal subjects (Leigh & Zee, 2006). In all positions, other than testing for rebound, the nystagmus, if seen, should be persistent; rebound nystagmus will decay. Following gaze stability with fixation present, it is repeated with fixation removed, asking the patient to gaze straight ahead, then to the right, left, up, and down, each time returning to center between each of the eccentric positions. It is not necessary to try and control the position of the eccentric eye locations laterally or up or down. Some patients will move the eyes to the extreme in the lateral directions, and this may produce physiologic endpoint nystagmus that without a visual target can be persistent. This is recognized by the following features: (1) the nystagmus is symmetric looking to the right or left; (2) it is of typically low slow component velocity ( 12º/sec or TotLE > 12º/sec

TotRE + TotLE > 22–30 deg/sec

Bilateral weakness

Hyperactivity

TotRE < 140º/sec and TotLE < 140º/sec

Fixation suppression

FI% < 0.6

RC or LC or RW or LW > 8 deg/sec TotRE < 110º/sec and TotLE < 110º/sec RC and LC < 50–60 deg/sec and RW and LW < 80 deg/sec 0.5–0.7

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weakness is within the range of 20% to 25%. Each laboratory is free to choose the value within this range that produces the best combination of sensitivity and specificity for its specific clinical settings. There are more discrepancies among different studies regarding the normative values for directional preponderance. This is likely related to the limitations associated with directional preponderance, which were discussed previously. The most common normative limit for directional preponderance is 30% but some laboratories use a lower value of 25%. As noted previously, it has now become clear that directional preponderance is of limited clinical value (Hain, 2014). As a result, some laboratories no longer use it. Those who wish to continue using directional preponderance should consider separating the contribution of baseline shift and gain asymmetry, because they represent two distinct abnormalities. The sum of peak caloric responses is used to determine hypoactivity (bilateral weakness) and hyperactivity of the vestibular pathways. It should be stated that the caloric test is not a particularly useful test to detect bilateral vestibular hypoactivity. Therefore, it should not be surprising that there are considerable differences among different studies about the normal limits for total caloric responses. These differences are related to the high variability of caloric stimulus and individual differences in heat transfer from the external auditory canal to the labyrinth. The lower normal limit for total caloric responses has been estimated to be anywhere from 22 to 30 deg/ sec (Barber & Stockwell, 1980; Jacobson et al., 1993). It is stipulated that the normal limit should apply only when caloric responses from the right and left ears are symmetric. To address this issue, some have recommended imposing a lower normal limit on the peak caloric responses of individual irrigations (e.g., all irrigations less than 8 deg/sec by BSA [2010]). An alternative approach is to define the threshold for bilateral weakness based on total responses from each ear. Stockwell (1993) defines the caloric test to be bilaterally weak when total responses from each ear are less than 12 deg/sec. Using this approach eliminates the possibility of misidentifying the test as bilateral weakness when the responses of only one ear are very small. Since the caloric test is of limited value in identifying patients with bilateral vestibular hypoactivity, one can simplify the process. If a patient is suspected of having bilateral caloric weakness using any of the above criteria, another test, such as the rotation test or the head impulse test, should be included in the evaluation protocol. The normative limits for hyperactive caloric responses have also been defined differently in dif-

ferent studies. Barber and Stockwell (1980) consider caloric responses as hyperactive when peak slowphase velocities exceed 50 deg/sec for each of the cool irrigations or 80 deg/sec for each of the warm irrigations. Jacobson et al. (1993) use the criteria of total cool and warm responses of greater than 99 deg/sec and 146 deg/sec, respectively, and total caloric response of greater than 221 deg/sec from both ears. Again, to account for asymmetric caloric responses and presence of spontaneous nystagmus, one can use total responses from either ear as the criterion for hyperactivity (see Table 12–2). The fixation index (FI%) represents the patient’s ability to suppress vestibular nystagmus. As with most caloric response parameters, there is no general agreement as to the normal limit for the fixation index. Some studies have suggested that any suppression of nystagmus (FI% 11.7

100

88

>17.1

100

98

>20.3

97

100

>7.5

100

94

>9.3

100

100

>9.9

93

100

Peak-to-peak amplitudes

N1 amplitudes

Click-oVEMP

Peak-to-peak amplitudes

>9.9

100

100

Click-oVEMP

N1 amplitudes

>2.5

100

68

>6.6

94

100

Source: Data from Zuniga, M. G., Janky, K. L., Nguyen, K. D., Welgampola, M. S., and Carey, J. P. (2013). Ocular versus cervical VEMPs in the diagnosis of superior semicircular canal dehiscence syndrome. Otology and Neurotology, 34, 121–126.

Table 16–6.  Ocular Vestibular-Evoked Myogenic Potential Sensitivity and Specificity for Patients with Superior Canal Dehiscence

Age Decade

Cutoff Value (µv) (threshold)

Sensitivity (%)

Specificity (%)

30s

> Posttraumatic stress disorder = Panic/ phobic

— Dysautonomia

Neurally mediated reflex syncope Postural orthostatic tachycardia syndrome

No psychiatric diagnosis >> Panic/ phobic = Generalized anxiety = Minor anxiety

Atrial or ventricular dysrhythmias

Panic/phobic = Generalized anxiety

PPPD and CNS illness

PPPD & dysrhythmias — Dysrhythmia

Source:  Adapted from Staab and Ruckenstein (2007).

score may be more valid than subscale scores. In our experience, patients may be more likely to acknowledge behavioral problems on the DHI (through total scores >25) than on dedicated anxiety or depression scales, though we employ both in daily practice. Several short and simple self-report questionnaires are available to screen patients with vestibular and balance conditions for clinically significant anxiety and depressive symptoms. The ones most widely used in primary care settings are the nine-item Patient Health Questionnaire (PHQ-9) and the seven-item Generalized Anxiety Disorder Scale (GAD-7). Both were derived from a clinician-administered screening package (Spitzer, Kroenke, & Williams, 1999) that was validated for use in adults with vestibular symptoms (Persoons et al., 2003). However, the self-report versions have superseded the older clinician-administered modules. In fact, the first two questions of the PHQ-9 and GAD-7 were combined into an ultra-short, 4-item questionnaire (the PHQ-4), which has nearly the same sensitivity and specificity for detecting clinically significant anxiety and depressive symptoms as the longer instruments. All patients who undergo vestibular testing at the authors’ institution are screened for psychiatric symptoms using the PHQ-4. The PHQ-9, GAD-7,

and PHQ-4 may be obtained free of charge without copyright restrictions at phqscreeners.org. An alternative to the PHQ/GAD screeners is the Hospital Anxiety and Depression Scale (HADS), which has seven questions for anxiety and seven for depression (Zigmond & Snaith, 1983). It is self-explanatory and easy to score, and correlates well with formal psychiatric assessments. The HADS has been used in patients with dizziness to screen for anxiety and depression (Grunfeld et al., 2003) and track the progress of medication treatment (Horii et al., 2007). Permission to use the HADS may be obtained from http://www.gl-assessment.co.uk

Treatment Options To date, there have been no large-scale, randomized, controlled trials of medications or other treatments for behavioral morbidity in patients with vestibular symptoms. Researchers continue to examine the benefits of medication, vestibular rehabilitation, and psychotherapy. In clinical practice, these three therapies may be combined depending on the needs of individual patients.

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Medications From 2002 to 2007, five uncontrolled studies (one case series and four open-label prospective trials) of SSRIs involving nearly 200 patients were conducted in the United States and Japan to investigate the potential benefits of these medications for treating patients with chronic dizziness (Horii et al., 2004, 2007; Simon et al., 2005; Staab et al., 2002, 2004). A synthesis of the findings is that SSRIs are safe and well tolerated by patients with persistent vestibular symptoms, despite dizziness being listed as a common side effect for this class of medications. SSRIs reduced chronic dizziness in patients with CSD regardless of the severity of coexisting psychiatric illness (Simon et al., 2005; Staab et al., 2002, 2004). However, SSRIs were not effective for patients with other chronic vestibular symptoms plus low levels of anxiety and depression (Horii et al., 2004, 2007; Simon et al., 2005). Studies using serotonin-norepinephrine reuptake inhibitors (SNRIs) yielded similar results (Horii et al., 2008; Staab, 2011a), with the potential added benefit that the SNRI venlafaxine might be effective for vestibular migraine (Staab, 2011a). More recently, the largest medication trial for PPPD to date was conducted in China (Yu, Xue, Zhang, & Zhou, 2018). This open-label, prospective study compared 45 patients with PPPD who were treated with sertraline alone with 46 patients with PPPD who were treated with sertraline plus cognitive behavior therapy (CBT). There was no untreated control group. Both treated groups improved, but the group that received combined interventions had a more robust response with a lower dose of medication. Goto et al. (2014) reported success in a case series of three patients with Ménière’s disease using sertraline to reduce residual daily dizziness that persisted after successful medicalsurgical treatment of major vertigo attacks. All of these findings await conformation by adequately powered, randomized controlled trials.

Vestibular Rehabilitation Vestibular and balance rehabilitation therapy (VBRT) is now commonly used to improve compensation in patients who have sustained acute vestibular losses, but it was first developed to treat patients with long-standing chronic dizziness, including many who now would be diagnosed with PPPD (Staab, 2011b). Randomized, comparative studies involving more than 400 patients have established VBRT as an effective treatment for

most types of chronic vestibular symptoms, though the mechanism is likely to be habituation (i.e., systematic desensitization), not compensation (Staab, 2011b). When used to habituate chronic vestibular symptoms, VBRT must be started more gently and advanced more slowly than is commonly done to enhance compensation after acute vestibular syndromes. In this manner, VBRT is also effective in reducing comorbid anxiety and depression (Meli et al., 2007). One retrospective study reported good satisfaction among patients with PPPD who underwent a single physical therapy consultation followed by performance of a home-based exercise program, though sensitivity to self-motion seemed to improve to a greater extent than sensitivity to visual flow and visual complexity (Thompson, Goetting, Staab, & Shepard, 2015).

Psychotherapy Two sets of studies investigated the efficacy of CBT for patients with PPV and CSD. Originally, CBT was developed to treat major depression, but variations on the core techniques have expanded its indications to anxiety, traumatic stress, and somatic symptom disorders as well as several functional conditions. Holmberg et al. (2006) showed that CBT reduced physical symptoms and related functional impairments in patients with chronic PPV, but its benefits did not persist at one year of follow-up (Holmberg et al., 2007). Edelman and colleagues (Edelman et al., 2012; Mahoney et al., 2013) were more successful. They captured patients at about eight months following acute vestibular syndromes, before CSD had become very chronic, and showed that a short course of CBT produced rapid benefits (Edelman et al., 2012) that were sustained six months later (Mahoney et al., 2013). This suggests that CBT may have prophylactic benefits for patients who demonstrate evidence of emerging PPPD, offering secondary prevention of this chronic condition before it develops completely. CBT and VBRT are complementary treatments that can be used together clinically. The hope is that CBT will address cognitive patterns that reinforce vestibular symptoms (e.g., “I’ll crash the car”) (Yardley et al., 2001), while VBRT will extinguish motion hypersensitivity and improve balance confidence. Pilot studies support this notion (Jacob et al., 2001; Johansson et al., 2001; Pavlou et al., 2004). In addition, the study by Yu, Xue, Zhang, and Zhou (2018) suggests that CBT can be a very useful complement to medication treatment, especially of PPPD.



23.  Behavioral Factors in Dizziness and Vertigo

Conclusions Perceived threats and anxiety have profound effects on balance function in completely normal individuals and patients with vestibular symptoms caused by neurotologic or psychiatric conditions. The threat/anxiety system changes the speed and intensity of postural control movements in response to perceived threats. Anxiety disorders may cause vestibular symptoms in the absence of neurotologic illnesses, while neurotologic illnesses may trigger new anxiety disorders or exacerbate preexisting ones. Patients with anxiety-related temperamental predispositions (neuroticism) seem to suffer greater physical and psychiatric morbidity in the aftermath of medical or psychiatric triggers of vestibular symptoms than patients without a significant anxiety diathesis. The syndrome of PPPD may sustain chronic morbidity long after the inciting events have resolved. The principal barriers to detecting behavioral morbidity in patients with vertigo, unsteadiness, and dizziness are a single-minded focus on the vestibular system as the source of these symptoms and misconceptions about the role of psychological mechanisms in sustaining vestibular complaints. Patients and practitioners frequently share this single-mindedness. With epidemiologic research showing that 30% to 50% of balance patients have psychiatric comorbidity, authors in Asia (Horii et al., 2007), Europe (Best et al., 2006), and the United States (Staab, 2006a, 2006b) have recommended that psychiatric screening become an integral part of neurotologic evaluations for patients presenting with acute or chronic vestibular symptoms. Simple and effective psychiatric screening tools are available for this purpose. Recent data suggest that serotonergic antidepressants, vestibular rehabilitation, and cognitive behavior therapy may alleviate physical and psychiatric morbidity in patients with chronic vestibular symptoms.

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disorder: Symptom profiles and test findings. American Journal of Otology, 11, 338–341. Söderman, A. C., Bagger-Sjöbäck, D., Bergenius, J., & Langius, A. (2002). Factors influencing quality of life in patients with Ménière’s disease, identified by a multidimensional approach. Otology & Neurotology, 23(6), 941–948. Söhsten, E., Bittar, R. S., & Staab, J. P. (2016). Posturographic profile of patients with persistent postural-perceptual dizziness on the sensory organization test. Journal of Vestibular Research, 26, 319–326. Spitzer, R. L., Kroenke, K., & Williams, J. B. (1999). Validation and utility of a self-report version of PRIME-MD: The PHQ Primary Care Study. JAMA, 282, 1737–1744. Staab, J. P. (2006a). Chronic dizziness: The interface between psychiatry and neuro-otology. Current Opinion in Neurology, 19, 41–48. Staab, J. P. (2006b). Assessment and management of psychological problems in the dizzy patient. Continuum: Lifelong Learning in Neurology, 12, 189–213. Staab, J. P. (2006c). Anxiety and depression in older patients with otorhinolaryngologic illnesses. In K. Calhoun, D. E. Eibling, M. K. Wax, & K. Kost (Eds.), Geriatric otolaryngology (pp. 633–646). New York, NY: Marcel Dekker. Staab, J. P. (2011a). Clinical clues to a dizzying headache. Journal of Vestibular Research, 21(6), 331–340. Staab, J. P. (2011b). Behavioral aspects of vestibular rehabilitation. NeuroRehabilitation, 29(2), 179–183. Staab, J. P. (2012). Chronic subjective dizziness. Neuro-otology 18(5), 1118–1141. Minneapolis, MN: Continuum. Staab, J. P. (2013). Behavioural neuro-otology. In A. M. Bronstein (Ed.), Oxford textbook of vertigo and imbalance (pp. 333–346). New York, NY: Oxford University Press. Staab, J.P., Eckhardt-Henn, A., Horii, A., Jacob, R., Strupp, M., Brandt, T., & Bronstein, A. (2017). Diagnostic criteria for persistent postural-perceptual dizziness (PPPD): Consensus document of the committee for the Classification of Vestibular Disorders of the Bárány Society. Journal of Vestibular Research, 27, 191–208. Staab, J., Eggers, S., Neff, B., & Shepard, N. (2010). Validation of a clinical syndrome of persistent dizziness and unsteadiness. Abstracts from the XXVI Bárány Society Meeting, Reykjavik, Iceland, August 18–21, 2010. Journal of Vestibular Research, 20(3–4), 172–173. Staab, J. P., Rohe, D. E., Eggers, S. D., & Shepard, N. T. (2014). Anxious, introverted personality traits in patients with chronic subjective dizziness. Journal of Psychosomatic Research, 76(1), 80–83. Staab, J. P., & Ruckenstein, M. J. (2003). Which comes first? Psychogenic dizziness versus otogenic anxiety. Laryngoscope, 113, 1714–1718. Staab, J. P., & Ruckenstein, M. J. (2005). Chronic dizziness and anxiety: Effect of course of illness on treatment outcome. Archives of Otolaryngology–Head and Neck Surgery, 131, 675–679. Staab, J. P., & Ruckenstein, M. J. (2007). Expanding the differential diagnosis of dizziness. Archives of Otolaryngology– Head and Neck Surgery, 13, 170–176.



Staab, J. P., Ruckenstein, M. J., & Amsterdam, J. D. (2004). A prospective trial of sertraline for chronic subjective dizziness. Laryngoscope, 114, 1637–1641. Staab, J. P., Ruckenstein, M. J., Solomon, D., & Shepard, N. T. (2002). Serotonin reuptake inhibitors for dizziness with psychiatric symptoms. Archives of Otolaryngology–Head and Neck Surgery, 128, 554–560. Stein, M. B., Asmundson, G. J. G., Ireland, D., & Walker, J. R. (1994). Panic disorder in patients attending a clinic for vestibular disorders. American Journal of Psychiatry, 151, 1697–1700. Swinson, R. P., Cox, B. J., Rutka, J., Mai, M., Kerr, S., & Kuch, K. (1993). Otoneurological functioning in panic disorder patients with prominent dizziness. Comprehensive Psychiatry, 34, 127–129. Takahashi, M., Ishida, K., Iida, M., Yamashita, H., & Sugawara, K. (2001). Analysis of lifestyle and behavioral characteristics in Meniere’s disease patients and a control population. Acta Oto-Laryngologica (Stockholm), 121, 254–256. Tecer, A., Tukel, R., Erdamar, B., & Sunay, T. (2004). Audiovestibular functioning in patients with panic disorder. Journal of Psychosomatic Research, 57, 177–182. Thompson, K. J., Goetting, J. C., Staab, J. P., & Shepard, N. T. (2015). Retrospective review and telephone follow-up to evaluate a physical therapy protocol for treating persistent postural-perceptual dizziness: A pilot study. Journal of Vestibular Research, 25, 97–103. Tschan, R., Best, C., Beutel, M. E., Knebel, A., Wiltink, J., Dieterich, M., & Eckhardt-Henn, A. (2011). Patients’ psychological well-being and resilient coping protect from secondary somatoform vertigo and dizziness (SVD) 1 year after vestibular disease. Journal of Neurology, 258, 104–112. Viaud-Delmon, I., Ivanenko, Y. P., Berthoz, A., & Jouvent, R. (2000a). Adaptation as a sensorial profile in trait anxiety: A study with virtual reality. Journal of Anxiety Disorders, 14, 583–601. Viaud-Delmon, I., Siegler, I., Israel, I., Jouvent, R., & Berthoz, A. (2000b). Eye deviation during rotation in darkness in trait anxiety: An early expression of perceptual avoidance? Biological Psychiatry, 47, 112–118. Wada, M., Sunaga, N., & Nagai, M. (2001). Anxiety affects the postural sway of the antero-posterior axis in college students. Neuroscience Letters, 302, 157–159.

23.  Behavioral Factors in Dizziness and Vertigo

Westphal, C. (1871). Die Agoraphobie, eine neuropathische Erscheinung, Zeitschrift für Psychiatrie, Berlin 3, 138–161. World Health Organization. (2018). Persistent posturalperceptual dizziness. ICD-11 for Mortality and Morbidity Statistics (Version: 04/2018). Retrieved from https://icd​ .who.int/browse11/l-m/en#/http%3a%2f%2fid.who.int​ %2ficd%2fentity%2f2005792829 Yan, Z., Cui, L., Yu, T., Liang, H., Wang, Y., & Chen C. (2016). Analysis of the characteristics of persistent posturalperceptual dizziness: A clinical-based study in China. International Journal of Audiology, 6(56), 1–5. Yardley, L., Beech, S., & Weinman, J. (2001). Influence of beliefs about the consequences of dizziness on handicap in people with dizziness, and the effect of therapy on beliefs. Journal of Psychosomatic Research, 50, 1–6. Yardley, L., Britton, J., Lear, S., Bird, J., & Luxon, L. M. (1995a). Relationship between balance system function and agoraphobic avoidance. Behavior Research and Therapy, 33, 435– 439. Yardley, L., Donovan-Hall, M., Smith, H. E., Walsh, B. M., Mullee, M., & Bronstein, A. M. (2004). Effectiveness of primary care-based vestibular rehabilitation for chronic dizziness. Annals of Internal Medicine, 141, 598–605. Yardley, L., Luxon, L. M., & Haacke, N. P. (1994). A longitudinal study of symptoms, anxiety and subjective well-being in patients with vertigo. Clinical Otolaryngology and Allied Sciences, 19, 109–116. Yardley, L., Verschuur, C., Masson, E., Luxon, L., & Haacke, N. (1992). Somatic and psychological factors contributing to handicap in people with vertigo. British Journal of Audiology, 26, 283–290. Yardley, L., Watson, S., Britton, J., Lear, S., & Bird, J. (1995b). Effects of anxiety arousal and mental stress on the vestibuloocular reflex. Acta Oto-Laryngologica, 115, 597–602. Yu, Y.-C., Xue, H., Zhang, Y.-X., & Zhou, J. (2018). Cognitive behavior therapy as augmentation for sertraline in treating patients with persistent postural-perceptual dizziness. BioMed Research International, Article ID 8518631. https:// doi.org/10.1155/2018/8518631 Zigmond, A. S., & Snaith, R. P. (1983). The Hospital Anxiety and Depression Scale. Acta Psychiatrica Scandinavica, 67, 361–370.

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24 Vestibular Rehabilitation Susan L. Whitney and Joseph M. Furman

Overview Vestibular rehabilitation is increasingly becoming an indispensable treatment modality for patients with dizziness and/or balance problems. Vestibular rehabilitation has taken on many forms over the years, from a group exercise class in the 1940s (Cawthorne, 1944; Cooksey, 1946) to its present form where people receive a customized exercise program (Alahmari et al., 2014; Rossi-Izquierdo et al., 2017; Whitney, Alghadir, & Anwer, 2016). This chapter provides an overview of the history of vestibular rehabilitation, what types of patients might be aided with a rehabilitation program, some basic principles of vestibular rehabilitation, and the typical outcomes from vestibular rehabilitation, including the positive and negative predictors of success. Vestibular rehabilitation was first described in the 1940s by Cooksey and Cawthorne, (Cawthorne, 1944; Cooksey, 1946) who developed and published their description of a group exercise program that was designed to decrease dizziness in persons with vestibular dysfunction from head injuries (postconcussion disorder and other cases of “giddiness”) (Cawthorne, 1944). Cawthorne (1944) noted that their exercise program was effective following postconcussion and with unilateral peripheral vestibular hypofunction. Cawthorne (1944) suggested that vestibular disorders can cause people to limit their activities of daily living as well as cause people to restrict their activities outside the home (e.g., work activities). Cawthorne’s (1944) group exercise program incorporated eye–head exercises designed to stimulate the semi-

circular canals and the otolith organs. Exercise was started early after onset of symptoms (i.e., as soon as it was deemed “safe”). Exercises were prescribed that gradually became faster and more difficult as the person improved. Patients participated in the Cawthorne group exercise program between 10 days up to a month, with the exercise program encompassing the “entire day” (Cawthorne, 1944). Ironically, parts of the Cawthorne–Cooksey exercise program today would be considered dangerous (Table 24–1). The original group exercise program had advanced patients walking up and down steps and ladders with eyes closed (Cawthorne, 1944; Cooksey, 1946). Cawthorne (1944) and Dix (1976) advocated that persons had better outcomes if seen early after vestibular insult, a thought supported by recent findings (Bamiou, Davies, McKee, & Luxon, 2000). Both Cawthorne (1944) and Cooksey (1946) suggested a gradually more difficult program of mental exercise and physical and occupational therapy in their program that occupied their entire day. Exercises generally started in supine position and progressed to walking with eyes open and closed. Mental exercises were incorporated one hour a day, and in occupational therapy, patients were advised to progress to perform their exercises in crowded or noisy circumstances. “Mental exercises” are not generally used today but all patients are encouraged to progress their exercise program in more visually challenging environments, such as crowded or visually stimulating situations as they improve. Dual-tasking is commonly incorporated into exercise programs of persons who are at less risk for falling (Lei-Rivera, Sutera, Galatioto, Hujsak, & Gurley, 2013). Cawthorne (1944) also advocated performing the

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Table 24–1.  Cawthorne-Cooksey Exercises as Adapted by Dix (A)  In bed

(1)  Eye movements — at first slow, then quick, (a) up and down, (b) from side to side, and (c) focusing on finger movement from 3 feet to 1 foot away from face. (2)  Head movements at first slow, then quick; later with eyes closed, (a) bending forward and backward, and (b) turning from side to side.

(B) Sitting (in class)

(1)  and (2) as in (A) (3) Shoulder shrugging and circling (4)  Bending forward and picking up objects from the ground

(C) Standing (in class)

(1)  Exercises (1) and (2) in (A), and (3) in (B) (2)  Changing from sitting to standing position with EO and EC (3) Throwing a small ball from hand to hand (above eye level) (4) Throwing a ball from hand to hand under knee (5)  Change from sitting to standing and turning round in between

(D) Moving about (in class)

(1)  Circle round center person who will throw a large ball and return it (2)  Walk across the room with EO and EC (3)  Walk up and down slope with EO and EC (4)  Walk up and down steps with EO and EC (5) Any game involving stooping or stretching and aiming such as skittles, bowls, or basketball

Note.  EO = eyes open; EC = eyes closed. Source: Reproduced from Dix, M. R. (1976). The physiological basis and practical value of head exercises in the treatment of vertigo. Practitioner, 217, 919–924. Reprinted with permission from Practitioner Medical Publishing Ltd.

exercises preoperatively so that patients were familiar with the exercises prior to surgery, which has recently been supported in the literature prior to inner ear surgery (Magnusson et al., 2009; Magnusson, Karlberg, & Tjernstrom, 2011). Cooksey (1946) suggested that the exercise programs were both physical and psychological. There have been links established between anxiety and vestibular disorders (Balaban & Thayer, 2001; Beidel & Horak, 2001; Eagger, Luxon, Davies, Coelho, & Ron, 1992; Guerraz et al., 2001; Gurr & Moffat, 2001; Holmberg, Karlberg, Harlacher, Rivano-Fischer, & Magnusson, 2006; Jacob & Furman, 2001; Jacob, Whitney, Detweiler-Shostak, & Furman, 2001; Nagaratnam, Ip, & Bou-Haidar, 2005; Nagarkar, Gupta, & Mann, 2000; Pollak, Klein, Rafael, Vera, & Rabey, 2003; Sklare, Konrad, Maser, & Jacob, 2001; Yardley, 1994; Yardley, Luxon, & Haacke, 1994; Yardley & Putman, 1992; Yardley &

Redfern, 2001). Studies also support the connections between the vestibular system and the autonomic nervous system (Balaban, 1999; Balaban & Porter, 1998; Balaban & Thayer, 2001), suggesting that there is an anatomic link between the vestibular apparatus and the regulation of blood pressure and breathing (Yates, 1996; Yates, Billig, Cotter, Mori, & Card, 2002; Yates & Bronstein, 2005). Most of the original ideas of Cooksey and Cawthorne are in use today in some form, although walking up slopes and stair climbing with eyes closed is not done in the United States. Group exercises are not typically performed because it is very difficult to organize groups of persons with similar complaints. Due to safety considerations, walking with eyes closed on any surface is performed with extreme caution and only with highly advanced patients. Eye/head exercises are performed with almost every person with vestibular



dysfunction, as suggested by Cooksey and Cawthorne, and their general principles of gradually increasing the difficulty and the speed of the activity appear to have been incorporated into all exercise programs used to address vestibular dysfunction. Dix (1976) suggested that people with head injuries, drug intoxication, and psychogenic dizziness were good candidates for rehabilitation. Dix (1976) was the first to describe the typical “stiff” gait that patients with vestibular disorders display, especially the difficulty with turning their trunk during gait. Fatigue was also described by Dix (1976), which is a common complication of vestibular disorders. Fatigue, especially at the end of the day for patients, can complicate their rehabilitation progress. The original exercises that Dix (1976) suggested for a home exercise program were performed for five minutes, three times a day for up to one to three months until the symptoms resolved (Dix, 1976). Today, it is commonly thought that exercise may need to be “dosed” in smaller quantities for the patient to be compliant with the exercise program. If exercises are done all at one time, the patient may feel worse, which is a negative factor related to exercise compliance. Norré and DeWeerdt (1981) suggested that habituation therapy might help to provoke dizziness and remediate dizziness symptoms in persons with vestibular disorders. Patients were asked to move into the dizziness provocative positions to decrease the intensity of the response. Differences in their program compared with the Cooksey–Cawthorne program were that their program was individualized and only patients with motion provoked symptoms were included. Thirty-four different positions were tested and the number of provocative positions decreased by over 50% within a two-month period (Norré & DeWeerdt, 1981). Fifty-three percent of the patients were symptom free, with 92% reporting at least partial improvement in symptoms. The Brandt–Daroff exercise was also developed in the 1980s to treat patients with motion-provoked dizziness (Brandt & Daroff, 1980). Brandt and Daroff suggested that people perform the exercise two times each day for at least 10 repetitions while they were hospitalized for up to 14 days. A 99% positive response rate was reported from the exercise with complete resolution of the patient’s benign paroxysmal positional vertigo (BPPV). Norré and Beckers later suggested that vestibular exercises needed to be customized based on their findings after developing a measure to record symptoms in 19 provocative positions (Norré & Beckers, 1988).

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Patients selectively had symptoms only in some of the positions tested, and Norré and Beckers suggested that the exercise program needed to be customized to meet the patient’s needs (Norré & Beckers, 1988). Norré and Beckers recorded the intensity and duration of symptoms after passive head movements and treated patients based on the specific deficits that they identified in their provocative movement testing. Active exercise was performed at home five times daily. Norré (1987) later reported that his individualized exercise program of habituation exercises was more effective in the reduction of symptoms than a general exercise program (Norré, 1987). McCabe (1970) suggested that patients with unstable vestibular disorders are not good candidates for rehabilitation, which is still true 44 years later. He reported on 15 years of experience with vestibular rehabilitation and stated that the following patient diagnoses benefited from exercises: central and peripheral postural vertigo, the “irritable labyrinth” with motion intolerance, labyrinthitis, temporal bone fracture, traumatic vertigo, destructive labyrinthectomy, and Wallenberg’s syndrome (McCabe, 1970). He reported that drugs used to mask symptoms appeared to prevent or slow the recovery process. Horak, Jones-Rycewicz, Black, and ShumwayCook (1992) subsequently attempted to determine if medication to suppress dizziness, a general conditioning program, or a vestibular rehabilitation program would be more effective in decreasing symptoms and enhancing postural control in persons with chronic vestibular hypofunction. Patients were treated twice a week for 6 weeks and there were improvements in dizziness in all groups. The only group that demonstrated changes in balance was the vestibular rehabilitation group (Horak et al., 1992). Many studies have demonstrated changes in postural control after vestibular rehabilitation (Asai, Watanabe, & Shimizu, 1997; Bamiou et al., 2000; Brown, Whitney, Wrisley, & Furman, 2001; Cass, Borello-France, & Furman, 1996; Gottshall, Hoffer, Moore, & Balough, 2005; Gurr & Moffat, 2001; Jacob et al., 2001; Konrad et al., 1992; Krebs, Gillbody, Riley, & Parker, 1993; Medeiros et al., 2005; Meli, Zimatore, Badaracco, De Angelis, & Tufarelli, 2006; Pavlou et al., 2004; Shepard & Telian, 1995; SmithWheelock, Shepard, & Telian, 1991; Suarez et al., 2003; Telian, Shepard, Smith-Wheelock, & Hoberg, 1991; Viirre & Sitarz, 2002). More recent studies have supported the use of vestibular rehabilitation in persons with both peripheral and central vestibular disorders. There is much more evidence for the use of vestibular rehabilitation in

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persons with peripheral vestibular hypofunction than any other vestibular condition, primarily because they are the easiest group to study and it is a common diagnostic category (Hall et al., 2016; Hillier & McDonnell, 2016). There is much more heterogeneity in central vestibular disorders, making them more difficult to study (Furman & Whitney, 2000).

Theoretical Considerations Vestibular Compensation and Recovery Patients with vestibular disorders often experience dizziness, vertigo, motion sickness, nausea, vomiting, difficulty with their vision, and difficulty with walking especially with head movements. It is not understood why some patients have all of the above symptoms and others only have a few. Time to recovery of function can vary from person to person, suggesting that there are many factors that affect recovery of function. Patients seem to recover from (i.e., compensate for) unilateral vestibular loss through movement, possibly via the brain’s ability to suppress the aberrant signal from the involved ear and the uncontrolled excitation from the intact ear. Central nervous system plasticity seems the most likely basis of recovery. For example, with a unilateral vestibular abnormality, vestibulo-ocular reflex (VOR) gain partially recovers over time, though never reaching its pre-lesion function, especially at high velocities of head movement (Curthoys & Halmagyi, 1995). A study by Bowman supports the concept of only partial recovery in persons with vestibular disorders; persons who have compensated well for a unilateral vestibular disorder continued to have functional deficits when queried (Bowman, 2004). Disorders of the cerebellum affect recovery. An intact cerebellar flocculus is important for vestibular adaptation to occur (Furman, Balaban, & Pollack, 1997). Vestibular adaptation is thought to be context specific (Zee, 2000); hence, exercise is often performed in various positions and in different environmental contexts and velocities. Smooth pursuit most likely stabilizes gaze at slower speeds. An error signal induces vestibular adaptation via slipping of the image on the retina during head movement (Zee, 2000). Visual stimulation appears to be critical for adapting the dynamic VOR. Zee (2000) reports that there is no increase in VOR gain if the person is not exposed to light. Beyond light exposure and movement, there is

some emerging evidence of neural “rewiring” within the central nervous system (CNS) after insult. The concept of neural sprouting (a form of plasticity) as a result of the sensory experiences from movement after a vestibular insult has been postulated as a mechanism for recovery (Dieringer, 1995). Sensory substitution is used to aid in the rehabilitation process (Hall et al., 2016). Patients are taught to use vision, somatosensation, and the signals remaining from the intact labyrinth to aid in the recovery process. Patients are instructed to use predictive saccades and the visual pursuit system to compensate for bilateral vestibular loss. Through practice, patients can learn to increase smooth pursuit gain (Herdman, 1998) or to generate saccades to decrease the visual blurring that occurs with fast head movements (Berthoz, 1988; Schubert & Zee, 2010). The cervico-ocular reflex (COR) — that is, eye movements elicited by changes in the position of the head on the torso — is sometimes utilized to attempt to substitute for the loss of VOR function, even though it appears that not all people may be able to utilize this reflex response (Schubert, Das, Tusa, & Herdman, 2004; Schubert & Minor, 2004). Schubert et al. (2004) have suggested that the COR may be adaptable with exercise training in some people with vestibular dysfunction. Age and sex do not appear to affect vestibular compensation (Herdman, Schubert, Das, & Tusa, 2003; Topuz et al., 2004; Whitney, Wrisley, Marchetti, & Furman, 2002). Length of symptoms also does not appear to affect the ultimate outcome in persons with unilateral vestibular hypofunction (Herdman et al., 2003). Generally, it is thought that people with peripheral vestibular disorders will have a better outcome than those with central vestibular disorders, especially disorders of the cerebellum, which is critical for VOR function (Brown, Whitney, Marchetti, Wrisley, & Furman, 2006; Furman & Whitney, 2000). Factors that appear to affect compensation abilities resulting in a negative outcome include a history of migraine (Wrisley, Whitney, & Furman, 2002), a history of anxiety and/or depression (Bowman, 2004), being younger (Bowman, 2004; Herdman, Blatt, Schubert, & Tusa, 2000; Whitney, Hudak, & Marchetti, 2000), cerebellar dysfunction (Brown et al., 2006), visual impairments (Herdman, 2000; Luxon, 2003), decreased distal sensation (Herdman, 2000; Whitney & Rossi, 2000), head injury (Davies & Luxon, 1995; Kentala, Viikki, Pyykko, & Juhola, 2000; Rubin, Woolley, Dailey, & Goebel, 1995; Shepard, Telian, Smith-Wheelock, & Raj, 1993; Whitney & Unico, 2001), intermittent symptoms (Clendaniel & Tucci, 1997; Herdman, 2000; Whitney &



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Rossi, 2000), progressive vestibular dysfunction (Whitney & Rossi, 2000), medical comorbidities (Shepard & Telian, 1993; Telian & Shepard, 1996; Whitney & Unico, 2001), vestibular suppressant medication (Bamiou et al., 2000; Herdman, 2000; Peppard, 1986), and physical restriction of daily activities (Fetter & Zee, 1988; Gustave et al., 1998; Lacour, Roll, & Appaix, 1976; Luxon, 2003). Table 24–2 presents additional reasons for negative outcomes. Youth as a negative predictive factor appears to be counterintuitive. It has been suggested that persons who are younger and seen in a vestibular clinic are more impaired than their older counterparts (Whitney, Hudak, et al., 2000) and that they may have higher expectations for recovery (Bowman, 2004). VOR gain can be significantly impaired after a vestibular disorder. Vertical VOR gain has been reported to be decreased by as much as 66%, whereas horizontal VOR gain was reduced by 50% toward the involved side and 25% toward the noninvolved side of Table 24–2. Negative Predictive Factors Related to Rehabilitation Outcomes • A history of an ocular motor tropia or phoria • A history of migraine (even a remote history) • Ankylosing spondylitis • Charcot-Marie Tooth disease • Coexisting neurologic dysfunction (visual field loss, ptosis, cognitive impairment, spasticity) • Convergence insufficiency • Convergence spasm • Involvement of the contralateral labyrinth • Diabetes • Externally restricted cervical range of motion (four-poster collar) • Fluctuating vestibular functioning • Glaucoma • Macular degeneration • Medication (certain CNS depressants) • Myopathy that results in loss of distal muscle strength • Parkinson disease • Peripheral neuropathy • Inactive lifestyle • Visual aids (progressive or trifocal lenses, monocular contact lenses)

the vestibular dysfunction (Allum, Yamane, & Pfaltz, 1988). Even after rehabilitation, dynamic gain deficits remain (Curthoys & Halmagyi, 1995). Bowman (2004) suggests that people who are well compensated continue to have some remaining functional limitations that adversely affect their lives.

Evidence That Exercise Can Help Persons with Peripheral and Central Vestibular Disorders The evidence appears clear that function improves following vestibular rehabilitation for persons with unilateral hypofunction (Clendaniel & Tucci, 1997; Cohen, John, Yakushin, Buettner-Ennever, & Raphan, 2002; H. Cohen, 1992, 1994; Cohen, Ewell, & Jenkins, 1995; H. Cohen, Kanewineland, Miller, & Hatfield, 1995; H. S. Cohen & Kimball, 2003, 2004a, 2004b; Corna et al., 2003; Cowand et al., 1998; Gill-Body, Krebs, Parker, & Riley, 1994; Herdman, 1990; Herdman, Blatt, & Schubert, 2000; Herdman, Clendaniel, Mattox, Holliday, & Niparko, 1995; Herdman et al., 2003; Horak et al., 1992; Krebs et al., 1993; Mruzek, Barin, Nichols, Burnett, & Welling, 1995; Norre, 1984; Norre & Beckers, 1988; Pavlou et al., 2004; Shepard & Telian, 1995; Shepard, Telian, & Smith-Wheelock, 1990; Shepard et al., 1993; Strupp, Arbusow, Maag, Gall, & Brandt, 1998; Szturm, Ireland, & Lessing-Turner, 1994; Telian & Shepard, 1996; Topuz et al., 2004; Whitney & Rossi, 2000; Yardley, Beech, Zander, Evans, & Weinman, 1998; Yardley, Burgneay, Andersson, et al., 1998; Yardley, Burgneay, Nazareth, & Luxon, 1998; Yardley et al., 2004). Persons with vestibular hypofunction are the best studied group, because they are more homogeneous than persons with central vestibular disorders. There is no consensus in the literature as to what is the best way to treat vestibular hypofunction. Treatment lengths vary from 4 to 12 weeks. The longer treatment times are primarily for persons with bilateral vestibular hypofunction or for persons with significant comorbid medical disorders, space and motion symptoms, or psychiatric symptoms associated with their dizziness. There is little evidence that persons with central vestibular disorders can be aided with vestibular rehabilitation (Furman & Whitney, 2000). A recent pilot randomized trial suggests that rehabilitation is effective with older adults with central vestibular disorders (Marioni et al., 2013) and with persons poststroke in the vertebro-basilar circulation (Balci, Akdal, Yaka, & Angin, 2013). Studies of persons with head trauma,

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cervical dizziness, cerebellar disorders, anterior inferior cerebellar artery and posterior inferior cerebellar artery stroke, and migraine have reported beneficial results following vestibular rehabilitation (Brown et al., 2006; Cohen, 1992; Cohen, Kanewineland, Miller, & Hatfield, 1995; Cowand et al., 1998; Gill-Body, Popat, Parker, & Krebs, 1997; Karlberg, Magnusson, Malmstrom, Melander, & Moritz, 1996; Rubin et al., 1995; Shepard & Telian, 1995; Suarez et al., 2003; Whitney & Unico, 2001; Whitney, Wrisley, et al., 2000; Wrisley, Sparto, Whitney, & Furman, 2000; Wrisley et al., 2002). Treatment lengths vary for persons with central vestibular disorders, but generally these patients are more difficult to treat and require more time for optimal rehabilitation outcomes. Those with central vestibular disorders have a better prognosis than those with combined peripheral and central vestibular disorders. Persons with cervical dizziness are often co-treated with physical therapy specifically for the neck, as it is not uncommon for a person’s dizziness to persist until her/his neck pain resolves. However, there is no strong evidence that manual therapy and vestibular rehabilitation in combination is superior to either intervention alone (Lystad, Bell, Bonnevie-Svendsen, & Carter, 2011). When considering an exercise program, patient safety is of optimal importance. Encouragement is essential, as patients do not like to make themselves dizzy. Experience in treating patients with vestibular disorders may make a difference in a patient’s outcome, as it is sometimes difficult to know how much exercise is excessive. Our general rule is that patients should not have symptoms for longer than 20 min after they complete their exercise program. Patients are strongly encouraged to bring on their symptoms during the exercises, although for some patients this is very difficult. Fear of dizziness can become a problem with persons with chronic symptoms, as patients begin to avoid activities or situations that provoke their symptoms. Computerized dynamic posturography (CDP), dizziness, fear of falling, balance confidence, selfefficacy, quality of life, anxiety, static postural measures, number of falls, gait measures, dynamic visual acuity, VOR gain, and the ability to perform transitional movements have all been shown to improve following rehabilitation (Brown, Renwick, & Raphael, 1995; Brown et al., 2001, 2006; Cohen, Heaton, Congdon, & Jenkins, 1996; Cohen, Kanewineland, et al., 1995; Cohen & Kimball, 2003, 2004b, 2005; Cohen, Kimball, & Stewart, 2004; Gill et al., 2002; Gill-Body & Krebs, 1994; Gill-Body et al., 1994, 1997; Herdman, 1990, 1995, 1997, 2000, 2003; Shepard & Telian, 1995; Shepard et al.,

1990, 1993; Szturm et al., 1994; Vitte, Semont, & Berthoz, 1994; Whitney et al., 2000; Whitney & Rossi, 2000; Whitney, Sparto, et al., 2006).

The Vestibular Evaluation History The most important aspect of the vestibular evaluation is the patient history. The patient usually can provide enough information by the end of the history to positively identify what the diagnosis is if the correct questions are asked. In order to standardize the questions, forms are used to assist the clinician in gaining a better understanding of the patient’s medical comorbidities and additional factors that may affect the dizziness. The data from the forms can speed up history taking and allow for more probing questions based on the already completed intake forms. The questions that are answered can guide additional queries by the clinician that can assist in determining patient diagnosis. In addition to the health intake forms, it is very important to ask specific questions about whether headache is related to the patient’s dizziness symptoms. Migraine is highly prevalent and is much more common in women than men. Most studies suggest that the vestibular population is approximately 60% to 65% women, suggesting that migraine may be a contributing factor in the high proportion of persons with vestibular disorders. It is not uncommon for persons with migraine headache to present with dizziness, vertigo, and space and motion symptoms as presenting complaints to an otology clinic (Cass et al., 1997; Neuhauser, Leopold, von Brevern, Arnold, & Lempert, 2001; Whitney et al., 2000). Migraine has been shown to be a negative predictor of recovery after vestibular rehabilitation, even with a remote history of migraine (Wrisley et al., 2002). Patients often report that they get sinus headaches or head pressure, without ever having had the diagnosis of migraine prior to attending a vestibular clinic. A history of the person’s falls is very important. Persons with vestibular disorders fall more frequently than others in the community (Herdman et al., 2000; Kristinsdottir, Jarnlo, & Magnusson, 2000; Murray, Hill, Phillips, & Waterston, 2005; Whitney, Hudak, et al., 2000; Whitney, Marchetti, Schade, & Wrisley, 2004; Whitney, Marchetti, & Schade, 2006). Determining the cause and circumstances surrounding the fall as well as whether there was any injury is an important part of



the history. Some causes of falls may require immediate medical notification, such as syncope, which is clearly not associated with a vestibular disorder. The area of assessment of falls risk is addressed in Chapter 25.

Physical Examination Strength, range of motion, and sensation are assessed to determine if they are negative factors that will affect recovery. Lower extremity weakness will affect the person’s ability to move, which is very important for vestibular compensation. In addition, it is very important to have adequate neck and foot range of motion. Neck range of motion will affect the ability of the person to compensate, and foot range of motion will affect the ability of the lower extremities to assist with compensation through increased weighting of somatosensation for postural control. Persons who have poor sensation distally fall frequently (Hughes, Duncan, Rose, Chandler, & Studenski, 1996; Lord & Clark, 1996; Maki, Perry, Norrie, & McIlroy, 1999; Marchetti & Whitney, 2005; Richardson & Ashton-Miller, 1996; Richardson, Ashton Miller, Lee, & Jacobs, 1996), only adding to the dysfunction associated with inadequate vestibular function. The typical oculomotor examination includes assessing motor performance of cranial nerves III, IV, and VI and an assessment of spontaneous nystagmus. In addition, gaze-evoked nystagmus is assessed. Typically, smooth pursuit and saccades are assessed visually for any major disruption in function. Patients are asked to follow a moving target and to quickly move their eyes from one target to another. In addition, vergence is assessed by asking the patient to follow a target moved toward the nose. Vergence is more difficult for older adults, but they should be able to follow the finger for at least part of the motion. With infrared (IR) goggles, the therapist will determine if the patient has a positive Dix–Hallpike test as well as determine if there is any nystagmus at rest without fixation. If the patient can fixate with no nystagmus in room light but has spontaneous nystagmus with IR goggles in place, it suggests a peripheral vestibular disorder. An inability to suppress nystagmus while fixating on a target with eyes open could indicate either an acute peripheral vestibular disorder or a central vestibular disorder. Head-shaking nystagmus is also assessed whereby the head is rotated in about 20 to 30 degrees of flexion (Hain, Fetter, & Zee, 1987). The head is rotated quickly to the right and left with IR goggles in place, and after approximately 20 head shakes the movement is

24. Vestibular Rehabilitation

stopped and the examiner visualizes any nystagmus and describes it. A normal response is no nystagmus when the motion is stopped by the examiner. The head impulse test is performed without goggles in order to assess the semicircular canals (Halmagyi & Curthoys, 1988). The person’s head is moved quickly either toward neutral (nose straight ahead) or away from neutral approximately 10 to 20 degrees while the patient focuses on an object in front of him or her. If the eyes are unable to maintain on the fixation point and one or more saccades are visualized, a peripheral vestibular disorder is suspected (Halmagyi & Curthoys, 1988; Kattah, Talkad, Wang, Hsieh, & Newman-Toker, 2009). Dynamic visual acuity is assessed while viewing an eye chart (Herdman et al., 2003; Herdman, Schubert, & Tusa, 2001; Rine & Braswell, 2003). The therapist first determines the patient’s static visual acuity. Then, the patient’s head is moved at approximately 2 Hz to the right and left while the patient is asked to read the letters on the chart. A drop of more than two lines often indicates a vestibular disorder. Improvement in dynamic visual acuity has been recorded after rehabilitation (Herdman et al., 2003). At the end of the oculomotor examination, the Dix–Hallpike maneuver is performed to determine if the patient has BPPV. Extremes of neck extension or rotation are avoided. Tests are also performed to determine if the patient has horizontal canal BPPV (see Chapter 11 for specifics about testing and treatment). Baseline data for the above are recorded and used for comparison at discharge. In addition, balance and gait data are collected to determine if there is any change over time.

The Vestibular Exercise Program Exercises are incorporated that attempt to enhance remaining vestibular, somatosensory, or visual functioning in persons with vestibular disorders. The most common diagnostic categories seen in physical therapy that have demonstrated positive change after vestibular rehabilitation are shown in Table 24–3. The most commonly provided vestibular exercise is VOR × 1 for people with vestibular dysfunction, whereby the person is asked to focus on a target while moving the head in either the pitch or the yaw plane. The VOR × 1 exercise is advanced by changing the backgrounds, the speed of the movement of the head, and the position of the patient. It is very important that

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Table 24–3. Diagnostic Groups That Have Improved After Vestibular Rehabilitation • AICA and PICA stroke • Anxiety-related dizziness • Benign paroxysmal positional vertigo • Bilateral hypofunction • Cerebellar disorders • Cervical vertigo • Head trauma • Labyrinthitis • Mal de debarquement • Ménière’s disease • Migraine dizziness • Multiple sclerosis • Multisensory disequilibrium • Neuronitis • Panic disorder with agoraphobia and dizziness • Postacoustic schwannoma • Posttraumatic dizziness (postconcussion disorders • Unilateral hypofunction

the patient always have the target in focus as he or she performs the exercise. Once VOR × 1 is mastered, the patient is often asked to perform VOR × 2, which is more difficult than VOR × 1. The head always goes in the opposite direction as the target is held at arm’s length, while the eyes remain focused on the target. The exercise requires a fair amount of coordination and intellect, so some patients are never able to perform it. More recently, equipment such as disco balls and virtual reality have been used to improve dizziness and function in persons with head trauma and those with uncompensated peripheral vestibular disorders (Garcia et al., 2013; Gottshall, Sessoms, & Bartlett, 2012; Llorens, Colomer-Font, Alcaniz, & Noe-Sebastian, 2013; Meldrum et al., 2012; Pavlou et al., 2012; Sparto, Furman, Whitney, Hodges, & Redfern, 2004; Sparto, Whitney, Hodges, Furman, & Redfern, 2004; Viirre, 1996; Whitney, Sparto, et al., 2006; Whitney, Sparto, Brown, et al., 2001). The equipment seems to be particularly useful in persons who are sensitive to motion in their environment, such as the person who cannot tolerate grocery shopping or going to a shopping mall. Gradual exposure seems to be a key factor in recovery.

Typically, exercises are started in the sitting position and then advanced to standing, then standing in more difficult positions, and finally during gait on flat surfaces progressing to gait on more unstable support surfaces. There is always a risk of the patient falling, so the therapist must be careful to avoid injury to the patient. Exercises should be written down and demonstrated to the patient. Pictures are ideal, as most patients forget what was said to them in the clinic and come back after practicing doing “novel” exercises, as they may not have fully understood the instructions. Exercises are provided to patients to attempt to enhance their somatosensation. Novel somatosensory devices are being employed to attempt to substitute for vestibular loss, including a vibrotactile vest (Honegger, Hillebrandt, van den Elzen, Tang, & Allum, 2013; Peterka, Wall, & Kentala, 2006; Sienko, Balkwill, Oddsson, & Wall, 2013; Wall, Oddsson, Horak, Wrisley, & Dozza, 2004) and vibrating insoles (Galica et al., 2009; Priplata, Niemi, Harry, Lipsitz, & Collins, 2003; Priplata et al., 2006). Exercises are performed in sitting and standing positions with the goal of having the person reweigh somatosensory inputs for enhanced postural control. Standing weight shifts with emphasis on “feeling” the feet with eyes open and closed. Patients are asked to roll balls under their feet in sitting with eyes closed to better “feel” where the ball is and to increase intrinsic toe strength. Rocking back and forth on the feet is also encouraged in sitting and standing. Lower extremity strengthening is always encouraged. Patients are asked to perform strengthening exercises in standing as much as possible, as most patients have difficulty with their balance in standing or walking rather than sitting. It is always important to ask the patient to increase his or her activity level, especially with walking. A walking program is encouraged for all patients in safe environments progressing to more difficult circumstances. One should avoid uneven terrain if the patient falls on the modified Clinical Test of Sensory Interaction and Balance (mCTSIB) with eyes open on a foam surface (see the detailed description of this assessment later in this chapter). If the patient is very impaired, walking in the house with a finger against the wall may help to provide additional proprioceptive input and steady the person’s gait pattern (Jeka, 1997). Obviously, the patient will be weaned from the wall as soon as possible and will be progressed to more difficult circumstances and environments. Walking in a grocery store is one of the most difficult activities for persons with vestibular disorders (Whitney et al., 2001). Standing on uneven surfaces, mini-tramps, or a piece of foam with eyes open are all methods used to



24. Vestibular Rehabilitation

enhance the use of vision. By disturbing proprioceptive inputs, one must use vision to assist with postural control if vestibular inputs are disrupted. Visual inputs are very important for postural control, and when removed make balance much more difficult. Standing with eyes closed on a flat surface usually will cause the somatosensory system to be used extensively, yet when you have the person stand on a foam pad, the patient may have to reweigh sensory inputs and rely more on vestibular inputs. If there is severe vestibular damage, the person may not be able to maintain the position. Thus, all three senses are used in daily activities, and when the vestibular system is disrupted, there is a shift in responsibilities with the other sensors having to work optimally to maintain postural control. Exercises are progressed in an incremental manner and as quickly as possible in order to improve function and return the person to work or play activities. Most people with vestibular disorders are older adults, yet some younger people experience vestibular dysfunction and are often disabled by their symptoms (Luxon, 2003). There is some evidence that, in addition to exercise, persons with vestibular disorders may be helped by behavioral therapy, relaxation/breathing exercises, and environmental modifications (Herdman, 2000; Johansson, Akerlund, Larsen, & Andersson, 2001; Monahan, Sharpe, Drury, Ertl, & Ray, 2002; Schmid, Henningsen, Dieterich, Sattel, & Lahmann, 2011; Siniaia & Miller, 1996; Whitney & Rossi, 2000; Yates, 1996). Patients are treated differently based on their presenting diagnoses and lab findings. Patients who have no remaining VOR, at least as well as we are able to test, are less likely to benefit from VOR exercises. Sensory substitution exercises are advised, especially for persons with bilateral vestibular hypofunction (Gillespie & Minor, 1999; Telian et al., 1991; Whitney & Rossi, 2000). It is very important to know not only the diagnosis, but also the laboratory findings in order to develop a customized exercise program. In one tertiary vestibular clinic, 22% of all the patients seen had a diagnosis of BPPV (Whitney, Marchetti, & Morris, 2005). Benign paroxysmal positional vertigo is often seen in addition to peripheral or central vestibular disorders, and should always be considered as a possibility either as the primary or as a secondary concern. The Dix–Hallpike maneuver should be performed on all patients presenting to the therapist.

Selected Cases Patients with various vestibular pathologies require targeted physical therapy interventions. A few cases

follow to attempt to illustrate how patients are treated differently based on their diagnoses, presenting symptoms, and comorbidities. To better understand the cases, basic rules about the measurement tools are provided. Generally, scores on the Dizziness Handicap Inventory (DHI) of 0 to 30 are considered mild, 31 to 60 are moderate, and >60 indicate severe dizziness (Whitney & Wrisley, 2004). Activities-Specific Balance Confidence (ABC) scores range from 0 to 100, with scores 10″ indicate less risk (Duncan et al., 1992).

Foam Posturography Brandt and colleagues were the first to suggest that standing on foam with eyes open and closed could be used as a form of rehabilitative exercise as well as a measurement tool (Brandt, Krafczyk, & Malsbenden, 1981). They demonstrated improvements in postural sway in control subjects after standing on foam with eyes open and closed with neck extension over a period of five days. They suggested that it could be used for rehabilitation. Different types of foam pads may yield different results, so care should be utilized to test the patient on the same type of foam (Figure 24–1). The Clinical Test of Sensory Interaction and Balance (CTSIB) was later developed based on Brandt et al.’s work (Shumway-Cook & Horak, 1986b) and the work of Nashner (Forssberg & Nashner, 1982; Horak & Nashner, 1986; Nashner, 1982; Nashner, ShumwayCook, & Marin, 1983). The CTSIB consists of six conditions, that is, standing on a flat firm surface and on a compliant foam surface under three different visual circumstances: eyes open, eyes closed, and while wearing a sensory conflict dome with feet together and shoes removed (Shumway-Cook & Horak, 1986a). The CTSIB can also be performed with feet comfortably apart (normal stance width) and with shoes on without a difference in score compared with standing with feet together, shoes removed (Whitney & Wrisley, 2004; Wrisley & Whitney, 2004). The CTSIB is easy to perform, but patients must be closely guarded to ensure that they do not fall. The foam pad must be secure on a firm surface so that it does not slip. Patients have been known to fall getting onto or off the foam pad, so care should be exercised not just during standing. The CTSIB was designed to assess reliance on visual, vestibular, and proprioceptive sensors for postural control. Time to maintain the position (30 s in the original paper) (Shumway-Cook & Horak, 1986b), amount of sway (as assessed with a sway grid) (Shumway-Cook & Horak, 1986b), fall or no fall (Cass et al., 1996), and sway angles (also assessed with a sway grid) (Shumway-Cook & Horak, 1986b) have been used as objective measures of CTSIB performance. The test has been widely used for patients with vestibular disorders (Cohen, Blatchly, & Gombash, 1993; Cohen et al., 1996; el Kashlan et al., 1998; Whit-

Figure 24–1.  When testing or treating patients with vestibular disorders, the thickness of the foam may affect patient performance. High-density foam versus very compliant foam will change patient behavior. All patients should be carefully watched when getting onto the foam, while standing on it, and while getting off the foam pad.

ney & Wrisley, 2004; Wrisley & Whitney, 2004). Testretest reliability of the CTSIB is high, with an r equal to or greater than 0.75 in older, community-living adults (Anacker & Di Fabio, 1992) and an r equal to 0.99 for interrater reliability and test-retest reliability in young adults (Cohen et al., 1993). Weber and Cass (1993) have reported a 90% agreement between the CTSIB and the Sensory Organization Test (SOT; Figure 24–2) of CDP and a 90% sensitivity and 95% specificity in adults with vestibular dysfunction using the foam pad in their office, yet there was no correlation between caloric or rotational chair findings and CTSIB findings (Weber & Cass, 1993). The CTSIB measures something different than what other vestibular findings provide. Performance on the CTSIB has been used to assess fall risk in persons with vestibular disorders (Cohen et al., 1993; el Kashlan et al., 1998; Weber & Cass, 1993),



24. Vestibular Rehabilitation

A Figure 24–2.  A. The person is viewing the virtual scene while standing on a platform that can be manipulated with a keystroke on the computer. Photo courtesy of Dr. Lewis Nashner, Bertec Corporation, Columbus, OH.  continues

older adults (Baloh, Corona, Jacobson, Enrietto, & Bell, 1998; Di Fabio & Seay, 1997; Sherrington & Lord, 1998), as well as persons with peripheral neuropathies (Dickstein, Shupert, & Horak, 2001). The CTSIB was able to identify 63% of older adults who were at risk for falling (Di Fabio & Seay, 1997). The sensory conflict dome is not used as much clinically as when the test was first devised. Wrisley and Whitney (2004) suggested a version of the test called the modified CTSIB (mCTSIB; Figure 24–3), where the dome is not used. The mCTSIB omits Conditions 3 and 6. It was reported by Cohen et al. (Cohen et al., 1993) that there were no differences between Conditions 2 and 3 and between Conditions 5 and 6. Patients who cannot stand on foam with eyes open (Condition 4) are not able to walk safely on

uneven surfaces, such as sand or gravel. Those who cannot stand on foam with eyes closed should not walk in the dark, especially on uneven surfaces. Having difficulty with Condition 4 is very common in older adults. Patients are asked to stand with eyes closed on the foam pad during Condition 5. Generally, persons with peripheral vestibular hypofunction fall on Conditions 5 and 6, although not always, if they are well compensated (Herdman, 2000). Even persons with decreased bilateral hypofunction may be able to stand during Condition 5 if they are well compensated (Brown et al., 2001; Telian et al., 1991). Condition 6 is the most difficult task, as conditions are ranked in hierarchical order, with Condition 1 the easiest and Condition 6 the hardest to accomplish. The

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B Figure 24–2.  continued  B. SOT results can help determine how to treat the patient. Most patients with vestibular disorders fall on Conditions 5 and 6. Patients who fall under Conditions 4 through 6 have a surface-dependent pattern. With exercise and movement, SOT scores can be improved. The use of SOT can be used to quantify change over time in persons with vestibular disorders. From NeuroCom International, Inc.

test involves standing with the visual dome in place while on the foam with eyes open. Sway is usually the greatest during Condition 6, although Cohen et al. found little difference in CTSIB 5 and 6 scores when

tested with young and older adults, and persons with vestibular dysfunction (Cohen et al., 1993). Typically, persons with unilateral vestibular hypofunction fall on both Conditions 5 and 6.

Figure 24–3. The modified Clinical Test of Sensory Interaction and Balance (mCTSIB) consists of four tests: standing on a solid surface eyes open and closed, and standing on a compliant surface eyes open and closed. 565

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Biomechanical constraints can affect the performance of the patient (Horak, 1987). Persons who have limited ankle range of motion, those with pain, or those with decreased strength or endurance will have their scores on the CTSIB affected because of physiologic constraints that are not related to their visual, vestibular, or proprioceptive systems.

Computerized Dynamic Posturography The SOT of the EquiTest™ (see Figure 24–2A) is a device that has often been used to quantify postural control. In addition to the SOT, the EquiTest device also includes a motor control test, whereby the floor is moved quickly forward or backward and pitches up and down at different speeds around the patient’s ankle joint while load sensors detect forces exerted by the feet. The SOT cannot be used to make a definitive diagnosis of vestibular dysfunction, nor can the CTSIB, although the SOT is often used to corroborate other physical examination findings. Scores on the CTSIB have been shown to moderately correlate with the SOT of CDP (el Kashlan et al., 1998; Weber & Cass, 1993). The six conditions are virtually the same, but instead of a visual conflict dome, the SOT incorporates a three-sided visual surround. During the SOT, there are combinations of the floor being sway-referenced and the walls being sway-referenced, providing a strong stimulus. The CDP attempts to isolate various aspects of postural controls, that is, reliance on visual, somatosensory, or vestibular information. Scores on the SOT can help to plan the treatment intervention, have been related to fall history, and provide objective data that can be used to assess change over time (Black, Angel, Pesznecker, & Gianna, 2000; Whitney, Marchetti, et al., 2006). O’Neill, Gill-Body, and Krebs (1998) reported improvements in the SOT score over time with patients with vestibular hypofunction undergoing vestibular rehabilitation, yet there was not a correlation between changes in functional performance and the SOT change scores. The relationship between the SOT of CDP and falls risk is somewhat controversial (Girardi, Konrad, Amin, & Hughes, 2001; Whitney, Marchetti, et al., 2006). Girardi et al. (2001) and Whitney, Marchetti, et al. (2006) report that the SOT is helpful in identifying persons who are at risk for falling. Improvements in SOT scores and fewer falls during the SOT have been reported by Black et al. at the end of an episode of care consisting of an individualized vestibular rehabilitation program (Black et al., 2000). Recurrent fallers had significantly lower SOT scores than those who were one-

time fallers or those who did not report a fall (Whitney, Marchetti, & Schade, 2006). Those patients who scored less than 38 on the SOT composite were 4.1 times more likely to be recurrent fallers (Whitney, Marchetti, et al., 2006). Tinetti and Williams (1997) have suggested that community-living older adults who fall are more likely to be admitted to long-term care facilities. As a result, some older adults may not be completely honest when they report their frequency of falling, and objective testing may be helpful.

Gait Assessment Gait Speed The most acceptable measure of gait performance is gait speed (Guralnik et al., 2000; Studenski et al., 2011). Changes in older adults of 0.1 m/s are considered clinically significant (Perera et al., 2006). The slower an older adult ambulates, the greater his or her risk of falling (Guralnik et al., 2000). Using a value of 0.56 m/s as a lower limit of normal, Van Swearingen and colleagues identified a sensitivity of 72% and a specificity of 74% in frail older adults for recurrent falls (Van Swearingen, Paschal, Bonino, & Chen, 1998). Normal walking speed to cross a signaled intersection is 1.27 m/s in young adults (Hoxie & Rubenstein, 1994). The speed of older adults crossing an intersection was reported at 0.86 m/s, with 27% of the older adults not reaching the other side of the road before the light changed at the intersection (Hoxie & Rubenstein, 1994). Vestibular disorders generally slow gait speed, making functional mobility in the community even more difficult for older persons. Patients with vestibular disorders are often asked to walk at different speeds to determine if they can accelerate or decelerate upon command. Patients with vestibular dysfunction have a tendency to walk with little trunk or head rotation, especially during turning. This “stiff gait” is classic of persons with vestibular disorders. Walking in busy environments around many people and in environments where there is high visual contrast (stripes, checkered floors) will make ambulation much more difficult for persons with vestibular disorders (Bowman, 2004; Bronstein, 2004). In fact, some patients may completely avoid such environments. Patients with significant space and motion symptoms may become ill in the above circumstances (Bowman, 2004; Jacob, Furman, & Balaban, 1996; Jacob, Furman, & Perel, 1996; Jacob et al., 1993). After one or two exposures, some patients will avoid going out to stores and



large social events to avoid feeling ill (Bowman, 2004). This avoidance behavior can lead to significant functional deficits (Bowman, 2004).

Timed “Up and Go” Test Another commonly used tool to assess progress over time is the TUG (Podsiadlo & Richardson, 1991). The tool was developed for use with frail older adults and it is one of the best validated tests used to assess balance during gait. Examiners ask patients to rise from a chair, walk 3 m, turn around, and come back and sit down in a chair. They can use the armrests to rise from the chair and are also permitted to use an assistive device. The TUG has been used to assess change over time in persons with vestibular disorders (Gill-Body, Beninato, & Krebs, 2000; Whitney et al., 2000; Whitney, Marchetti, et al., 2004; Whitney & Rossi, 2000; Whitney, Sparto, et al., 2006; Whitney, Wrisley, et al., 2000, 2004, 2005) and is often used to assess fall risk (Bischoff et al., 2003; Cohen & Kimball, 2004b; Di Fabio & Seay, 1997; Dite & Temple, 2002; Newton, 1997; Rockwood, Awalt, Carver, & MacKnight, 2000; Shumway-Cook, Brauer, & Woollacott, 2000). It has also been reported to be related to difficulty performing activities of daily living (Pod­ siadlo & Richardson, 1991). The test-retest reliability of the TUG test has been reported as r = 0.99 in community-dwelling older adults with multiple comorbidities (Podsiadlo & Richardson, 1991). With increasing age, TUG scores increase (Medley & Thompson, 1997) and increase by the use of a walking aid (Medley & Thompson, 1997; ShumwayCook et al., 2000). The height of the chair used will also affect TUG performance (Siggeirsdottir, Jonsson, Jonsson, & Iwarsson, 2002), with lower chairs making it more difficult for persons to perform the test, resulting in increased (worse) TUG scores. Standardization of procedures is very important for consistent results with the TUG. One should use the same chair each time and be consistent with the instructions. The voice command is important. Podsiadlo and Richardson (1991) suggested that the test be performed at the person’s comfortable speed. If the examiner speaks loudly, the person is more likely to ambulate as quickly as possible, making comparisons between visits more difficult. In older adults, scores of >13.5 s on the TUG test have been related to fall risk (Shumway-Cook et al., 2000). Persons with vestibular disorders who scored >13.5 s to perform the TUG were 3.7 times more likely to have reported falling within the last six months (Whitney, Marchetti, et al., 2004). Patients with scores

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>11.1 s were five times more likely to have reported a fall in the last six months (Whitney, Marchetti, et al., 2004), suggesting that the TUG is a very useful tool to assess fall risk in persons with vestibular disorders. Whitney et al. have reported that the TUG scores of persons with vestibular disorders were like healthy people in their 80s (Steffen, Hacker, & Mollinger, 2002; Whitney, Marchetti, et al., 2004). Healthy men and women in their 70s often score between 8.5 and 9 s on the TUG (Podsiadlo & Richardson, 1991), suggesting that patients with vestibular disorders have significant gait impairment, as the mean TUG score of a cohort of persons with vestibular disorders was 12 s (Whitney, Marchetti, et al., 2004).

Dynamic Gait Index The DGI was developed to record dynamic gait performance (Shumway-Cook & Woollacott, 1995). Shumway-Cook and Woollacott first published the tool in their textbook (Shumway-Cook & Woollacott, 1995). It has been used in persons with vestibular disorders to record change over time in their dynamic gait (Brown et al., 2006, 2001; Hall, Schubert, & Herdman, 2004; Whitney, Wrisley, et al., 2000). The DGI consists of eight walking tasks including: (1) walking, (2) walking at different speeds, (3) walking with yaw head movements, (4) walking with pitch head movements, (5) walking over objects, (6) walking around objects, (7) walking, turning, and stopping quickly on command, and (8) walking up and down steps. The DGI takes about 5 to 10 min to complete and provides the clinician with information about fall risk. Scores of ≤19 on the DGI have been related to fall risk in persons with vestibular disorders (Hall et al., 2004; Whitney, Hudak, et al., 2000; Whitney, Marchetti, et al., 2004). The functional gait assessment (FGA) is more sensitive to change than the original DGI (Marchetti & Whitney, 2006; Marchetti, Lin, Alghadir, & Whitney, 2014). Marchetti and Whitney developed a fouritem DGI that appears to provide similar data to the eight-item DGI, but takes half of the time (Marchetti & Whitney, 2006). The four-item DGI consists of the following items: walking on a level surface, walking with changes of speed, and walking with head movements in the pitch and yaw planes. The DGI-4 had slightly higher sensitivity and specificity than the eight-item DGI for identifying persons who had reported one fall (Marchetti & Whitney, 2006). Recently, a modified version of the original DGI was developed to expand the capabilities of the test (Shumway-Cook, Taylor, Matsuda, Studer, & Whetten, 2013).

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Summary Graded balance and eye/head exercises help patients with vestibular disorders recover from the vestibular insult. Movement is key to functional recovery. Recovery most likely occurs as a result of plasticity within the nervous system. Patients must be encouraged to move after a vestibular disorder. There is clear evidence that balance function in people with peripheral vestibular disorders can be enhanced by rehabilitation. There is less evidence available about functional changes in persons with central vestibular disorders. The central vestibular group is much more difficult to study as they are a very heterogeneous group. There is emerging evidence to support vestibular rehabilitation for persons with central vestibular disorders.

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Yardley, L. (1994). Contribution of symptoms and beliefs to handicap in people with vertigo — a longitudinal study. British Journal of Clinical Psychology, 33, 101–113. Yardley, L., Beech, S., Zander, L., Evans, T., & Weinman, J. (1998). A randomized controlled trial of exercise therapy for dizziness and vertigo in primary care. British Journal of General Practice, 48(429), 1136–1140. Yardley, L., Burgneay, J., Andersson, G., Owen, N., Nazareth, I., & Luxon, L. (1998). Feasibility and effectiveness of providing vestibular rehabilitation for dizzy patients in the community. Clinical Otolaryngology and Allied Sciences, 23(5), 442–448. Yardley, L., Burgneay, J., Nazareth, I., & Luxon, L. (1998). Neuro-otological and psychiatric abnormalities in a community sample of people with dizziness: A blind, controlled investigation. Journal of Neurology, Neurosurgery, and Psychiatry, 65(5), 679–684. Yardley, L., Donovan-Hall, M., Smith, H. E., Walsh, B. M., Mullee, M., & Bronstein, A. M. (2004). Effectiveness of primary care-based vestibular rehabilitation for chronic dizziness. Annals of Internal Medicine, 141(8), 598–605. Yardley, L., Luxon, L. M., & Haacke, N. P. (1994). A longitudinal study of symptoms, anxiety and subjective well-being in patients with vertigo. Clinical Otolaryngology, 19(2), 109–116. Yardley, L., Masson, E., Verschuur, C., Haacke, N., & Luxon, L. (1992). Symptoms, anxiety and handicap in dizzy patients: Development of the Vertigo Symptom Scale. Journal of Psychosomatic Research, 36(8), 731–741. Yardley, L., & Putman, J. (1992). Quantitative analysis of factors contributing to handicap and distress in vertiginous patients: A questionnaire study. Clinical Otolaryngology and Allied Sciences, 17(3), 231–236. Yardley, L., & Redfern, M. S. (2001). Psychological factors influencing recovery from balance disorders. Journal of Anxiety Disorders, 15(1–2), 107–119. Yates, B. J. (1996). Vestibular influences on the autonomic nervous system. Annals of the New York Academy of Sciences, 781, 458–473. Yates, B. J., Billig, I., Cotter, L. A., Mori, R. L., & Card, J. P. (2002). Role of the vestibular system in regulating respiratory muscle activity during movement. Clinical and Experimental Pharmacology and Physiology, 29(1–2), 112–117. Yates, B. J., & Bronstein, A. M. (2005). The effects of vestibular system lesions on autonomic regulation: Observations, mechanisms, and clinical implications. Journal of Vestibular Research, 15(3), 119–129. Zee, D. S. (2000). Vestibular adaptation. In S. J. Herdman (Ed.), Vestibular rehabilitation (2nd ed., pp. 77–87). Philadelphia, PA: F. A. Davis.

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25 The Aging Vestibular System: Implications for Rehabilitation Dara Meldrum and Courtney D. Hall

Introduction The incidence of dizziness and vertigo increases considerably with age. In a large random sample of over 2,000 participants, 33% of those over 70 years of age responded affirmatively when asked whether they were “troubled by vertigo, dizziness, disturbed balance or general unsteadiness,” and this number rose to 50% in those over 80 years (Jonsson, Sixt, Landahl, & Rosenhall, 2004). The course of recovery and subjective experience of symptoms associated with vestibular disorders in older adults differs from those of younger adults. Due to concomitant increased incidence of comorbidities, polypharmacy, and age-related sensory loss across visual, proprioceptive, and hearing systems, the underlying contributors to dizziness, vertigo, and imbalance are multifactorial in older populations and not always vestibular in origin. In older adults presenting to family doctors, pre-syncope is the most common cause of dizziness, followed by medication and then peripheral vestibular dysfunction. Furthermore, the majority of older adults have multiple causes for their dizziness (Maarsingh et al., 2010) and in a small minority, the causes are unidentifiable (Katsaraks, 1994). In those over 70 years of age, the one-year prevalence of vertigo that is vestibular in origin has been estimated at 8.8%, almost double that of the general adult population (Neuhauser et al., 2005). Additionally, the one-year prevalence of benign paroxysmal positional vertigo (BPPV) is almost seven times higher in those over age 60 compared with 18- to 39-year-olds (Von Brevern et al., 2007).

Older adults are likely to have undiagnosed vestibular abnormalities (Jacobson, McCaslin, Grantham, & Piker, 2008; Oghalai, Manolidis, Barth, Steward, & Jenkins, 2000) resulting in a longer duration of symptoms before diagnosis (Lawson, Johnson, Bamiou, & Newton, 2005; Pollak, Kushnir, Shpirer, Zomer, & Flechter, 2005). In one study, 80% of elderly individuals referred to a falls clinic with unexplained falls were found to have unidentified vestibular impairment on laboratory vestibular function testing. Furthermore, only 32% of the older adults reported vertigo/dizziness (Liston et al., 2014). Compared with younger adults, older adults are less likely to complain of true vertigo (spinning) and nausea, instead reporting postural unsteadiness or falling (Piker & Jacobson, 2014). Recent onset vestibular pathology in older individuals causes disproportionate effects on balance and gait, in part due to normal age-related deterioration across sensory systems. Recently it has been established that acute unilateral vestibular loss causes more impairment in balance and gait control for individuals over 60 years of age compared with younger adults, and those over 60 exhibit a slower recovery (Scheltinga, Honegger, Timmermans, & Allum, 2016). It is well documented that there is an increase in falls incidence and fall-related injury with increased age. Approximately one-third of community-dwelling individuals 65 years and older fall in a given year (Tromp et al., 2001), with that rate increasing to approximately 42% in individuals 75 years and older (Downton & Andrews, 1991). Overall the rate of fall-related injury is low, with approximately 10% of all falls resulting in

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injury; however, the rate of fall-related injuries rises dramatically with age: the annualized rate in adults 65 to 74 years of age is 55 per 1,000 and in adults 75 years and older is 115 per 1,000, with the injury rate of women being twice that of men (Adams, Martinez, Vickerie, & Kirzinger, 2011; Peel, Kassulke, & McClure, 2002). Of concern is that fewer than half of older fallers report a fall to their physicians; thus, it is incumbent on health care providers to direct the case history to identify falls incidence and fall risk in their older patients (Stevens et al., 2012). There are many contributors to falls, including but not limited to gait and balance impairments, lower extremity weakness, and dizziness and vertigo. A systematic review revealed that dizziness/vertigo is a major risk factor for falls and increases the risk of falling twofold (Deandrea et al., 2010). In fact, dizziness is among the most prevalent complaints for which people seek medical help, and the incidence increases with advancing age (Colledge, Wilson, Macintyre, & MacLennan, 1994). Individuals with vestibular deficits demonstrate a greater incidence of falls than their agematched healthy counterparts, and the degree of deficit appears to impact the incidence of falling: individuals with bilateral versus unilateral vestibular hypofunction have a greater incidence of falls (Herdman, Blatt, Schubert, & Tusa, 2000). Dizziness is often related to vestibular dysfunction, which can be treated effectively with vestibular exercises. Most of our knowledge about the role of the vestibular system in postural control is derived from studies of individuals with loss of vestibular function and animal studies. Vestibular pathology, although more severe than age-related changes in vestibular function, provides insight into the contribution of age-related decrements in vestibular function to postural instability. However, two caveats need to be taken into account. Caveat 1: Interpretation of information garnered from studies involving vestibular loss is confounded by the fact that the findings reflect both the loss of vestibular function and the compensation for that loss. Caveat 2: Additionally, until recently vestibular loss was defined by measuring the function of the horizontal semicircular canals only. Thus, studies of people with vestibular loss may be muddled because of remaining otolith or even vertical canal function in some but not all subjects. We are now able to measure the function of the vertical semicircular canals, the saccule, and the utricle using such methods as video head impulse testing (vHIT; see Chapter 14), off-axis rotational testing (OVAR; see Chapter 13), vestibular evoked myogenic potentials (VEMPs; see Chapter 16), and measurement of subjective visual vertical (SVV; see Chapter 13). However,

little is known about differences in postural control in people with loss of horizontal semicircular canal versus otolith organ function and even less about the interaction of vestibular loss and aging. This chapter provides a general review of the effect of aging on the sensory systems contributing to postural stability, the functional impact of VOR functioning on postural control, and the evidence supporting the role of vestibular rehabilitation in the remediation of imbalance and gaze instability in older adults.

Age-Related Changes in the Postural Control System The ability to maintain postural stability under different environmental conditions is critical to the ability to safely perform activities of daily living. Postural control is a sensorimotor process that involves the dynamic interplay among multiple body systems, including the central nervous system and both sensory and musculoskeletal systems (Horak, Wrisley, & Frank, 2009). Postural stability refers to the ability to maintain the center of mass of the body positioned over the small base of support provided by the feet, either of which may be moving. Age-related changes are evident in all of the systems — both sensory and motor — that contribute to postural control (reviewed in the sections below); thus, an accumulation of nonspecific changes distributed across body systems results in a multifactorial problem that requires assessment of, and rehabilitation for, multiple systems.

Age Effects on the Vestibular System Postural stability is a multisensory motor task that depends on reliable input from the vestibular, somatosensory, and visual systems. The vestibular system, particularly the otolith organs, provides important information about self-motion, perception of verticality, and gravity. The two types of vestibular sensory organs (the semicircular canals and otolith organs) contribute to gaze and postural stability. When functioning normally, the vestibulo-ocular reflex (VOR; see Chapter 4) generates eye movements that are equal and opposite to head rotation, which enables images to remain stable on the fovea during head motion and ensures gaze stability during head motion. The otolith organs, the utricle and saccule, sense linear acceleration, head tilt, and gravity. Vestibular input for postural control is modulated via the vestibulospinal reflexes (VSRs; see



25. The Aging Vestibular System: Implications for Rehabilitation

Chapter 4). The lateral vestibulospinal tract receives a majority of input from the otolith organs and cerebellum and aids in tonic contractions of the antigravity muscles in the lower extremities. The VOR is better understood as it is relatively simple and for excitatory input involves a three-neuron arc, whereas the VSR is much more complex, involving inputs from both semicircular canal and otolith organs and multiple connections to neck, trunk, and leg muscles. The effects of aging on the vestibular system are well documented both anatomically and physiologically for all vestibular sensory organs (semicircular canals and otolith organs), although the functional impact of these age-related changes is less well understood (Zalewski, 2015). Morphological studies reveal that sensory hair cells degenerate with age in both the cristae of the semicircular canals as well as the maculae of both otolith organs (Johnsson, 1971; VelazquezVillasenor et al., 2000). In the semicircular canals the rate of hair cell loss is greater for type I versus type II hair cells, but in the otolith organs both cell types are lost at the same rate (Merchant et al., 2000). There is some evidence for sparing of hair cells in the utricle (Gopen, Lopez, Ishiyama, Baloh, & Ishiyama, 2003). A parallel reduction occurs in fibers of the vestibular nerve and the vestibular nuclei, such that the number of vestibular sensory hair cells and nerve cells decrease by approximately 20% to 40% between the ages of 40 and 75 years (Lopez, Honrubia, & Baloh, 1997; Park, Tang, Lopez, & Ishiyama, 2001; Richter, 1980; Rosenhall, 1973). There is evidence that brain activation changes with age such that there is an age-related decline in functional connectivity in the central vestibular pathways and an increase in temporal variability of the functionalMRI blood-oxygen-level dependent imaging signal in response to direct stimulation of the peripheral vestibular end organs via galvanic stimulation (Cyran, Boegle, Stephan, Dieterich, & Glasauer, 2016). Results from physiologic testing of VOR function in terms of age-related changes are mixed. Some studies report a reduced VOR gain during rotatory chair testing at higher velocities in older versus younger subjects (Baloh, Jacobson, & Socotch, 1993), whereas other studies have shown minimal influence of age on the VOR response (Furman & Redfern, 2001; Wall & Black, 1984). Measurement of VOR function at more realistic speeds of head rotation used in vHIT (peak head velocities of 150° to 300°/s) have demonstrated relatively constant VOR gain with age-related declines beginning after 70 to 80 years of age (Li et al., 2015; McGarvie et al., 2015). Mossman and colleagues (2015) estimated that VOR gain declines by 0.012 per decade as age increases from 20 to 80 years.

Examination of utricular otoconia obtained during surgery revealed degenerative changes with advancing age, varying from fissures and surface roughening to fractures and loss of otoconia material (Walther et al., 2014). Age-related reduction in the number of otoconia in the otolith organs has also been identified in postmortem temporal bones (Igarashi, Saito, Mizukoshi, & Alford, 1993). These age-related changes in otoconia may predispose older individuals to BPPV and contribute to the decline of otolith function. Age-related changes to the otolith organs have been consistently demonstrated across studies using VEMP testing. The cervical VEMP (cVEMP), a test of saccular/inferior vestibular nerve function, shows reduced response rates, reduced amplitude, and increased threshold in individuals over the age of 60 (Akin, Murnane, Tampas, & Clinard, 2011; Su, Huang, Young, & Cheng, 2004). Similar age-related reductions in response rates, reduced amplitude, and prolonged latency have been reported for the ocular VEMP (oVEMP), a test of utricular/superior vestibular nerve function (Tseng, Chou, & Young, 2010). Agrawal and colleagues (2012) performed vestibular function testing in a cross-sectional study of healthy older adults and identified age-related declines in both semicircular canal and otolith function. Specifically, they identified the highest proportion of deficits in the semicircular canals, followed by the saccule, and the lowest proportion of decline in the utricle. Vestibular perceptual thresholds (the smallest movement at which an individual perceives it correctly) change with advancing age. Bermúdez Rey et al. (2016) found that vestibular thresholds increased with age for yaw and roll movements and for translations. Translation thresholds were more affected (increased) by age than yaw motion thresholds. Roll tilt thresholds were correlated with the inability to stand on foam with eyes closed (the Romberg foam balance test). The authors postulated that the increased vestibular thresholds could therefore play a role in falls. More recently, Lupo and Barnett-Cowan (2017) investigated agerelated differences in fall perception and found that the perception of the onset of a fall took twice as long in the older group (88 ms versus 44 ms). One of the primary roles of the VOR is to stabilize gaze during head movement. Measurement of visual acuity during head movements provides a functional assessment of gaze stability and can be performed using either clinical or computerized tests. During the dynamic visual acuity (DVA) test the head moves at a predetermined velocity and the target size is systematically decreased. The DVA score is the difference between static visual acuity and visual acuity during

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head movements. The computerized DVA test is a highly reliable test in adults (r = 0.79 to 0.83) (Herdman et al., 1998; Rine et al., 2013). During the computerized gaze stabilization test (GST) the target remains fixed at a predetermined size, and head velocity is systematically increased. The computerized GST has demonstrated fair to good reliability (Ward, Mohammad, Whitney, Marchetti, & Furman, 2010). Both the DVA and GST tests differentiate vestibular patients from normal controls, providing support that these measures give estimates of the VOR contribution to gaze stability (Goebel et al., 2007; Herdman et al., 1998). Furthermore, both DVA and GST tests have demonstrated a significant relationship with age, indicating worse performance with increasing age (Herdman et al., 1998; Honaker & Shepard, 2010; Li et al., 2014; Ward et al., 2010). In a large study, Li, Beaumont, Rine, Slotkin, and Schubert (2014) demonstrated that DVA scores remained stable until middle age and then started to decline at age 50 years.

Age Effects on the Visual System Multiple changes in vision occur with aging. All of the following are reduced: acuity, depth perception, contrast sensitivity, adaptation, and ability to detect motion in the visual field (Elliott, Yang, & Whitaker, 1995; Gilmore, Wenk, Naylor, & Stuve, 1992; Weale, 1975). Visual acuity decreases by 0.01 logMAR per year from the seventh decade on and is weakly correlated with impaired functional balance (Baloh et al., 1993). Additionally, poor visual acuity has been found to predict falls in older adults (Lord, Rogers, Howland, & Fitzpatrick, 1999). Some studies have suggested that visual measures other than static visual acuity (e.g., reduced contrast sensitivity or depth perception) are stronger correlates of impaired postural control (Lord & Dayhew, 2001; Lord & Menz, 2000; Turano, Rubin, Herdman, Chee, & Fried, 1994). For example, in a cohort of community-dwelling older adults (age 63 to 90 years), whereas both visual acuity and contrast sensitivity were individually correlated with postural sway while standing on a compliant surface, in a multiple regression analysis, contrast sensitivity, depth perception, and quadriceps strength were independent predictors of postural sway (Lord & Menz, 2000). Of note, this model explained only 21% of the variance and the authors concluded that other variables such as vestibular function, tactile sensitivity, and strength of other muscle groups were needed to fully explain postural sway. Given the contribution of both motor and sensory systems to balance control, it is to be expected

that more complex models of postural control are needed. Era and colleagues (1996) demonstrated that good visual acuity, vibration sense, strength, and reaction times explained reduced postural sway (i.e., better postural stability) in a large sample of communitydwelling older adults. An increased reliance on vision for postural control is evident by an increased postural sway in older versus younger subjects when proprioceptive information is reduced and the visual environment is modified (Peterka & Black, 1990; Poulain & Guraudet, 2008). Furthermore, when peripheral vision is occluded along with reduced proprioceptive inputs, older adults exhibit more postural sway than young adults (Manchester, Woollacott, Zederbauer-Hylton, & Marin, 1989). Cataracts are common in older adults, and other eye conditions, such as glaucoma and macular degeneration, are associated with increasing age. These diseases can negatively affect postural control. Elderly subjects with visual impairment demonstrate more postural sway during challenging balance tasks than those with no visual impairment (Chen, Fu, Chan, & Tsang, 2012). Studies in healthy older adults show that when vision is blurred experimentally with lenses designed to simulate a cataract, mediolateral instability is observed during stepping up or down, indicating the importance of vision for the control of precision in stepping (Buckley, Heasley, Scally, & Elliott, 2005). Older adults are less able to deal with inaccurate sensory information, suggestive of an inability to integrate and re-weight sensory input centrally and produce an appropriate response (Gauchard, Lion, Perrin, & Parietti-Winkler, 2012; Wade, Lindquist, Taylor, & Treat-Jacobson, 1995). There is evidence that central processing is slowed, leading to longer latencies in postural responses to perturbations, particularly when sensory input is novel (Peterka & Black, 1990; Stelmach, Teasdale, Di Fabio, & Phillips, 1989; Sundermier, Woollacott, Jensen, & Moore, 1996; Woollacott, ShumwayCook, & Nashner, 1986). Not only do older adults sway more in response to visual flow (Haibach, Slobounov, & Newell, 2009; Wade et al., 1995), but the effect of visual flow is amplified in older adults with impaired balance, thus placing them at even greater risk for falls when vision is inaccurate (Sundermier et al., 1996). It may be that the increased reliance on vision for postural sway is due to a decline in proprioceptive ability. Toledo and Barela (2014) compared postural sway in healthy young and older persons under the moving room paradigm, in which the walls move and the floor remains still, resulting in inaccurate visual input. Older participants swayed more than younger participants. Moreover, a multivariate analysis of the contributions



25. The Aging Vestibular System: Implications for Rehabilitation

of sensory and motor systems to the increased sway revealed that proprioceptive ability (measured by sensitivity to passive motion) was the main contributor to postural sway.

Age Effects on the Somatosensory System Several changes have been identified in proprioceptive function with aging. Increased muscle spindle capsule thickness, loss of intrafusal muscle fibers, and impaired muscle spindle sensitivity have been reported; however, these changes can be highly individualized (see Goble, Coxon, Wenderoth, Van Impe, & Swinnen, 2009). An age-related decrease in cutaneous sensation due to a loss of Pacinian and Meissner’s receptors results in reduced deep tendon reflex responses and decreased vibration sense at the ankles (Baloh, Ying, & Jacobson, 2003). Cutaneous afferents are known to be important in postural control. If the plantar surface of the foot is anesthetized, the amplitude of muscle responses is reduced in the soleus muscles (Do, Bussel, & Breniere, 1990). Kristinsdottir and colleagues (2001) demonstrated the effect of decreased vibration sense on postural control by comparing healthy younger adults (mean age = 37.5 years) with healthy older adults stratified by vibration sense (mean age = 74.6 years). In general, older age was correlated with greater sway; however, reduced vibration sensation resulted in significantly greater sway compared with older and younger adults with intact vibration perception. Vision attenuated sway in all individuals, but to a lesser extent in older subjects with diminished vibratory sensation. Interestingly, one-third of the older subjects exhibited head shaking–induced nystagmus, suggesting that vestibular impairment may have been a contributing factor to impaired postural stability.

Age Effects on the Neuromuscular System Aging results in decreased muscle mass and strength (sarcopenia). Numerous mechanisms are thought to be responsible for sarcopenia, including changes in protein synthesis, proteolysis, neuromuscular integrity, muscle fat content, as well as lifestyle factors (physical activity and nutrition) (Doherty, 2003). There is a nearly 40% reduction in muscle fiber numbers, especially type II fast twitch fibers, between the ages of 20 and 89 years, resulting in loss of muscle strength and power (Narici & Kayser, 1995; Porter, Vandervoort, & Lexell, 1995). Muscle strength peaks in the third decade and begins to decline in the fourth (Metter, Conwit, Tobin,

& Fozard, 1997). Studies have measured a 1% to 3% per year decline in skeletal muscle maximum voluntary contraction in healthy adults, with a steeper decline after the fifth and sixth decades, although there is considerable heterogeneity among older adults (Goodpaster et al., 2006; Hurley, 1995; Rantanen et al., 1998). Strength of the lower extremities is important in postural control. Reduced ankle muscle strength is associated with decreased ability to recover from induced postural perturbations (Carty, Barrett, Cronin, Lichtwark, & Mills, 2012; Fujimoto, Hsu, Woollacott, & Chou, 2013), and reduced plantar flexor strength has been found to be associated with a reduction in the limits of stability (Melzer, Benjuya, Kaplanski, & Alexander, 2009) and increased postural sway (Bok, Lee, & Lee, 2013). Fukagawa, Wolfson, Judge, Whipple, and King (1995) found that lower limb strength was a predictor of loss of balance during the sensory organization test and an independent predictor of falls. Quadriceps strength was found to be one of the three best predictors of increased mediolateral sway in a modified tandem Romberg test with eyes closed (Lord et al., 1999). Both reduced quadriceps and hip abduction strength have been associated with an increased likelihood of taking multiple protective steps during balance testing as well as future fall risk (Hilliard et al., 2008; Lord et al., 1999). Older adults demonstrate a loss of postural control, and lateral stability appears to be the most affected (Lord et al., 1999). Longer onset latencies in distal muscles, disorganized muscle recruitment, and longer periods of coactivation have also been found during perturbations in older subjects compared with younger subjects (Manchester et al., 1989; Tang & Woollacott, 1998; Woollacott et al., 1986). Elderly subjects at risk of falling have been found to use stepping, reaching, and hip strategies more than those not at risk of falling (who tend to use the ankle strategy) (Maki & McIlroy, 2006; Mille et al., 2013). Older adults initiate stepping at lower amplitudes of instability than younger adults. For example, Mille and colleagues (2013) found that when a mediolateral perturbation was provided by a motorized waist pull system, older subjects took multiple steps, often directed laterally, to regain balance, whereas younger subjects regained balance with a single step. The loss of mediolateral control may be due, in part, to inability to produce adequate hip muscle torque and increased trunk stiffness when an unexpected perturbation is induced (Rogers & Mille, 2003). As well as taking multiple steps, older adults more frequently initiate arm movements and use a reach and grasp strategy to recover balance after a perturbation (Maki & McIlroy, 2006).

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Age and Attentional Demands of Postural Control A common complaint voiced by individuals with vestibular dysfunction is difficulty concentrating; nearly half of people with vestibular disorders surveyed reported moderate to severe difficulty focusing attention (Alghwiri, Alghadir, & Whitney, 2013; Jacobson & Newman, 1990). This effect may be the result of increased utilization of attentional resources due to impaired balance following vestibular loss; alternatively, this effect may be as a result of cognitive changes related to vestibular dysfunction (Bigelow & Agrawal, 2015). The impact of attentional demands on postural control has been explored using the dual-task paradigm. The dual-task methodology assumes that limited cognitive resources, specifically attentional capacity, can be allocated to activities at any given time and that performance of any task requires a given proportion of that capacity (Abernethy, 1988). Therefore, multiple tasks performed simultaneously compete for available resources, and when the available attentional resources are exceeded, performance degrades in one or both of the activities (Abernethy, 1988). Using the dual-task paradigm, researchers have demonstrated that the processes used to maintain balance require attentional resources (Kerr, Condon, & McDonald, 1985). Not only does postural control require attentional resources, but also the demands on attentional resources increase in the presence of increased age and impaired balance (Shumway-Cook & Woollacott, 2000). In older individuals with impaired balance control, performing even simple cognitive tasks leads to further impairments of balance (Shumway Cook, Woollacott, Kerns, & Baldwin, 1997). Older adults with balance impairment demonstrated significantly more postural sway (i.e., greater instability) than either young or old healthy subjects under dual-task conditions (Kerr et al., 1985; Shumway-Cook & Woollacott, 2000). More importantly, some older adults with impaired balance who had been able to maintain balance under a single-task condition fell under dual-task conditions (Shumway-Cook & Woollacott, 2000). There is accumulating evidence that an impaired ability to allocate attention to gait under dual-task situations is a powerful predictor of falls in older adults (Mirelman et al., 2012) and is associated with cognitive capacity, specifically executive functions (Li, Bherer, Mirelman, Maidan, & Hausdorff, 2018). There is reportedly a significant relationship between poorer cognitive performance and vestibular dysfunction, and a recent review suggests that vestibular dysfunction is associated with worse performance for specific cognitive abilities, especially visuospatial skills, attention, and executive func-

tions (Bigelow & Agrawal, 2015). One study of adults with age-related decline of vestibular function (based on cVEMP and vHIT) and without evident vestibular pathology such as BPPV or Meniere’s disease examined performance on a navigation task (Xie et al., 2017). The spatial navigation task, the Triangle Completion Task, involved walking a triangular path without visual or auditory input. Older adults with vestibular impairment demonstrated poorer spatial navigation (i.e., more veering) than healthy older and younger adults. Studies involving individuals with vestibular deficits demonstrate interference between postural control and cognitive task performance. Redfern, Talkowski, Jennings, and Furman (2004) tested healthy controls and well-compensated patients with surgically induced unilateral vestibular loss. For both groups, postural sway increased during the dual-task conditions. However, reaction times for patients were slower than controls under all postural conditions, including sitting as well as standing. This is a surprising finding given the minimal balance requirements involved in sitting, but is consistent with studies demonstrating that increased attentional resource utilization is required to process and integrate multiple sensory inputs and for VOR suppression (Talkowski, Redfern, Jennings, & Furman, 2005; Yardley, Gardiner, Lavie, & Gresty, 1999). Yardley et al. (2001) also found poorer cognitive performance for patients with uncompensated vestibular dysfunction of various etiologies, compared with healthy control subjects, under all postural conditions, including sitting and standing. Reaction time for both groups increased with increasing postural demands (from sitting to standing on a stable surface to standing on a sway-referenced surface); although in this study, in contrast to Redfern’s findings, there were no additional dual-task costs for patients with vestibular dysfunction compared with healthy controls. Individuals with vestibular dysfunction performed significantly worse walking under cognitive dual-task conditions on either the cognitive (Nascimbeni, Gaffuri, Penno, & Tavoni, 2010 ) or walking task (Roberts, Cohen, & Sangi-Haghpeykar, 2011), suggesting that vestibular dysfunction increases the attentional demands of walking. The mechanisms underlying the relationship between vestibular dysfunction and cognition are not clear. Vestibular dysfunction may directly cause changes in brain structure and function involving central vestibular pathways, such as atrophy of the hippocampus that leads to impaired spatial memory as suggested by Brandt and colleagues (2005). Alternatively, the impaired postural control related to vestibular dysfunction may increase the attentional demands of gait and dynamic balance, leaving fewer resources available for performing a cognitive dual task.



25. The Aging Vestibular System: Implications for Rehabilitation

Epidemiological studies have identified a significant relationship between hearing loss and falls, although the mechanisms underlying the relationship are unclear (Lin & Ferrucci, 2012; Viljanen et al., 2009). One hypothesis is that older adults with hearing loss are more likely than older adults with normal hearing to have vestibular loss and related decreased postural stability due to a common mechanism that damages both cochlear and vestibular sensory organs and/or their pathways, leading to hearing and vestibular loss. For example, Zuniga and colleagues (2012) identified a significant relationship between hearing loss and reduced cVEMP amplitude (i.e., reduced saccular function). Additionally, there were significant relationships between age and noise exposure with hearing and saccular function, suggesting that the noise exposure resulting in hearing loss may also damage the vestibular system. Another hypothesis is that older adults with hearing loss require greater listening effort, which utilizes more cognitive resources. This leaves fewer cognitive resources available during challenging balance tasks and increases fall risk, especially under dual-task conditions. Ryan et al. (2019) used EEG as an objective measure of listening (or cognitive) effort while performing a words-in-noise listening test to examine the effect of increased listening task difficulty. In easier listening conditions, EEG frequency power reflects a change in cognitive state, independent of performance measures of accuracy. It is hypothesized that the changes observed in EEG frequency power reflect the listening effort that listeners report, but clinical measures have been unable to detect this change.

Functional Impact of VOR on Postural Control As demonstrated in the previous section, age-related changes in the vestibular system are well documented. However, the specific contributions of reduced VOR and VSR to balance deficits in older adults are less clear, as there are conflicting findings between measures of vestibular function and measures of balance and gait. The increase in postural sway with aging during static balance testing using computerized posturography is well known and was first demonstrated by Peterka and Black (1990). In their study of healthy subjects across a wide range of ages (7 to 81 years), the correlation between VOR gain and postural sway was weak; however, otolith organ function was not assessed. More recently, Serrador, Lipsitz, Gopalakrishnan, Black, and Wood (2009) found a significant correlation between age-related reduction in otolith organ

response and increased postural sway during static balance testing. Age-related changes in gait are well documented and include slowing of gait speed and cadence and reduced step length (Herssens et al., 2018). Age-related slowing of gait speed has been associated with age-related declines in saccular function (Layman et al., 2015), whereas slower cadence and longer stride length and stance time have been associated with agerelated declines in horizontal semicircular canal vestibular function (Anson, Pineault, Bair, Studenski, & Agrawal, 2019). Hall, Schubert, and Herdman (2004) first identified DVA (see Chapter 9) as an important predictor of the degree of fall risk reduction in individuals with unilateral vestibular deficits. Honaker and Shepard (2011, 2013) examined the use of computerized DVA and GST testing to identify fall risk in older adults. In a small sample of older adults with a history of recurrent falls (n = 16; 4 of 16 had unilateral vestibular hypofunction), a cut-point of >0.25 logMAR during DVA testing demonstrated good sensitivity (87% for rightward head movement and 80% for leftward head movement) and specificity (61%) for identifying fallers (Honaker & Shepard, 2011). In addition, the DVA test and Dynamic Gait Index (DGI) (total scores 67 years of age) had significantly better dizziness outcomes six months after an internet-based vestibular rehabilitation program compared with controls, whereas in those less than 67 years of age the differences (compared with control) were no longer evident at six months.

Effect of Age on Fall Risk Reduction General findings from several studies reveal that age does not affect rehabilitation outcomes: older adults improve to a similar extent as younger adults with vestibular deficits, although older adults may need more treatment sessions, perhaps because of multiple comorbidities (Cohen & Kimball, 2003; Shepard, Telian, Smith-Wheelock, & Raj, 1993; Whitney et al., 2002). Whereas older and younger adults demonstrate similar improvements in DGI scores following vestibular rehabilitation, one retrospective study showed that a greater proportion of older adults remained at risk for falls at discharge (45% of older adults versus 11% of younger adults) (Hall, Schubert, & Herdman, 2004). Older adults may remain at risk for falls at discharge due to comorbidities or polypharmacy, and their effects on balance may mandate an assistive device to prevent falls in older patients.

Impact of Newer Technologies on Rehabilitation In the past decade, the availability of low-cost technology to provide biofeedback, virtual reality, and gaming systems (such as the Nintendo Wii) has resulted in a



25. The Aging Vestibular System: Implications for Rehabilitation

proliferation of studies investigating their effectiveness in rehabilitation. Care needs to be taken when incorporating technology in the rehabilitation of older adults, because older adults are generally less confident in using technology and are also less likely to use technology (Czaja et al., 2006). However, initial case studies and uncontrolled studies suggest that older adults are open to technology in rehabilitation (Meldrum, Glennon, Herdman, Murray, & McConn-Walsh, 2012; Taylor et al., 2012; Williams, Doherty, Bender, Mattox, & Tibbs, 2011) and a recent systematic review has further clarified the role that technology may play in rehabilitation (Booth, Masud, Connell, & Bath-Hexstall, 2014). Randomized controlled trials have found conflicting results in the use of gaming for balance rehabilitation (Szturm, Betker, Moussavi, Desai, & Goodman, 2011; Toulotte, Toursel, & Olivier, 2012). Toulotte and colleagues (2012) found that community-dwelling older adults who played the Nintendo Wii Fit over a period of 20 weeks improved static balance, but a combination of the Wii Fit plus additional exercise conferred the most benefit to dynamic balance. On the other hand, Stzurm et al. (2011) demonstrated a superior effect in the gaming group on Berg Balance Scores and Activities Balance Confidence Scores compared with conventional therapy in frail elderly. This finding was supported by Griffin, McCormick, Taylor, Shawis, and Impson (2012), who found that the Wii Fit Plus, when combined with conventional physical therapy, conferred an additional improvement in TUG and functional reach scores. A recent systematic review of the effectiveness of virtual reality interventions in improving balance concluded that evidence to support the use of gaming to improve impairments, activity limitations, and participation in older adults is weak at present (Booth et al., 2014). Adherence and acceptability were generally positive, but initial training and monitoring for safety in the home were factors that needed attention in the trials. Importantly, no evidence for superiority of virtual reality over conventional therapy was found using meta-analysis (Booth et al., 2014). Using a higher-end, clinic-based virtual reality system, the Balance Rehabilitation Unit, Duque et al. (2013) found evidence of superiority for use of virtual reality in reducing falls and reducing fear of falling in the elderly, compared with usual care (which included the Otago balance rehabilitation program). The role of technology in vestibular and balance rehabilitation for older adults is becoming clearer and it can be concluded that it appears to achieve similar outcomes to those from a conventional rehabilitation program. Studies specific to vestibular-impaired elderly are lacking at present, but recent trials in patients with unilateral peripheral vestibular loss that included

elderly subjects found no evidence of superiority of a Nintendo Wii Fit vestibular rehabilitation program compared with conventional rehabilitation (both home based) (Meldrum et al., 2015; Phillips et al., 2018). In the former study, adherence was similar between the two groups, and there was evidence that the Nintendo Wii Fit group enjoyed the treatment more and found the balance exercises less difficult and less tiring. The systems described above pertained mainly to retraining balance and mobility, but more recently, systems incorporating the Wii remote controller (Chen, Hsieh, Wei, & Kao, 2012) and the iPod (Huang, Sparto, Kiesler, Siewiorek, & Smailagi, 2014) have been designed to track head velocity in order to retrain gaze stability. These systems are likely to become commercially available for future rehabilitation. Access to vestibular rehabilitation is limited for many individuals (Bush & Dougherty, 2015; Van Vugt et al., 2017). During the recruitment process in one study, only 3% of those with dizziness had been offered vestibular rehabilitation prior to enrollment, despite a mean duration of 12 years of dizziness symptoms (Yardley et al., 2004). Technology may be of benefit in solving problems of access. Geraghty et al. (2017) provided an internet-based vestibular rehabilitation program and found it superior to usual care and effective in reducing symptoms of dizziness, with an effect size that was comparable to face-to-face care. The median age of those participating was 67.l years, suggesting acceptance of technology-based rehabilitation, which was supported by a qualitative study during the trial (Essery, Kirby, Geraghty, & Yardley, 2017). However, there was a much higher drop-out rate in the internetbased compared with the usual-care group (30% versus 13.2%). Pavlou, Bronstein, and Davies (2013) also reported a 55% drop-out rate in patients performing a home-based DVD exercise program with minimal faceto-face interaction. Thus, technology may not solve all problems of access, and face-to-face care is likely to be an essential component for successful rehabilitation outcomes.

Impact of Fear of Falling on Outcomes Psychological factors such as fear of falling (FOF), anxiety, and depression have an added negative effect on physical impairments, and evidence suggests that these factors are more prevalent in older individuals with vestibular impairment. FOF is defined as “low perceived self-efficacy at avoiding falls during essential, nonhazardous activities of daily living” (Tinetti, Richman, & Powell, 1990, p. 239) and is commonly measured using a dichotomous yes/no question of

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“Are you afraid of falling?” or indirectly with balance efficacy scales (e.g., the Activities-specific Balance Confidence [ABC] scale or Falls Efficacy Scale). FOF has been found in approximately 30% of communitydwelling older adults in longitudinal studies of aging and has a negative impact on mobility (Donoghue, Cronin, Savva, O’Regan, & Kenny, 2013; Reelick, van Iersel, Kessels, & Rikkert, 2009; Rochat et al., 2010). For example, when anxiety, number of previous falls, number of medications, and level of activity were controlled for, FOF was independently associated with reduced gait speed in a sample of older adults (Reelick et al., 2009). This finding has been confirmed by two large longitudinal studies which also controlled for physical, mental, and cognitive health (Donoghue et al., 2013; Rochat et al., 2010). These findings are important given that slow gait speed has been implicated in falls (Ambrose, Paul, & Hausdorff, 2013; Dunlap, Perera, Van Swearingen Wert, & Brach, 2012), with a 7% increase in fall risk for every 0.1 m/s reduction in gait speed (Verghese, Holtzer, Lipton, & Wang, 2009). Dizziness is associated with an increase in FOF in older adults. Two case-control studies (Burker et al., 1995; Perez-Jara et al., 2012) found a significantly greater prevalence of FOF (47% and 71%, respectively) in older patients attending dizzy clinics compared with agematched healthy controls (3% and 31.2%, respectively). In a cross-sectional study of elderly patients with vestibular impairment, Marchetti, Whitney, Redfern, and Furman (2011) found that 42% of elderly vestibularimpaired patients had FOF and impaired balance and gait that were significantly associated with lower ABC scores. Significant associations were also found with anxiety, depression, and general health. A qualitative study of older patients with dizziness and FOF uncovered themes such as embarrassment, depression, and anxiety and the perception of being a burden on family members. Almost all patients reported feeling anxious about falling and dizziness, with many reporting they were more sedentary and limited the places they went as a result of FOF (Honaker & Kretschmer, 2014). More recently, Harun, Bridges, and Agrawal (2016) found similar themes in a qualitative study of older adults with age-related vestibular loss. FOF was common and walking was universally reported as difficult. Anxiety, fatigue, activity limitations, and reduced participation with decreased driving ability and independence were also common concerns. That FOF is independently associated with reduced gait and balance raises the question of causative factors. Slower gait speed with shorter stride lengths is associated with a more cautious gait pattern and is found in healthy controls in conditions where postural threat is

perceived — for example, when walking on an elevated walkway (Brown, Gage, Polych, Sleik, & Winder, 2002). Gait during this task is modified to a greater extent in older individuals and even more so when healthy older adults are compared with older adults who have FOF (Delbaere, Sturnieks, Crombez, & Lord, 2009). Postural threat is also associated with a generalized stiffening of the body, indicated by increased co-contraction and decreased sway (Carpenter, Adkin, Brawley, & Frank, 2006; Nagai et al., 2012; Osler, Tersteeg, Reynolds, & Loram, 2013). It is postulated that the modification of the postural response reflects an adaptive response to control the body’s momentum and exert more control over the center of mass in order to prevent falls. Studies specifically investigating gait in vestibular-impaired populations have shown that while gait speed is slower in these populations, it appears to be chosen, as demonstrated by an ability to walk at greater cadences when asked to do so (Krebs, Gill-Body, Parker, Ramirez, & Wernick-Robinson, 2003) and thus lending support to an adaptive theory. In conclusion, the changes in gait seen in the elderly with FOF or vestibular impairment (or both) may reflect a conscious modification of gait to avoid falls (Delbaere et al., 2009). Anxiety and depression are closely linked to both FOF and vestibular impairment and should be taken into account when planning vestibular rehabilitation in this population.

Does Therapy Have to Be Individualized or Can Group Therapy Work? It is not clear as to whether individualized therapy or group therapy is superior when rehabilitating older patients with vestibular dysfunction. A recent systematic review found five studies that exclusively investigated vestibular rehabilitation in older subjects (Ricci et al., 2010). Group therapy rather than individualized therapy was the most common mode of therapy administration in the clinical setting. Only one study compared two types of vestibular rehabilitation (Cawthorne-Cooksey–based exercises versus adaptation exercises) and no differences were found between the two treatments. The other four studies in the review compared vestibular rehabilitation with no treatment and found significant improvement in most measures of balance, gait, and dizziness. In four of the five studies, exercises were performed at home with weekly visits to a therapist for progression; in the other, exercises were performed exclusively at home. The review concluded that in middle-aged and older patients receiving vestibular rehabilitation, there is insufficient evidence at



25. The Aging Vestibular System: Implications for Rehabilitation

present to recommend one form of rehabilitation over another or individual exercise versus group exercise. Strength training is rarely included as a component of vestibular rehabilitation. Two retrospective reviews of vestibular rehabilitation in older populations incorporated lower limb strengthening (Cronin & Steenerson, 2011; Macias, Massingale, & Gerkin, 2005). However, no study has measured the specific impact of the strength training on outcomes. This would be of great interest, given the role of strength in postural stability discussed above and the positive effect of strengthening on gait stability in elderly who have functional limitations (Hausdorff et al., 2001; Krebs, Jette, & Assmann, 1998).

Conclusion There are many factors involved in postural stability and many of the systems involved undergo age-related changes. Assessment and treatment of dizziness and imbalance in older adults require a multidimensional approach. Health care professionals should not consider age-related declines in the vestibular system in isolation. The non-vestibular motor and sensory systems such as vision, proprioception, hearing, and muscle strength and their contributions to dizziness and imbalance also require consideration. Furthermore, the increased likelihood of comorbidities and polypharmacy in older populations must also be taken into consideration. Taken together, multidisciplinary teams offering multi-component management and treatment are likely to have the best outcomes. There is sufficient evidence presently to support successful vestibular rehabilitation outcomes in older adults. Access to vestibular and balance rehabilitation remains a barrier. However, the use of technology in vestibular rehabilitation is rapidly evolving and may improve access. Technology is likely to be adopted by older adults, but is not likely to be well received if provided isolated from face-to-face care.

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26 Topographical Localization of Vestibular System Impairment Gary P. Jacobson, Erin G. Piker, Richard A. Roberts, Devin L. McCaslin, and Nabih M. Ramadan

Introduction A comprehensive evaluation of the vestibular system implies a functional assessment will occur of the five structures that make up the peripheral end organs for each ear, as well as an assessment of the integrity of the central nervous system connections. The wide availability of contemporary measures for evaluating the vestibular system should provide the clinician with some reassurance that it is possible to assess all 10 end organs with modern-day electroneurodiagnostic tech-

niques. This chapter adds to previous work (Curthoys, 2012; Curthoys & Manzari, 2013; Jacobson et al., 2011) which provided a framework for the identification of common patterns of impairment on electroneurodiagnostic tests and their associated anatomical and physiological correlates. A summary of available vestibular function tests and the anatomy they assess is shown in Table 26–1. A summary of possible test patterns and the structures that are impaired is shown in Table 26–2. The physiological origins of the common vestibular function measures provide the clinician with a unique opportunity

Table 26–1.  Quantitative Vestibular Tests and the Anatomy They Assess Structure(s)

Test

Utricle/superior vestibular nerve

Ocular VEMP (Vestibulo-[Utriculo])-ocular Reflex)

Saccule/inferior vestibular nerve

Cervical VEMP (Vestibulo-[Sacculo])-collic Reflex)

Anterior semicircular canal/ superior vestibular nerve

Video Head Impulse Test (high acceleration, natural head movement VOR)

Posterior semicircular canal/ inferior vestibular nerve

Video Head Impulse Test (high acceleration, natural head movement VOR)

Horizontal semicircular canal/ superior vestibular nerve

Rotary Chair (low-mid frequency VOR function)

Caloric testing (very low-frequency VOR function) Video Head Impulse Test (natural head movement and high-frequency VOR) 597

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Balance Function Assessment and Management

Table 26–2.  Summary Table Showing Patterns of Test Results and the Structures That Are Impaired (Where Appropriate)

Impairment

Caloric

Horizontal vHIT

Vertical vHIT

cVEMP

oVEMP

Normal

N

N

N

N

N

hSCC

A ipsi

A ipsi

N

N

N

aSCC

N

N

A contra downward impulse

N

N

pSCC

N

N

A ipsi upward impulse

N

N

Utricle

N

N

N

N

A ipsi ear stimulated

Saccule

N

N

N

A ipsi

N

Sup. Vestib. n.

A ipsi

A ipsi

A contra downward impulse

N

A ipsi ear stimulated

Inf. Vestib. n.

N

N

A ipsi downward impulse

A ipsi upward impulse

N

Total unilateral

A ipsi

A ipsi

A ipsi

A ipsi

A ipsi ear stimulated

Note. A = abnormal, N = normal, contra = contralateral, ipsi = ipsilateral, p = posterior, a = anterior, h = horizontal Source:  Jacobson, G. P., 2019, adapted from Barin, 2019, personal communication.

to, in many cases, make statements about (1) if an impairment exists, (2) if one exists, whether the impairment affects the peripheral or central vestibular system, (3) if it is a peripheral impairment, which of the end organs are impaired, (4) if the peripheral impairment is unilateral or bilateral, (5) the degree of impairment, and (6) whether static and/or dynamic compensation has occurred in the wake of the injury. In this chapter we will provide a brief overview of the innervation and perfusion patterns of the vestibular system. We will then discuss how patterns of vestibular test results can assist the clinician in localizing vestibular impairments and highlighting findings reported in common vestibular pathologies. The chapter will conclude with a series of illustrative case studies.

Innervation Patterns The bipolar ganglion cells of the vestibular branch of cranial nerve VIII (CN VIII) divide in the internal auditory canal to form the inferior and superior

branches (See Figure 4–1 in Chapter 4) The superior branch of the vestibular nerve sends the anterior ampullary nerve to innervate the crista of the superior (anterior) semicircular canal. The superior vestibular nerve (SVN) also sends the horizontal ampullary nerve to innervate the crista of the lateral (horizontal) semicircular canal. Finally, the SVN sends the utricular nerve to innervate the macula of the utricle. The inferior vestibular nerve (IVN) innervates the saccular macula. Additionally, the IVN innervates the crista of the posterior semicircular canal with the posterior ampullary nerve. Given these innervation patterns, it is possible to have a discrete injury affecting one or more of the ampullary nerves and/or nerves innervating the otolith end organs. For example, an injury affecting the SVN would produce an impairment in neural conduction from the anterior and lateral semicircular canals, and the utricle to the vestibular nuclei. This disorder would result in abnormal test results for the ipsilesional caloric, anterior and lateral vHIT, and ocular vestib-



26. Topographical Localization of Vestibular System Impairment

ular-evoked myogenic potential (oVEMP) tests. The cervical VEMP (cVEMP) test and posterior canal vHIT test would be normal. Alternately, a lesion affecting the IVN would produce an abnormal ipsilesional cVEMP and posterior canal vHIT test but normal caloric, anterior and lateral vHIT, and oVEMP tests.

Vascular Perfusion Patterns Blood perfusion of the vestibular system (Figure 26–1) occurs through the labyrinthine artery (i.e., also referred to as the internal auditory artery). The labyrinthine artery most commonly arises from the anterior inferior cerebellar artery (AICA). The artery divides

into two branches, the common cochlear artery and the anterior vestibular artery as it courses through the internal auditory canal. The common cochlear artery divides into the main cochlear artery and posterior vestibular artery. The main cochlear artery and modiolar arteries perfuse the cochlea. The posterior vestibular artery perfuses the posterior semicircular canal and the saccule. The anterior vestibular artery perfuses the utricle, a small part of the saccule and lateral and superior semicircular canals. A loss of blood supply from the AICA or the labyrinthine arteries has the potential to produce a devastating injury affecting the function of the ipsilesional membranous labyrinth. A loss of blood supply

Figure 26–1. Diagram of the vascular perfusion pattern for the peripheral vestibular system. Art = artery, Lat = lateral, Post = posterior, Ant = anterior, SCC = semicircular canal.

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from either the common cochlear artery or vestibulocochlear artery would result in damage to the cochlea, posterior semicircular canal, and saccule. That is, the patient would demonstrate sensorineural hearing loss and an abnormal, or absent, cVEMP on the ipsilesional side. The oVEMP, lateral vHIT, and caloric tests would be normal. A loss of blood supply from the anterior vestibular artery would produce an injury affecting the ipsilesional utricle and lateral and anterior semicircular canals. Accordingly, a patient with this combination of impairments would be expected to show normal ipsilesional auditory function and normal cVEMP tests and abnormal or absent caloric, anterior and lateral vHIT, and oVEMP tests. A loss of blood flow from the main cochlear artery would produce sudden deafness on the ipsilesional side. An isolated injury to the posterior vestibular artery would be expected to have no effect on auditory function or the caloric, anterior and lateral vHIT, and oVEMP tests, but would demonstrate evidence of impairment on the ipsilesioned side on the cVEMP test, as well as the posterior canal vHIT.

Vestibular Test Patterns Associated with Specific Impairments, Diseases, or Disorders Utricle and Saccule Table 26–3 shows a pattern of test results that might be encountered in an isolated impairment affecting the

saccule. Table 26–4 shows a pattern of test results that might be encountered in an impairment affecting the utricle. The knowledge that each vestibular end organ is innervated by a branch of either the superior or inferior vestibular nerve suggests that patients may report a broad range of symptoms depending on which part, or parts, of the peripheral vestibular system are affected by disease. Patients who complain of abnormal unprovoked sensations of linear acceleration and deceleration have been reported to have impairments affecting the utricle, saccule, and/or the inferior and/or anterior vestibular nerves. In this regard, Seo et al., (2008) studied 18 patients with undiagnosed dizziness. The patients were evaluated with the cVEMP. The cVEMP was abnormal in 71% of their patients and those patients reported a falling sensation. Of this subsample, 83% reported unsteadiness lasting seconds. The investigators reported their belief that the falling sensation was related to both saccular hydrops and unknown saccular disorders. Murofushi et al., (2012) examined 10 patients who complained of an episodic tilting sensation. The spells lasted from a few minutes to 1 hour, although most often the spells lasted a few minutes. Caloric tests were all normal. The cVEMP was normal in half of the patients (5/10), but 8/10 patients failed to generate an oVEMP on one side. It was the author’s opinion that the utricular impairments (i.e., oVEMP abnormalities) were the sources of the episodic tilting sensation. Pelosi et al., (2013) reported that patients with unilaterally impaired utricular function show an increased prevalence of postural instability or a swaying-rocking sensation. Additionally, Curthoys and Manzari

Table 26–3. Sample Findings in an Isolated Saccule Impairment Test

Structure Lateral

Superior

oVEMP

Utricle

Saccule

Posterior

Normal

cVEMP

Reduced or Absent

vHIT

Normal

Rotary Chair

Normal

Caloric

Normal

Normal

May be more common as we age; associated with unsteadiness

Normal



26. Topographical Localization of Vestibular System Impairment

Table 26–4. Summary Table for Expected Test Results in an Isolated Utricular Impairment Test

Structure Lateral

Superior

oVEMP

Utricle

Saccule

Posterior

Reduced or Absent

cVEMP

Normal

vHIT

Normal

Rotary Chair

Normal

Caloric

Normal

Normal

Normal

May be more common as we age; associated with unsteadiness; emerging evidence isolated finding of unilateral absent/asymmetric oVEMP with all other results normal is common in patients with vestibular migraine.

(2013) have reported that patients with impairment affecting just one otolith end organ may complain of severe symptoms when they are in the acute stages of the disease. The authors stated that this loss of function “causes severe, dramatic symptoms.” Further the investigators stated that patients do not complain so much of vertigo as they do of postural unsteadiness that is severe enough to make the patient concerned that he/she might fall.

Vestibular Neuritis Tables 26–5 and 26–6 show a summary of findings associated with either anterior vestibular nerve neuritis or inferior vestibular nerve neuritis. The pattern of findings that helps to identify vestibular neuritis begins with a history of severe vertigo and accompanying nausea and vomiting of long duration (e.g., days to weeks). Viral inflammation is the presumed cause and most commonly when the impairment is unilateral the superior vestibular nerve is affected (Lee et al., 2019). A patient with vestibular neuritis affecting the superior vestibular nerve would be expected to demonstrate a stereotypical pattern of impairment for lateral semicircular canal (i.e., a unilaterally abnormal caloric test and ipsilesional abnormal lateral canal video Head Impulse Test [vHIT]), anterior semicircular canal (i.e., abnormal ipsilesional superior canal vHIT), and utricle (i.e., abnormal oVEMP when the auditory stimulus is presented to the affected ear). The saccule (i.e., cVEMP test) and posterior semicircular canal (i.e.,

posterior semicircular canal vHIT) should be normal. Alternatively, a less common inferior vestibular nerve involvement (Lee et al., 2019) would present with the opposite results (Park et al., 2018), including normal test results for the lateral semicircular canal (caloric and vHIT), anterior semicircular canal (vHIT), and utricle (oVEMP). Tests of the saccule (cVEMP) and posterior semicircular canal (posterior canal vHIT) on the affected side would be abnormal. The clinician should be mindful that it is possible to have viral disease affecting both nerves simultaneously (i.e., occurring ~40% of the time; Lee et al., 2019). When this occurs there will be abnormalities for all end organs. If there is impairment of auditory function on the affected side, then the diagnosis would favor labyrinthitis instead of neuritis. Finally, it is possible to obtain similar results with ischemic disease. As an example, recall that the anterior vestibular artery provides the predominant blood flow to the same structures innervated by the superior vestibular nerve. It would be possible to have an anterior vestibular artery occlusion that impaired the function of the sensory structures with no involvement of the nerve. The pattern of test results would be the same.

Ménière’s Disease There have been several reports describing the diagnostic pattern associated with Ménière’s disease, and it is summarized in Table 26–7. The most frequently reported pattern is a unilaterally abnormal (or bilaterally abnormal in bilateral Ménière’s disease) caloric test

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Balance Function Assessment and Management

Table 26–5. Sample Findings One Might Observe for a Patient with a Superior Vestibular Nerve Neuritis Test

Structure Lateral

Superior

oVEMP

Utricle

Saccule

Posterior

Abnormal ipsi ear stimulated

cVEMP

Normal

vHIT

Reduced Gain / Saccades

Rotary Chair

Reduced Gain / Increased Phase / Asymmetry

Caloric

Reduced or Absent on the affected side

Reduced Gain / Saccades

Normal

Structures innervated by superior branch are affected. Could also occur with labyrinthine ischemia of anterior vestibular artery.

Table 26–6. Summary Table of Sample Findings for a Patient with an Inferior Vestibular Nerve Neuritis Test

Structure Lateral

Superior

oVEMP

Utricle

Saccule

Posterior

Normal

cVEMP

Reduced or Absent

vHIT

Normal

Rotary Chair

Normal

Caloric

Normal

Normal

Structures innervated by inferior branch are affected

Reduced Gain / Saccades



26. Topographical Localization of Vestibular System Impairment

Table 26–7. Summary Table Showing Test Results That Might Be Encountered from a Patient with Ménière’s Disease Test

Structure Lateral

Superior

oVEMP

Utricle

Saccule

Posterior

Variable

cVEMP

Variable

vHIT

Normal

Rotary Chair

Normal

Caloric

Abnormal ipsilesional

Normal

Normal

Pattern of abnormal LF response (calorics) with normal high frequency response (vHIT); with continued damage, expect greater impairment

combined with a bilaterally normal lateral semicircular canal vHIT. There have been at least two potential explanations for this pattern of results (McCaslin et al., 2015; McGarvie et al., 2015). As noted previously, the caloric stimulus is roughly equivalent to a sinusoidal stimulus of 0.003 Hz. The vHIT test represents a more “ecologically valid” stimulus (i.e., a frequency encountered often in everyday life) of 1 to 6 Hz. The lateral canal cristae ampullaris consists of both type I and type II hair cells and irregularly and regularly discharging afferent neurons, respectively. The type I hair cells are represented in the central portion of the horizontal canal cristae and they connect to irregularly discharging afferents. These hair cells transduce high frequency and high acceleration head movements. The type II hair cells are located in the periphery of the cristae. They connect to regularly discharging type II neurons and encode low-frequency head movements (Hullar et al., 2005). It has been reported by Tsuji et al. (2000) that the increased endolymphatic pressure associated with Ménière’s disease affects primarily the type II hair cells. The effects of the abnormally increased endolymphatic pressure from repeated hydropic episodes damages preferentially the type II hair cells that transduce low frequencies. This explains why a low frequency test (i.e., the caloric test) would be ipsilesionally abnormal but the test of high frequency function (vHIT) would be normal. A second explanation was offered by McGarvie et al. (2015). The authors stated that the mode of stimulation of the horizontal semicircular canal cristae is different for the caloric stimulus (i.e., creation of convection current unilaterally) versus a natural stimulus

like sinusoidal oscillation (i.e., even though the end result of a shearing effect between the cupula and hair cell stereocilia is the same). It was the contention of the investigators that repeated dilation of the lateral semicircular canal ampulla would result in a condition where instead of creating a single hydrostatic force (i.e., that yields a single convection current) that is capable of increasing fluid pressure against the cupula, there are instead multiple smaller, local convection currents that are incapable of creating sufficient hydrostatic force to deflect the cupula. This would explain how there could be a condition where a caloric test could be abnormal but a vHIT test could be normal. Where this pattern of results occurs it is highly likely the patient’s history will support the diagnosis of Ménière’s disease. No consistent pattern of VEMP abnormalities has been identified.

Vestibular Migraine Table 26–8 provides a summary of test results that might be encountered from a patient with vestibular migraine (VM). Zaleski and colleagues (2015) have commented on the numbers of patients with vestibular migraine who demonstrate oVEMP abnormalities. Similarly, Makowiec and colleagues (2018) reported a relationship between the results of cVEMP and oVEMP tests and the diagnosis of vestibular migraine that may be a neurodiagnostic phenotype for vestibular migraine. This was a retrospective review of the records of 212 adult patients who were evaluated in the same tertiary care center. Patients who showed bilaterally absent

603

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Balance Function Assessment and Management

Table 26–8. Summary Table Showing Test Results That Might Be Encountered from a Patient with Vestibular Migraine Test

Structure Lateral

Superior

oVEMP

Utricle

Saccule

Posterior

Absent/ abnormal

cVEMP

Normal

vHIT

Normal

Rotary Chair

Normal

Caloric

Normal

Normal

Normal

Pattern of abnormal/absent oVEMP with normal cVEMP

VEMPs were excluded from the investigation. The dependent variable was 1 of 4 cVEMP and oVEMP test outcomes, which were as follows: (1) normal cVEMP + normal oVEMP, (2) abnormal cVEMP + abnormal oVEMP, (3) abnormal cVEMP + normal oVEMP, and (4) normal cVEMP + abnormal oVEMP. There was a significant relationship between the diagnosis of vestibular migraine and the cVEMP and oVEMP test outcomes. Specifically, 22% to 28% of the patients in groups 1 and 2 were diagnosed with vestibular migraine. However, none of the subjects (0 out of 17) in group 3 (abnormal cVEMP + normal oVEMP) were diagnosed with vestibular migraine, whereas, 72% of subjects (51 out of 71) in group 4 (i.e., normal cVEMP + abnormal oVEMP) were diagnosed with vestibular migraine. The abnormal oVEMP results in group 4 were either amplitude asymmetries or total unilateral absence of the oVEMP. Patients with normal cVEMPs and unilaterally abnormal oVEMPs were 87 times more likely to be diagnosed with vestibular migraine compared with patients with abnormal cVEMPs and normal oVEMPs. Similarly, Zeleski et al. (2015) reported a large number of bilaterally absent oVEMPs occurring in a significant proportion of patients with vestibular migraine (i.e., 28% bilaterally absent) compared with controls (0% bilaterally absent oVEMPs). When they were present, the amplitudes were significantly reduced and often asymmetric in the group with vestibular migraine. Our group has found that patients with VM as compared with those with other vestibular disorders are highly likely to have abnormal oVEMP and normal cVEMP. Additionally, we observed that patients with VM have asymmetric oVEMP, which is in line

with clinical, imaging, electrophysiologic, and cerebral blood flow studies that demonstrate asymmetry of brain electrophysiologic and hemodynamic functions in migraine. The mechanisms of VM are poorly understood and hypotheses on its pathophysiology largely derive from knowledge of migraine with aura pathogenesis. For example, calcitonin gene-related peptide (CGRP), the excitatory central neurotransmitter glutamate, and the potent vasodilator nitric oxide (NO) all are believed to play major roles in the mechanisms of the migraine aura and its accompanying manifestations of pain, photophobia, phonophobia, and nausea. These same substances are involved in normal and abnormal functions of the vestibular system. To this end, it has been shown that hair cells release CGRP (Popper, Ishiyama, Lopez, & Wackym, 2002). Furthermore, Lee and Jones have argued that glutamate is a major transmitter of the vestibular afferents (Lee & Jones, 2017). Also, NO is known to modulate vestibular nuclei function (Smith, 2000). Consequently, it is reasonable to hypothesize that aberrant modulation of CGRP, NO, or glutamate systems can manifest either as migraine with typical aura when the dural vessels and the occipital cortex are the underlying neuro-anatomic substrates, or as vestibular migraine when the vestibulo-ocular pathways are involved. In addition to the overlapping involvement of NO, CGRP, and glutamate in common forms of migraine with aura and VM, one can infer that reciprocal connections between the vestibular nuclei and the trigeminal nucleus caudalis (TNC) (Marfurt & Rajchert, 1991) may be implicated in VM. TNC is involved both



26. Topographical Localization of Vestibular System Impairment

in peripheral (e.g., neurogenic inflammation, endothelium-mediated vasodilation, peripheral sensitization) and in central (e.g., central pain transmission, central sensitization) migraine mechanisms.

Superior Semicircular Canal Dehiscence Syndrome Much has been written about the place that vestibular electroneurodiagnostics plays in the diagnosis of superior semicircular canal dehiscence syndrome (SSCDS). This area is addressed in detail in Chapter 16 and, as such, we will reprise this area briefly herein with Table 26–9 providing a summary of test findings. The disorder of SSCDS results in the creation of a “mobile third window” over the superior semicircular canal. This third window alters the impedance of the labyrinth with a resulting magnification of the force that is applied to the endolymph and otoliths in the saccule and utricle (e.g., think of the difference between jumping up and down on a firm surface compared with jumping up and down on a trampoline). The abnormally increased force in the affected otolith end organs results in abnormal augmentation of the cVEMP and

oVEMP. The abnormal augmentation is manifested in abnormally reduced VEMP thresholds (usually 150 deg/sec) and where those eye movements are replaced with overt and covert saccades. These findings suggest that the peripheral vestibular system is physiologically incapable of responding to stimuli from 0.003 Hz (i.e., the effective frequency of the stimulus of the caloric test), to 0.01 to 0.32 Hz (i.e., frequencies that are associated with the rotary chair test), to 1 to 6 Hz (i.e., the frequencies that are associated with the vHIT). Where this occurs the likelihood of restoration of function is poor. Physical therapy aimed at increasing the use of the remaining two interdependent senses for bal-ance (i.e., vision and the somatosenses) is important. In addition to difficulties with balance, bilateral vestibular failure can produce deficits in visuospatial memory. Brandt and colleagues (2005) reported that BVF was associated with a 16.9% reduction in the mass of the hippocampus. The impact of this impairment appears to be on visuospatial memory (i.e., as opposed to general memory). These are patients who might have difficulty finding their car in a large mall

Abnormally low gain

parking lot because they are unable to recall the relationship between the location of their car and visual landmarks. It is likely that sooner or later assessments of individuals with BVF will include assessment of cognitive functions such as visuospatial memory. There are a number of diseases and disorders that can result in BVF and these include: exposure to medications that have vestibulotoxic properties, genetic predisposition, and cerebellar ataxia, neuropathy vestibular areflexia syndrome (i.e., CANVAS).

Case Reports Demonstrating Reproducible Patterns that Occur in Clinical Data Case 1 For purposes of comparison, Case 1 (Figure 26–2, A–D) shows (A) caloric, (B) cVEMP, (C) oVEMP test results, and (D) lateral semicircular canal vHIT test results obtained from a patient with bilaterally normal peripheral and central vestibular system function.



26. Topographical Localization of Vestibular System Impairment

Figure 26–2.  A–D. Results of vestibular function studies for Case 1. The tests include:the caloric test, both ocular and cervical VEMP tests and lateral semicircular canal vHIT test results. For this case caloric, VEMP and lateral canal vHIT tests are normal. Accordingly, the patient shows no evidence of having a peripheral vestibular system impairment.

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Case 2 The patient is a 43-year-old male with a previous diagnosis of Ménière’s disease on the left side in 1993. In 1995 he underwent a left vestibular nerve section as a definitive procedure. The patient reported vertigo following the nerve section. The patient also reported a history of tinnitus and hearing loss on the left side. He reported that his hearing has become poorer on the left side. Over the past six months the patient felt slightly off-balance but denied vertigo, nausea, or vomiting. His medical history was significant for anxiety, ulcerative colitis, and gastroesophageal reflux disease. His physical examination was unremarkable. A brain MRI was interpreted as normal. Immittance testing showed

the patient to have bilaterally normal tympanometry and normal ipsilateral and contralateral acoustic reflex thresholds. An audiometric examination (Figure 26–3) showed the patient to have essentially normal pure tone thresholds on the right side and a mild, flat sensorineural hearing loss on the left side (i.e., the ipsilesional side). Results of quantitative vestibular testing (Figure 26–4, A–D) showed the patient to have an (A) absent caloric response, (B) an absent cVEMP, and (C) an absent oVEMP on the left side (i.e., the side of the vestibular nerve section). The vHIT results (D) were consistent with a deafferentation of the superior vestibular nerve.

Figure 26–3. Audiometric test results for Case 2. The patient has a mild-moderate sensorineural hearing loss with a small conductive component.



26. Topographical Localization of Vestibular System Impairment

Figure 26–4.  A–D. Vestibular function studies for Case 2. The pattern of results is consistent with a unilateral (leftsided), profound peripheral vestibular system impairment. See text for details.

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Case 3 The patient is a 50-year-old female with a six-week history of persistent true vertigo. The patient stated that the vertigo increased in severity with changes in her head position. The patient also reported a headache history, although she did not report a temporal relationship between the headaches and the vertigo. Her medical history was significant only for deep vein thrombosis in the left lower extremity and right upper extremity deep vein thrombosis. Immittance testing showed the patient to have normal tympanometry and ipsilateral and contralateral stapedial reflex thresholds

bilaterally. Pure tone audiometry (Figure 26–5) was bilaterally normal with the exception of a notched mild sensorineural hearing loss at 2000 Hz and 4000 Hz on the left side. Quantitative vestibular system testing (Figure 26–6, A–D) showed the patient to have a significant left-sided caloric asymmetry (43% asymmetry; A), a bilaterally symmetrical cVEMP examination (5% asymmetry; B), a significant left-sided oVEMP asymmetry (36% asymmetry; C), and an abnormal lateral canal vHIT on the left (D). Collectively the findings suggest a left-sided peripheral vestibular system impairment affecting the superior vestibular nerve.

Figure 26–5.  Audiometric test results for Case 3. The patient shows a mild, notched, left-sided, sensorineural hearing loss.



26. Topographical Localization of Vestibular System Impairment

Figure 26–6.  A–D. Results of quantitative vestibular function studies are consistent with a left-sided peripheral vestibular system impairment affecting the superior vestibular nerve. See text for details. That is, tests of the saccule and/or inferior vestibular nerve are normal whereas the caloric test and, probably the oVEMP tests are abnormal on the left side.

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Case 4 The patient is a 46-year-old female with a diagnosis of left Ménière’s disease. She received this diagnosis in 2000. The Ménière’s disease began with fluctuant vertigo and hearing loss, fullness, and tinnitus in her left ear. Over the past 10 years she has had spells of vertigo, hearing loss, and tinnitus occurring approximately every three months. In the more recent past the spells have occurred one to two times per week. She has been managed conservatively with a low salt diet, oral vestibular suppressants (diazepam), and transtympanic dexamethasone. The patient reported having had an MRI that was interpreted as normal. An audiometric examination (Figure 26–7) showed the patient to have an asymmetrical sensorineural hearing loss with poorer hearing on the left side. The impairment affected the high frequencies on the right side and was moderate

in degree. On the left side the hearing loss was flat and moderate in degree. The patient demonstrated normal tympanometry and normal ipsilateral and contralateral acoustic reflex thresholds bilaterally. Quantitative vestibular system testing (Figure 26–8, A–D) showed the patient to have symmetrical caloric responses (A; 16% asymmetry), an abnormally small cVEMP on the left side (B; 50% asymmetry), and bilaterally symmetrical oVEMPs (C; 8% asymmetry). The lateral canal vHIT examination (D) was normal. Collectively the findings suggested a left-sided peripheral vestibular system impairment affecting the saccule and/or the inferior vestibular nerve. As stated previously, there is no expected pattern of VEMP results in patients with Ménière’s disease, but the abnormal left cVEMP was on the expected side and in this case the only abnormal vestibular test finding.

Figure 26–7.  Audiometric test results for Case 4. The patient shows a moderate to severe sensorineural hearing impairment on the left side.



26. Topographical Localization of Vestibular System Impairment

Figure 26–8.  A–D. Quantitative vestibular test results supporting the presence of a left-sided peripheral vestibular system impairment affecting the saccule and/or the inferior vestibular nerve. That is, while the caloric and oVEMP test results are normal, the cVEMP test is abnormal. See text for details.

Case 5 Figure 26–9, A–D shows test results for an isolated right lateral semicircular canal impairment. This patient demonstrates a 68% right unilateral weakness (Figure 26–9, A–D) and an abnormal lateral canal vHIT on the right side (B). However, the cVEMP examination is bilaterally normal (C), as is the oVEMP exami-

nation (D). Taken together the results suggest that the saccule and inferior vestibular nerve are functioning normally. Additionally, the superior vestibular nerves are functioning normally (i.e., the oVEMPs are normal). The sole aberrations are the asymmetric caloric and vHIT tests, suggesting an impairment affecting the right lateral semicircular canal.

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Figure 26–9.  A–D. Quantitative vestibular function studies showing the patient to have an impairment affecting the right horizontal semicircular canal. That is, the oVEMP and cVEMP tests are normal suggesting normal superior and inferior vestibular nerves are functioning normally, however, the caloric test is abnormal suggesting an isolated horizontal canal impairment on the right. See text for details.

Case 6 This case illustrates test results for a patient with a right-sided utricular impairment. This patient (see Figure 26–10, A–D) shows a symmetrical (i.e., a 5%

asymmetry) monothermal warm caloric examination (Figure 26–10A). Additionally, the patient’s cVEMP test is bilaterally normal (e.g., there is a 2% amplitude asymmetry; B). The oVEMP examination revealed a 47% amplitude asymmetry which is abnormal (C). The



26. Topographical Localization of Vestibular System Impairment

Figure 26–10.  A–D. Results of quantitative vestibular function studies supporting the presence of an impairment affecting the right utricle. That is, unlike the previous case, the caloric test is bilaterally normal as is the cVEMP examination. However, the oVEMP test is abnormal on the right side. See text for details.

horizontal canal vHIT is normal (D). In total, the normal cVEMP suggests that both the saccules and inferior vestibular nerves are functioning normally. The normal caloric test tells us that the lateral semicircular canals are functioning normally, as is the superior division of the vestibular nerve. In this example the abnormal right oVEMP examination suggests a selective impairment of the right utricle.

Summary The vestibular test patterns discussed in this chapter are summarized in Table 26–2. These patterns are the most commonly encountered in everyday clinical practice. It is likely that, with time, we will identify additional diagnostic patterns.

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References Curthoys, I. S., & Manzari, L. (2013). Otolithic disease: Clinical features and the role of vestibular evoked myogenic potentials. Neuro-Otology, 33, 231–237. Hullar, T. E., & Minor, L. B. (1999). High-frequency dynamics of regularly discharging canal afferents provide a linear signal for angular vestibuloocular reflexes. Journal of Neurophysiology, 82, 2000–2005. Lee, C., & Jones, T. A. (2017). Neuropharmacological targets for drug action in vestibular sensory pathways. Audiology and Otology, 21, 125–132. Lee, J. Y., Park, J. S., & Kim, M. B. (2019). Clinical characteristics of acute vestibular neuritis according to the involvement site. Otology & Neurotology, 40(6). https://doi.org/​ 10.1097/MAO.0000000000002226 MacDougall, H. G., Garvie, L. A., Halmagyi, G. M., Curthoys, I. S., & Weber, K. P. (2013). Application of the video head impulse test to detect vertical semicircular canal dysfunction. Otology & Neurotology, 34, 974–979. Makowiec, K. F., Piker, E. G., Jacobson, G. P., Ramadan, N. M., & Roberts, R. A. (2018). Ocular and cervical vestibular evoked myogenic potentials in patients with vestibular migraine. Otology & Neurotology, 39, 561–567. Manzari, L., Burgess, A. M., McGarview, L. A., & Curthoys, I. S. (2013). An indicator of probable semicircular canal dehiscence: Ocular vestibular evoked myogenic potentials to high frequencies. Otolaryngology–Head and Neck Surgery, 149, 142–145. Marfurt, C. F., & Rajchert, D. M. (1991). Trigeminal primary afferent projections to “non-trigeminal” areas of the rat central nervous system. Journal of Comparative Neurology, 303, 489–511. McCaslin, D. L., Rivas, A., Jacobson, G. P., & Bennett, M. L. (2015). The dissociation of video head impulse test (vHIT) and bithermal caloric test results provide topological localization of vestibular system impairment in patients

with “definite” Meniere’s disease. American Journal of Audiology, 24, 1–10. McGarvie, L. A., Curthoys, I. S., MacDougall, H. G., & Halmagyi, G. M. (2015). What does the dissociation between the results of video head impulse versus caloric testing reveal about the vestibular system in Meniere’s disease? Acta-Otolaryngologica, 135, 859–865. Murofushi, T., Nakahara, H., & Yoshimura, E. (2012). Assessment of the otolith-ocular reflex using ocular vestibular evoked myogenic potentials in patients with episodic lateral tilt sensation. Neuroscience Letters, 515, 103–106. Park, J. S., Kim, C. H., & Min-Beom, K. (2018). Comparison of video head impulse test in the posterior semicircular canal plane and cervical vestibular evoked myogenic potential in patients with vestibular neuritis. Otology & Neurotology, 39, e263–e268. Pelosi, S., Schuster, D., Jacobson, G. P., Carlson, M. L., Haynes, D. S., Bennett, M. L., Rivas, A., & Wanna, G. P. (2013). Clinical characteristics associated with isolated unilateral utricular dysfunction. American Journal–Head and Neck Medicine and Surgery, 34, 490–495. Popper, P., Ishiyama, A., Lopez, I., & Wackym, P. A. (2002). Calcitonin gene-related peptide and choline acetyltransferase colocalization in the human vestibular periphery. Audiology and Neurotology, 7, 298–302. Seo, T., Miyamoto, A., Node, M., & Sakagami, M. (2008). Vestibular evoked myogenic potentials of undiagnosed dizziness. Auris Nasus Larynx, 35, 27–30. Smith P. F. (2000). Pharmacology of the vestibular system. Current Opinion in Neurology, 13, 31–37. Tsuji, K., Velazquez-Villasenor, L., Rauch, S. D., Glynn, R. J., Wall, C., III, & Merchant, S. N. (2000). Temporal bone studies of the human peripheral vestibular system: Meniere’s disease. Annals of Otology, Rhinology, and Laryngology, 181​ (Suppl.), 26–31. Zaleski, A., Bogle, J., Starling, A., Zapala, D. A., Davis, L., Wester, M., & Cevette, M. (2015). Otology & Neurotology, 36, 295–302.

27 Challenging Cases Neil T. Shepard

Introduction The following four cases represent ones that were difficult to diagnose with a single diagnosis, requiring multiple diagnoses to explain their symptoms. Also, they were difficult to diagnose and manage without the use of an interprofessional practice (IPP) team. While challenging, these are not outside the range of possibility for the types of dizzy problems that could show up at any clinic that specializes in the dizzy patient. Whether a clinic has the breadth of knowledge and experience to deal with these complex cases is important to recognize so referrals to an appropriate facility could be made at the outset. Therefore, the purpose for this chapter is to provide examples of patients who need a true collaborative practice model. The IPP team that consulted on these patients were in the Dizziness and Balance Disorders Program at the Mayo Clinic in Rochester, Minnesota. This was a fully integrated IPP team where an initial triage was used to decide on the appointments needed for the patient and then all the appointments (in the different departments) were established (by a specially trained scheduler) and given to the patient. The appointments were typically over a three- to fiveday interval. The triage process consisted of a questionnaire and review of the patient’s outside records by one of four audiologists trained to recognize the information that would call for consults by various professionals within the multidisciplinary program along with testing needed prior to the consults. The consultations could be in medical ENT, neurotology, neurology (specialist in dizziness), psychiatry (specialist in dizziness), audiology, imaging studies (CT/MRI), physical therapy (therapist trained specifically in vestibular and bal-

ance rehabilitation therapy), gerontology (division of primary internal medicine), pediatric neurology, and pediatric psychiatry. Each of the consults resulted in an entry into the electronic health record prior to the next consult (or a private note to the next consultant). Usually, the last consultant would pull together the recommendations from the prior consults and make sure the patient was aware of the overall treatment plan.

Case 1 43-Year-Old Female Patient’s Chief Complaint and Past Medical History from the Questionnaire and Outside Clinic Notes The patient’s primary symptom complaint was that of constant non-vertiginous dizziness exacerbated by head/visual motion, visual complexity, and reading. In addition, she reported episodic spontaneous vertigo events. Based on her outside clinical records, she had in the past and currently received diagnoses of migraine headaches. She was reported in 1999 to have documented fluctuant and progressive hearing loss on the left. In 2000 she began to have spontaneous vertigo events, each lasting one to two hours multiple times per month. Ménière’s disease on the left side was diagnosed by an outside neurotologist and the patient started on dietary restrictions and a chemical diuretic. These measures proved unsuccessful. In 2004 she underwent a left endolymphatic sac decompression procedure and

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obtained good control over her spontaneous spells of vertigo for a period of three years. In 2007 she again started with spontaneous spells of vertigo; however, the first spell of external vertigo lasted constantly for four days and then resolved. The spells began to increase in frequency and were typically longer than 24 hours for the external vertigo. (Note: by the diagnostic criteria for Ménière’s disease by the International Classification of Vestibular Disorders committee of the Barany Society, the spells of external vertigo can last up to 24 hours but not longer [LopezEscamez et al., 2015].) It is reported that between the vertiginous spells she would have non-vertiginous dizziness provoked by visual complexity and moving visual scenes. As the spells increased in 2007 into 2008, she began having falls with the spells. Therefore, in 2008 she had a left vestibular nerve section. This provided good control of the spontaneous events along with a reduction in visually provoked symptoms of non-vertiginous dizziness but not an elimination of these symptoms for the subsequent year. After a year’s time, the spontaneous spells began to return and continued into 2009. The surgeon had a suspicion of an incomplete nerve section that was allowing the Ménière’s disease to manifest again in symptoms. In 2009, 50% of spontaneous events were followed by a focal headache, with the other 50% with light and odor sensitivity. She was offered a labyrinthectomy but declined and sought a second opinion for her symptoms at the Mayo Clinic in Rochester. Patient’s Neurotologic History and Test Results Obtained at the Mayo Clinic She was seen by this author and the following history was obtained. Her current symptoms were a sensation of self-motion (vertigo in her head) that was present 24/7, exacerbated with head movement, visual motion, visual complexity, and repeated noise. Added to this were spontaneous events of external vertigo. She reported falls but these did meet criteria for a Tumarkin crisis event (she did not describe loss of tonus in the anti-gravity muscles, but a loss of balance with the spells of external vertigo). She clearly met the criteria for migraine headaches in the past as well as at the current time by the International Classification of Headache Disorders, third edition (ICHD III) (IHS, 2018). She also met the criteria for vestibular migraines (Lembert et al., 2012). She continued to report left hearing fluctuations with the spontaneous spells of vertigo. Other than postoperative changes she had a normal MRI of the brain without and with contrast and normal internal auditory canals bilaterally. She had been seen

earlier in the day for a hearing evaluation (Figure 27–1) and full vestibular function tests that showed no abnormal nystagmus with or without visual fixation present. Mild disruptions in smooth pursuit but in the presence of a normal MRI was interpreted as likely related to her migraine headaches. Clinical head impulse tests, with warm and ice water caloric tests and rotational chair all showed a severe left peripheral hypofunction in a partial state of physiologic compensation but with minimal residual function remaining on the left. Clinical Impressions at This Point

1. The patient likely had left Ménière’s, but this was no longer active. 2. The present cause for the spontaneous spell of vertigo was that of vestibular migraine. 3. She had developed persistent postural perceptual dizziness (PPPD; Staab et al., 2017) that was causing her daily background symptoms. Recommendations at This Point

1. Consult with neurotologist regarding possibly active Ménière’s disease (already established). 2. Consult with neurotologist who specialized in dizziness for review of possible active vestibular migraine as the current cause for the spontaneous event of vertigo (already established). 3. Consult with psychiatrist who specialized in dizziness for review of the likely development of PPPD as the current cause for her background symptoms. 4. Initiate vestibular and balance therapy for her sensitivities to a variety of head movements, visual motion, visual complexity, visual patterns with habituation style of exercises (she did not need gaze stabilization exercises). Impressions from the Three Additional Consults n Neurotologist — Left Ménière’s not the likely

cause of current symptoms, more likely vestibular migraine with PPPD. n Neurologist — Left Ménière’s not the likely cause of the current symptoms with vestibular migraine resulting in the vertigo events together with the development of PPPD. n Psychiatrist — Patient meets criteria for PPPD together with that of vestibular migraine, both of which are currently active in producing her symptoms. Ménière’s is not currently active, but she has major depression, posttraumatic stress disorder, and additional psychological factors affecting her ongoing medical conditions.

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Figure 27–1.  Shown is the audiogram and associated speech and immittance test results for the patient in Case 1.This demonstrates normal pure tone hearing thresholds with excellent speech recognition on the right with normal tympanogram and acoustic reflexes. The left ear shows a moderate sensorineural hearing loss with 70% speech recognition and again normal tympanogram and acoustic reflexes. Refer to the key in the figure for explanation of the symbols.

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Overall Recommendation The above impressions were summarized for her at the psychiatric consult, which was her final consult prior to meeting with the physical therapist to initiate that aspect of her treatment plan. It was recommended:

within a four-day interval. Therefore, while there was a delay in getting assessment and treatment started, the wait for an integrated IPP team was worthwhile.

Case 2

n She should maintain current medication for

depression. n Prophylactic migraine therapy was to be started first with non-antidepressant (e.g., topiramate, gabapentin). n She should start habituation exercises for desensitization for visual motion and complexity and cognitive behavioral therapy if this is available in her local area. n There should be no further aggressive treatment for Ménière’s. Learning Points n Even though the initial diagnosis may well

be correct for what was causing the beginning symptoms, this needs to be revisited, especially as symptoms change in character. It is important not to lose sight of the fact that the current symptoms may be from other disorders that now are taking center stage. In this case, migraine headaches were always present, but it wasn’t until the spells started to take on a character too long for Ménière’s disease that vestibular migraine should have been considered as an alternative to Ménière’s. n As with other patients who have multiple diagnoses, decisions need to be made as to what is giving the patient the most difficulty and the greatest functional impairment and start treatment with that focus. In this case it seemed apparent that vestibular migraines and PPPD were at the center of all her current symptoms and therefore that is where the focus of the treatment was aimed. She may well have minor aspects of Ménière’s, but this is not causing any major symptoms at this point and therefore the recommendation that no further aggressive treatment should be used for Ménière’s, as that could well add to her present symptoms and overall increase of her symptoms. n She had to wait four months to be scheduled for the above listed appointments, but once they were started, all the above took place

37-Year-Old Male Patient’s Chief Complaint and Past Medical History from the Questionnaire and Outside Clinic Notes The patient’s chief complaints were heart palpitations that have subsided with lightheadedness and vertigo in spells that have continued to date. Outside clinic notes on the referral revealed that in 2015 of December he began to experience lightheadedness and vertigo with heart palpitation after the use of Propecia and Rogaine for hair loss. The palpitations subsided but the dizziness continues. He was diagnosed with benign paroxysmal positional vertigo (BPPV) initially that was suggested as unilateral at first, then changed to bilateral. Additionally, the patient reports that he has difficulty walking in the dark. A prior vestibular evaluation was reported as finding “vestibular dysfunction,” and oscillopsia was subsequently diagnosed. No further details were provided. An MRI of the brain and cervical spine with an MR angiography (MRA) of the brain indicated all without and with contrast showed normal findings. Electrocardiograms, Holter monitor, and a stress echocardiogram were all also reported as normal other than a few premature ventricular contractions. A subsequent cardiovascular consult did not find the dizziness to be related to his cardiovascular complaints of heart palpitation and he was started on medication to be used for control of the palpitations. Patient’s Test Results and Neurotologic History Obtained at the Mayo Clinic in December 2015 Audiometrics demonstrated normal pure tone hearing with 4 kHz notch thresholds and 100% speech recognition with normal immittance bilaterally. Vestibular and balance studies revealed negative findings for anxiety and depression via the Hospital Anxiety and Depression Scale (HADS) (Zigmond & Snaith, 1983). No abnormal nystagmus without or with visual fixation was present. Pursuit and saccade tests



were normal (see Chapter 10). Video Head Impulse Test (vHIT) demonstrated severely low gains (2 kHz. The hearing test was repeated ×2 in March 2008 with no change in hearing bilaterally. Also in March 2008 he had an MRI of the brain without and with contrast, with an IAC protocol that was reported as fully normal. In April 2008 he underwent a videonystagmography (VNG) that demonstrated a 63% right reduced vestibular response (RVR) with normal ocular motor findings. He was seen by an ENT, and Ménière’s disease on the right was diagnosed secondary to the hearing loss greater on the right, and the spontaneous spells of vertigo with durations reported to be minutes to hours. By May 2008 he was reported to have had three additional spells of spontaneous vertigo. His audiogram at that time showed a significant improvement in hearing on the right to match that of the left. A repeat audiogram in July 2008 demonstrated a return of the low-frequency hearing loss in the right. He reported that loud sounds would cause an increase in his now constant unsteadiness.



In August 2009 he was again seen by an ENT with symptoms continuing. It was recommended that he stay on a low sodium diet and take Dyazide (i.e., diuretic) along with Meclizine and Valium on a regular basis daily. Audiometric evaluation in 2012 showed left ear hearing to be unchanged from 2008. The right now showed a moderate SN loss across frequencies (0.25 to 8 kHz). Patient’s Test Results and Neurotologic History Obtained at the Mayo Clinic Spring 2015 Audiometrics demonstrated a mild to severe SN loss 2 to 8 kHz, with 90% speech recognition on the left. The right ear showed poor normal to severe SN loss 0.25 to 8 kHz, 80% speech recognition and normal immittance bilaterally. Vestibular and Balance Studies.  Patient was nega-

tive for anxiety/depression via HADS test (Zigmond & Snaith, 1983). No abnormal nystagmus with visual fixation was present. However, up-beat nystagmus was noted when visual fixation was removed only for gaze up. Hallpike and roll tests were negative. Pursuit and saccade tests were normal. Alternating bithermal water caloric irrigations demonstrated a 59% right RVR with no significant directional preponderance (see Chapter 12). Sinusoidal total body rotational chair showed a mild increased phase lead at 0.01 Hz and normal phase from 0.04 to 0.32 Hz, with normal gain across all frequencies and a marginal right to left slow component velocity asymmetry implying a right hypofunction (or left irritative lesion, but by the caloric test the right hypofunction was consistent with the other tests) (see Chapter 13). Ocular and cervical VEMPs were normal bilaterally. The cVEMP threshold response curves showed an upward shift in the most sensitive frequency, bilaterally (Zhu et al., 2014). Video HIT showed normal gain for all six semicircular canals. Postural control assessment was normal for reaction to induced forward and backward sway (MCT) and for maintaining quiet stance under changing sensory input conditions (SOT). Direct office exam taken by the author in the evening after the vestibular function testing in the morning showed left beating, left and right mastoid vibration induced nystagmus with visual fixation removed (see Chapter 9). No other nystagmus with or without visual fixation present was noted. Pursuit and saccade testing and ocular counter roll responses for static roll of the

27.  Challenging Cases

head to the right and left were normal. Horizontal and vertical post-headshake nystagmus was negative. He was negative for palatal tremor and was normal on all aspects of his cranial nerve examination and general neurological examination. His otologic examination was normal for the external auditory canals with normal tympanic membrane movement. Summary of his findings showed right peripheral vestibular hypofunction in a partially compensated state physiologically for nystagmus (had mild asymmetry on rotary chair) and fully compensated state functionally for maintaining quiet stance (his SOT results were normal). No indications of central vestibular system involvement were noted. Direct interview was taken by this author. First, the patient denied ever having any form of head injury or skull fracture from a motorcycle accident. He reported that in the 1970s, noise exposure to his right ear produced a hearing loss on the right side that has been with him to present. While this could be the explanation for the right hearing loss, it does not rule out the development of a form of Ménière’s disease (old term, delayed endolymphatic hydrops) that can develop from a longstanding hearing loss (Lopez-Escamez et al., 2015). In 2007 he developed an upper respiratory infection (URI) and suffered an increased hearing loss on the right with aural fullness. After the resolution of URI, the increased hearing loss and aural fullness remained through to present. Two months after the URI he started having spontaneous spells of external vertigo ranging 15 to 30 minutes, multiple times per month continuing to present. Headaches or light sensitivity were both denied with these shorter spells of vertigo. Over the years he began to have infrequent spells of external vertigo these lasting one to six hours, at a frequency of four or five spells in the prior 12 months. He reports that 100% of the long spells (one hour or greater) had significant photophobia and all spells long or short had phonophobia that occurred with the spells. His detailed headache history showed that he met ICHD criteria for migraine headaches in the past, with ocular migraines past and present with one headache/year meeting migraine criteria. (IHS, 2018). Given the accompanying symptoms with the long spells of dizziness, those met the criteria for vestibular migraine (Lempert et al., 2012); however, the phonophobia (sensitivity to sounds) for the shorter spells in isolation could well be a component of Ménière’s disease or migraine. He reports an increase in tinnitus and aural fullness on the right with decrease in hearing on the right, all resolving after the spell resolves. This is a symptom

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that can be attributable to Ménière’s disease, but this is also reported with migraine events. Starting after the spells in 2007 he began to realize he was not returning to a normal baseline between the spontaneous spell with unsteadiness/dizziness between the spells. These background symptoms have increased in frequency and duration, so currently they are 24/7. These symptoms are now reported to be worsened with postural changes, visual motion (limited), visual complexity, visual patterns, and limited head movements that are rapid or repeated in nature. Impressions and Learning Points n Does he have Ménière’s disease on the right?

A diagnosis of Ménière’s disease can’t be ruled out given the fluctuant hearing, vestibular hypofunction right, normal vHIT, shift up in cVEMP most sensitive frequency (bilaterally), and spells of spontaneous vertigo, but what is missing? Progression of hypofunction over seven years in the presence of repeating vertigo spells. If these were of a Ménière’s origin, you would expect some progression of his hypofunction and at the time he was seen at Mayo for vestibular testing his caloric testing was the same as that obtained in 2008. Progression of hearing loss on the right over 7 years would be expected if the hearing loss described were fluctuations due to Ménière’s disease. His original hearing loss was from noise exposure and was exacerbated by a URI, which could make the typical progression in hearing loss different from that where Ménière’s disease is the origin. n What is the most likely cause for the longer

spell?

Vestibular migraine. Meeting ICHD criteria for migraine headaches and criteria for vestibular migraine makes a very good case for these longer spells being of migraine origin. Does this rule out Ménière’s disease? No, vestibular migraine and Ménière’s disease can coexist and both be responsible for a portion of the spells the patient experiences. n What is causing the persistent background

symptoms between spells?

Likely PPPD. He meets the diagnostic criteria for this disorder (Staab et al., 2017). Could the constant symptoms be secondary to the peripheral asymmetry that is only partially compensated?

The asymmetry would not cause the sensitivity to visual stimuli but could increase sensitivity to rapid head movements. n What are his major problems?

Vestibular migraine and PPPD would be the primary sources of his major symptoms and we could assume that not only the long spells but also the shorter ones are both of migraine origin. Recommendations n Consult with neurotology re the possible

Ménière’s disease and any suggested treatment. n Consult with a behavioral medicine program for dizziness in psychiatry for the PPPD and possible vestibular migraine (the psychiatrist who specializes in dizziness is also an expert in vestibular migraine). n Consult with physical therapy for initiation of habituation exercises for head movement sensitivity, sensitivity to visual motion and patterns (visual vertigo exercises) and visual complexity (store walking exercises). As with the patient in Case 1, he does not need balance and gait exercises or gaze stabilization exercises, since he has no complaints or finding in these two areas. If controlling the vestibular migraine events stops all the spells, then there is no Ménière’s disease active currently. If controlling the vestibular migraine events only stops the longer events, then what is left may need to be treated as active Ménière’s disease. He was seen by one of the neurotologists and it was felt that his presentation was not classic for active Ménière’s disease. He was also seen in the behavioral medicine division of psychiatry and that consult revealed that he did have PPPD and vestibular migraine and recommended: n Start venlafaxine (Effexor) 37.5 mg for two

weeks then 75 mg with increase up to 150 mg as needed. This serotonin-norepinephrine reuptake inhibitor may take care of migraine activity as well; if not, an additional prophylactic may be needed (see Chapter 23 for a discussion of the medications used for PPPD and migraine). n Start vestibular and balance therapy for habituation exercises (Thompson et al., 2017).



27.  Challenging Cases

Case 4

for stimulation to the right and fully absent reflexes for stimulation to the left consistent with the degree of hearing loss. 81-Year-Old Female Vestibular and balance studies revealed negative for anxiety but positive for depression via HADS Patient’s Chief Complaint and Past test. No abnormal nystagmus without or with visual Medical History from the Questionnaire fixation present. Hallpike and roll tests were negative and Outside Clinic Notes bilaterally. Pursuit and saccade tests were normal when The patient’s chief complaint from her intake question- compared with age related normative ranges. Ice water naire was that of 24/7 unsteadiness/dizziness exac- caloric irrigations (50 cc of 2 to 3 deg C water over a erbated by visual motion, head movements, visual 15 sec interval) gave absolute responses of 9 deg/sec complexity, and walking in the dark. She reported from the right and 3 deg/sec from left. Sinusoidal rotary chair demonstrated significantly onset of symptoms in 2012. abnormal phase lead of a magnitude that would be From her provided outside records, in 1998 an supportive of bilateral pathology (phase angle greater audiogram demonstrated normal hearing on the right than 68 deg), abnormally low gain from 0.01 to 0.08 with a moderate to severe SN loss on the left first Hz with left > right SCV asymmetry 0.01 to 0.04 Hz noticed with gentamicin use for peritonitis in 1981. (implying a left hypofunction greater than the right In 2004 repeat audiogram demonstrated normal hearhypofunction) (see Chapter 13). ing on the right but the left now showed a flat severe Video HIT showed low gains for both horizontal SN loss with 16% speech recognition. Another repeat and posterior canals with normal gain for the anterior audiogram was performed in 2012, again with normal canals. hearing on the right and the left with the flat severe Ocular VEMPs were absent bilaterally with the SN loss but now 72% speech recognition and normal cervical VEMP absent on left and marginally present immittance bilaterally. on the right. These findings imply possible bilateral In 2012 a VNG was performed which reported no otolith involvement for the utricles and saccules or response to caloric irrigations (the report did not indiboth superior and inferior vestibular portion of the VIII cate whether this was performed using air or water — ​ nerve involvement (see Chapter 16). water is the more reliable  — see Chapter 12) on the left Postural control assessment by the MCT gave norwith the right giving absolute responses of 6 to 7 deg/ mal results for reaction to induced forward and backsec for warm and cool irrigations, and otherwise a fully ward sway. SOT showed 4/6 fall reactions when foot normal study. support surface cues were simultaneously disrupted In 2015 an MRI of the brain without and with conwith absent or disrupted visual cues. Raw traces for trast with IAC protocol was performed. The results both the MCT and the SOT showed high frequency low showed symmetric bilateral hypertrophic olivary degenamplitude sway and a ringing behavior after center eration (a finding that is many times associated with a direct clinical finding of oculo-palatal myoclonus but to of mass perturbations (a continuing oscillating behavdate this had not been reported to have been investi- ior that slowly diminishes). This is likely a reduction gated or seen). Mild to moderate diffuse parenchymal in the proprioceptive/somatosensory input from the volume loss without hydrocephalus were considered ankle/plantar surface of the foot, and this finding age related changes. MRI of the neck without and with needs to be verified with direct examination for poscontrast, compared with MRA neck December 2011 sible sensory neuropathy (Diener, Dichgans, Bacher, & showed stable mild proximal right subclavian artery ste- Guschlbauer, 1984). Mayo direct interview was taken by the author. nosis, possibly related to posterior kinking of the vessel. She reports noticing unsteadiness worse in the dark after the 1981 gentamicin treatment along with left Patient’s Test Results and Neurotologic History side hearing loss. She continued to walk and force the Obtained at the Mayo Clinic November 2015 issue of unsteadiness, and over time when in good Audiometrics showed mild to moderate SN loss 6 to lighted situations, the unsteadiness resolved but con8 kHz with 100% speech on the right but a severe SN tinued to the present to have problems in the dark. She loss 0.25 to 6 kHz with profound loss at 8 kHz and 0% denied any oscillopsia until this last year and then only speech on the left with normal tympanograms bilater- with rapid walking. In 2012 she reports the return of ally with normal contra and ipsilateral acoustic reflexes unsteadiness in the light but denied any symptoms

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when sitting or any symptoms provoked by or exacerbated by visual motion or visual complexity when sitting, but these bother her when standing and walking. As a result of these symptoms, she is now withdrawing from social situations and staying at home with her husband, further isolating herself. Direct office examination was performed by the author. Gait was normal for stride length, heal toe strike, walking on heels and toes but she was unable to perform tandem walking with eyes opened. Saccadic testing was normal and pursuit testing was explainable by age. Ocular counter roll was absent to the right and left. Clinical HIT was positive for both lateral canals. Mastoid vibration provoked right beating nystagmus. Pneumatic otoscopy was normal other than exostosis of the external auditory canals bilaterally (she had a history of cold-water swimming as a child and teenager). Normal neurological and cranial nerve evaluation was negative. No palatal tremor or pendular nystagmus was noted but the examination was done without the use of a tongue blade. Deep tendon reflexes were 0/3 (absent) at the ankles, 2/3 (mildly reduced) at the knees, 3/3 (normal) at the elbows. She showed a moderate reduction in vibratory sensation at both ankles and absent at the great toe on the left and reduced at the great toe on the right. She had normal strength and range of motion in the lower limbs bilaterally. Impressions and Learning Points n Is there a bilateral hypofunction?

Yes, evidenced by hypofunction in the horizontal/posterior canals and utricles bilaterally. The saccule on the left showed marginal functioning and the one on the right was normal with preserved anterior canals. n Was this a result of the gentamicin in 1981? If

so, why greater involvement on the left?

Good evidence to suggest that the gentamicin was the cause of the bilateral hypofunction. She effectively did her own therapy and was able to do very well until 2012. n Does gent always affect both labyrinths in the

same manner?

n Are there any indications for central system

involvement?

None from our laboratory testing or from the direct examination that was performed, but the MRI findings are of concern for ataxia. She was seen the next day by the neurologist that specializes in dizziness and balance disorders with the same findings as given above for the direct examination. However, when he looked for palatal tremor, he was able to get her tongue down and got a good look at the post pharyngeal space and did observe palatal tremor that was synchronous with very subtle pendular nystagmus. This is shown in Video 27–1 on the companion website. It is very easy to perform the look for the palatal tremor and takes less than a minute, but the use of a tongue blade is important to get a good look at the post pharyngeal space. This is a low yield test, but it is important not to miss this sign, and if seen and the patient has not had an MRI it would be important to acquire the MRI. Final Impressions n Bilateral peripheral vestibular hypofunction

secondary to gentamicin use with asymmetrical effect on both the vestibular system and hearing worse on the left. n Progressive ataxia with oculopalatal tremor from inferior olivary hypertrophic degeneration. n Mild to moderate sensory neuropathy. n No indications of CANVAS, since the bilateral hypofunction is not idiopathic. Recommendations n Initiate a vestibular and balance rehabilitation

program for bilateral hypofunction. She was provided with this program in writing. She was to follow up in her local area with a physical therapist trained to provide the rehabilitation. n Seek psychological consult regarding her depression and developing agoraphobic behavior.

Typically, but you can have differential effects as shown here (Fee, 1980). n What else could be exacerbating her unsteadi-

ness working synergistically with the bilateral hypofunction?

The noted mild to moderate sensory neuropathy.

References Diener, H. C., Dichgans, J., Bacher, M., & Guschlbauer, B. (1984). Characeteristic alterations of long-loop “reflexes” in patients with Friedreich’s disease and late atrophy of



cerebellar anterior lobe. Journal of Neurology, Neurosurgery, and Pschiatry, 47(3), 580–592. Fee, W. E. (1980). Aminoglycoside ototoxicity in the human. Laryngoscope, 90, 1–19. Frejo, L., Giegling, I., Teggi, R., Lopez-Escamez, J. A., & Rujescu, D. (2016). Genetics of vestibular disorders: Pathophysiological insights. Journal of Neurology, 263(Suppl. 1), 45–53. IHS (International Headache Society). (2018). The International Classification of Headache Disorders, 3rd ed. Cephalgia, 38, 1–211. Jen, J. C. (2011). Genetics of vestibulopathies. Advances in OtoRhino-Laryngology (Basel), 70, 130–134. Lempert, T., Olesen, J., Furman, J., Waterston, J., Seemungal, B., Carey, J., Bisdorff, A., . . . Newman-Toker, D. E. (2012). Vestibular migraine: Diagnostic criteria. Journal of Vestibular Research, 22(4), 167–172. Lopez-Escamez, J. A., Carey, J., Chung, W. H., Goebel, J. A., Magnusson, M., Mandala, M., . . . Bisdorff, A. (2015). Diagnostic criteria for Ménière’s disease. Journal of Vestibular Research, 25(1), 1–7. Staab, J. P., Eckhardt-Henn, A., Horii, A., Jacob, R., Strupp, M., Brandt, T., & Bronstein, A. (2017). Diagnostic criteria

27.  Challenging Cases

for persistent postural-perceptual dizziness (PPPD). Journal of Vestibular Research, 27(4), 113–125. Strupp, M., Kim, J., Murofushi, T., Straumann, D., Jen, J. C., Rosengren, S. M., Della Santina, C. C., & Kingma, H. (2017). Bilateral vestibulopathy: Diagnostic criteria. Journal of Vestibular Research, 27(4), 177–189. Szmulewicz, D. J., McLean, C. A., MacDougall, H. G., Roberts, L., Storey, E., & Halmagyi, G.M. (2014). CANVAS an update: Clinical presentation, investigation and management. Journal of Vestibular Research, 24, 465–474. Thompson, K. J., Goetting, J. C., Staab, J. P., & Shepard, N. T. (2015). Retrospective review and telephone follow-up to evaluate a physical therapy protocol for treating chronic subjective dizziness: A pilot study. Journal of Vestibular Research, 25, 97–104. Zhu, Y., McPherson, J., Beatty, C., Driscoll. C., Neff, B., Eggers, S., & Shepard, N. T. (2014). Cervical VEMP threshold response curve in the identification of Ménière’s disease. Journal of the American Academy of Audiology, 25, 278–288. Zigmond, A. S., & Snaith, R. P. (1983). The Hospital Anxiety and Depression Scale. Acta Psychiatrica Scandinavica, 67, 361–370.

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Appendix I

Pathophysiology Signs and Symptoms of Dizziness Neil T. Shepard

Introduction The discussion to follow is formatted differently than the rest of the chapters in this text. At the end there are suggested additional readings in place of the traditional references. These readings contain further details about the disorders discussed below and the interested reader is referred to these for more information. The structure of this chapter is that of a variety of different pathologies, both peripheral and central, that result in primary complaints of dizziness. This is not meant to be an exhaustive list but to include major disorders that one could expect to encounter in a clinic specializing in problems with balance and dizziness. These are introduced with a vignette for each, giving symptoms, signs, classic treatments, prognosis for recovery, and suspected lesion site. It was felt that while further information on each of the disorders can be had from the additional readings (and in some chapters of this text), this would serve as a quick reference for other chapters of this text. The disorders are organized peripheral to central and common to rare within the peripheral and central categories. First, we start with some general information related to the pathophysiology of the production of dizziness symptoms.

What Is Meant by Dizziness From the International Classification of Vestibular Disorders committee of the Barany Society, a published

attempt has been made to put definitions with terms commonly used by patients to describe their symptoms. In general, as we proceed with the vignettes for the disorders, this language will be used for consistency. Basically short definitions given are: n Vertigo — any sensation of movement when

not occurring

n Unsteadiness — general or actual ataxia and

possible falls

n Anything that is not vertigo/unsteadiness

is dizziness (e.g., lightheadedness [near syncopal event], giddiness); and combinations of the above.

In taking the patient’s history it is important to obtain symptom descriptions that are specific in nature. Detailed characterizations of the patient’s symptoms can be of significant help in narrowing the etiological possibilities for the patient. The reader is referred to Chapter 7 for a detailed discussion of the elements needed in the history that is acquired from the patient with dizziness. To characterize a patient’s symptoms the following characteristics are needed. 1. Temporal course of the symptoms — Are they paroxysmal lasting measured in sec, minutes, hours, days, weeks OR are they continuous with exacerbation lasting sec, minutes, hours, days, weeks? 2. Type of dizziness — Are the symptoms that of vertigo, unsteadiness, falls, dizziness (lightheadedness), disorientation? Are there traveler symptoms

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along with the primary complaints? These can include nausea and vomiting, headaches, heart palpitations, feelings of panic, drop attacks without and with loss of consciences, any of the “Ds,” diplopia, dysphagia, dysarthria, dysmetria, and asymmetric muscle weakness. The importance about recognizing any of the “Ds” is that these symptoms point to the posterior fossa as a possible source for the symptoms. 3. Onset of symptoms — If episodic, do the symptoms start spontaneously, OR are they provoked by head motion or visual motion? Symptoms that are truly spontaneous only are not helped with the use of vestibular and balance therapy whereas those that are provoked by something can many times be approached with vestibular rehabilitation therapy. Note you can have combinations of spontaneous and provoked symptoms. 4. The patient’s perception of their hearing — This can signal involvement in the auditory system, e.g., tinnitus, aural fullness, progressive or fluctuant loss of hearing unilaterally or bilaterally. Table AI–1 shows how the symptom characterizations can be used to help reduce the etiological possibilities for an individual patient. The table is not meant to be exhaustive by any means but is used as an example. Next would be the addition of signs from the clinical direct or laboratory examinations to add to the information from the symptoms.

Vertigo Without and With Labyrinthine Involvement Independent of the lesion site, the underlying pathophysiology for the generation of the symptom of external vertigo requires that two constraints be met, these are: 1. asymmetrical neural activity must exist between the left and the right, and 2. the asymmetry must develop rapidly. The asymmetrical neural activity could occur anywhere from the labyrinth through lesions in the pons and even posterior cerebellum. It is, however, highly unlikely to get external vertigo from a lesion above the level of the pons — more likely to get unsteadiness/imbalance and/or lightheadedness. It is equally as unlikely to get external vertigo from a lesion in the areas served by the anterior circulation — carotid arteries. Here again unsteadiness/imbalance and/or lightheadedness would be the more common symptoms. Differentiation of labyrinthine versus posterior fossa lesions by symptoms would typically involve the presentation of one or more of the Ds. It is possible to have labyrinthine involvement without the symptom of vertigo by not having one of the two constraints given above realized. This would be in the realm of “Chronic Dizziness.” Unilateral Labyrinthine/VIII n involvement can occur without vertigo if the lesion develops slowly and insidiously, and the central compensation process is functioning normally,

Table AI–1.  Characterizations of the Symptoms and How They Narrow the Differential Diagnosis Temporal Characteristics

“Dizziness” Characteristics

Auditory Characteristics

Episodic Seconds

HM–HP provoked

Normal

BPPV; Uncomp stable lab; VBI

Episodic Sec– Min 20% difference between CW & CCW directions?

Significant asymmetric results in peak SPV indicate peripheral UVL and side of loss

Eye closure (eyes must be open when chair starts and stops)

References Akin, F. W., Murnane, O. D., Pearson, A., Byrd, S., & Kelly, J. K. (2011). Normative data for the subjective visual vertical test during configuration. Journal of the American Academy of Audiology, 22(7), 460–468. Baloh, R. W., & Honrubia, V. (1990). Clinical neurophysiology of the vestibular system (2nd ed.). Philadelphia, PA: F.A. Davis. Baloh, R. W., & Honrubia, V. (1998). Vestibular physiology. In C. Cummings, J. Fredrickson, L. Harker, C. Krause, M. Richardson, & D. Schuller (Eds.), Otolaryngology–head and neck surgery (3rd ed., pp. 2584–2622). St. Louis, MO: Mosby. Baloh, R. W., & Honrubia, V. (2001). Clinical neurophysiology of the vestibular system (3rd ed.). Philadelphia, PA: F. A. Davis. Baloh, R. W., Honrubia, V., & Kerber, K. A. (2011). Baloh and Honrubia’s clinical neurophysiology of the vestibular system (4th ed.). New York, NY: Oxford University Press. Baloh, R. W., Honrubia, V., Yee, R. D., & Hess, K. (1984). Changes in the human vestibule-ocular reflex after loss of peripheral sensitivity. Annals of Neurology, 16(2), 222–228. Baloh, R. W., Sills, A. W., & Honrubia, V. (1979). Impulsive and sinusoidal rotatory testing: A comparison with results of caloric testing. Laryngoscope, 89, 646–654. Barber, H., & Stockwell, C. (1980). Manual of electronystagmography (2nd ed.). St. Louis, MO: C.V. Mosby. Brey, R. H., McPherson, J. H., & Lynch, R. M. (2008a). Background and introduction to whole body rotational testing. In G. Jacobson & N. Shepard (Eds.), Balance function assessment and management (pp. 253–280). San Diego, CA: Plural Publishing. Brey, R. H., McPherson, J. H., & Lynch, R. M. (2008b). Technique, interpretation, and usefulness of whole body rotational testing. G. Jacobson & N. Shepard (Eds.), Balance

function assessment and management (pp. 281–317). San Diego, CA: Plural Publishing. Curthoys, I. S., & Halmagyi, G. M. (1996). How does the brain compensate for vestibular lesions? In R. Baloh & G. Halmagyi (Eds.), Disorders of the vestibular system (pp. 145–154). New York, NY: Oxford University Press. Demer, J. L. (1996). How does the visual system interact with the vestibulo-ocular reflex? In R. Baloh & G. Halmagyi (Eds.), Disorders of the vestibular system (pp. 73–84). New York, NY: Oxford University Press. Furst, E. J., Goldberg, J., & Jenkins, H. A. (1987). Voluntary modification of the rotary induced vestibulo-ocular reflex by fixating imaginary targets. Acta Otolaryngologica, 103(5–6), 232–240. Goldberg, J. M., Wilson, V.J., Cullen, K. E., Angelaki, D. E., Broussard, D. M., Bütner-Ennever, J.A., . . . Minor, L. B. (2012). The vestibular system: A sixth sense. New York, NY: Oxford University Press. Goulson, A. M., McPherson, J. H., & Shepard, N. T. (2016). Background and introduction to whole-body rotational testing. In G. Jacobson & N. Shepard (Eds.), Balance function assessment and management (pp. 347–364). San Diego, CA: Plural Publishing. Gresty, M. A., & Lempert, T. (2001). Pathophysiology and clinical testing of otolith dysfunction. In P. Tran Ba Huy & M. Toupet (Eds.), Otolith function and disorders (pp. 15–33). New York, NY: Karger. Highstein, S. (1996). How does the vestibular part of the inner ear work? In R. Baloh & G. Halmagyi (Eds.), Disorders of the vestibular system (pp. 3–11). New York, NY: Oxford University Press. Jacobson, G. P., Piker, E. G., Do, C., McCaslin, D. L., & Hood, L. (2012). Suppression of the vestibule-ocular reflex using visual and nonvisual stimuli. American Journal of Audiology, 21(2), 226–231.

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Leigh, R. J., & Zee, D. S. (2006). The neurology of eye movements (4th ed.). New York, NY: Oxford University Press. Møller, C., White, V., & Ödkvist, L. M. (1990). Plasticity of compensatory eye movements in rotary tests. II. The effect of voluntary, visual, imaginary, auditory and proprioceptive mechanisms. Acta Otolaryngologica, 109(3–4), 168–178. Ödkvist, L. (2001). Clinical and instrumental investigational otolith function. In P. Tran Ba Huy & M. Toupet (Eds.), Otolith function and disorders (pp. 68–76). New York, NY: Karger. Paige, G. D. (1989). Nonlinearity and asymmetry in the human vestibule-ocular reflex. Acta Otolaryngologica, 108, 1–8. Raphan, T., & Cohen, B. (1996). How does the vestibuloocular reflex work? In R. Baloh & G. Halmagyi (Eds.), Disorders of the vestibular system (pp. 20–47). New York, NY: Oxford University Press. Raphan, T., Matsuo, V. & Cohen, B. (1979). Velocity storage in the vestibule-ocular reflex arc (VOR). Experimental Brain Research, 35, 229–248. Schönfeld, U. & Clarke, A. (2011). A clinical study of the subjective visual vertical during unilateral centrifugation and static tilt. Acta Oto-Laryngologica, 131, 1040–1050. Schwarz, D. W. F., & Tomlinson, R. D. (2005). Physiology of the vestibular system. In R. Jackler & D. Brackman (Eds.), Neurotology (2nd ed., pp. 91–121). Philadelphia, PA: Elsevier Mosby. Shepard, N. T., Goulson, A. M. & McPherson, J. H. (2016). Clinical utility and interpretation of whole-body rotation. In G. Jacobson & N. Shepard (Eds.), Balance function assess-

ment and management (pp. 365–390). San Diego, CA: Plural Publishing. Shepard, N. T., & Telian, S. A. (1996). Practical management of the balanced disordered patient. San Diego, CA: Singular Publishing Group. Stockwell, C. W. & Bojrab, D. I. (1997). Background and technique of rotational testing. In G. Jacobson, C. Newman, & J. Kartush (Eds.), Handbook of balance function testing (pp. 237–248). San Diego, CA: Singular Publishing Group. Tusa, R. J., Grant, M. P., Buettner, U. W., Herdman, S. J., & Zee, D. S. (1996). The contribution of the vertical semi-circular canals to high velocity horizontal vestibule-ocular reflex (VOR) in normal subjects and patients with vestibular nerve section. Acta Otolaryngologica, 116(4), 507–512. Valko, Y., Hegemann, S. C., Weber, K. P., Straumann, D., & Bockisch, C. J. (2011). Relative diagnostic value of ocular vestibular evoked potentials and the subjective visual vertical during tilt and eccentric rotation. Clinical Neurophysiology, 122, 398–404. Wetzig, J., Reiser, M., Martin, E., Bregenzer, N., & von Baumgarten, R. J. (1990). Unilateral centrifugation of the otoliths as a new method to determine bilateral asymmetries of the otolith apparatus in man. Acta Astronautica, 21(6/7), 519–525. Wuyts, F. L., Hoppenbrouwers, M., Pauwels, G., & Van de Heyning, P. H. (2003). Utricular sensitivity and preponderance assessed by the unilateral centrifugation test. Journal of Vestibular Research, 13, 227–234. Zalewski, C. (2018). Rotational vestibular assessment. San Diego, CA: Plural Publishing.

Index Note:  Page numbers in bold reference non-text material.

A ABC (Activities-Specific Balance Confidence Scale), 148, 157–158, 588 vestibular rehabilitation and, 559 Abducens nerve, 48 palsies and, 49 Abduction, defined, 47 Ablative vestibular surgery, 509 for vertigo, 515 Abortive migraine medications, vestibular migraine and, 497 Acoustic neuroma, 526 Action potential (AP), 440 Activities-Specific Balance Confidence Scale (ABC), 148, 157–158, 588 vestibular rehabilitation and, 559 Acute attack of vertigo” subscale (VACU), 154 Acute lesion, gaze-evoked nystagmus, 211 Adaptive test (ADT) presentation of results, 388 normal sample, 389 slow support surface rotations, 388 Adduction, defined, 47 ADHD (Attention deficit hyperactivity disorder), 479 Adolescent idiopathic scoliosis, 479 ADT (Adaptive test) presentation of results, 388 normal sample, 389 slow support surface rotations, 388 Afferent development of, 25–27 innervation ampullar epithelia, 31 macular epithelia, 31 neurite terminals, vestibular, 26 neurons, 22 physiology, 72–75 Air conducted stimuli, 401–403 irrigators, 260–261

righting reflex, 31 Airway infection, pediatric vertigo and, 458 Alcohol, vestibular migraine and, 497 Alcohol (ethanol), vestibular dysfunction and, 307 Alexander, Gustav, criticizes Róbert Bárány, 11 Alexander’s law, 115, 210, 214 gaze-evoked nystagmus, 211, 212 nystagmus and, 168 Alprazolam, 489 panic disorder and, 491 Alzheimer’s disease, 525 American National Standards Institute (ANSI) air irrigators and, 260 Committee on Hearing, Bioacoustics, and Biomechanics (CHABA), 262 Aminoglycoside antibiotics, vestibular dysfunction and, 307 Amphetamine, vestibular dysfunction and, 307 Amplification, oVEMP, 427 An Historical Survey of Vestibular Equilibration, 6 Ankle, movement strategy and, 96 Annulus of Zinn, 45 ANSI (American National Standards Institute) air irrigators and, 260 Committee on Hearing, Bioacoustics, and Biomechanics (CHABA), 262 Anterior inferior artery syndrome, 519 Anterior semicircular canal BPPV, 240–242 Anteroventral regions, of otocyst, 20 Anticholinergics, 492 Anticonvulsants, 307 Antidepressants, 307 Antihistamines, 491 Antipsychotics, vestibular dysfunction and, 307 Anxiety 19th century descriptions of, 530 disorders balance and, 5335 reflexes and, 534 Ménièré’s disease and, 539 vestibular migraine and, 539 AP (Action potential), 440

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“Aphysiologic” pattern, 534 Apogeotropic nystagmus, horizontal semicircular canal BPPV with, 247–250 Archives of Otolaryngology, 439 Aristotle, 1 principle human senses, 8 Arnold–Chiari malformation, 180, 215, 526 Arrhythmias, presyncope/syncope and, 128 Aspartame, vestibular migraine and, 497 Aspirin, vestibular dysfunction and, 307 Asthma, anticholinergics, 492 Asymmetric hearing loss, offending labyrinth and, 511 Asymmetrically impaired ocular pursuit, lateral medullary syndrome and, 524 Ataxia, vertigo and, 127 Atenol, vestibular migraine and, 497 Ativan, 489, 491 vestibular dysfunction and, 307 Atmospheric changes, vertigo and, 132 Attention, vestibular dysfunction and, 582 Attention deficit hyperactivity disorder (ADHD), 479 Auditory evoked response, 440 localization, 5 neuropathy, 471 Autism, 479 Autoimmune hearing loss treatment, Ménièré’s disease and, 493 Automatic movement system, 93–94 postural, 94 coordination of, 94–97 into strategies, 96 responses, 383 voluntary movements and, 100 Autonomic regulation, vestibular contributions to, 132 Autonomic system, 78

B BAI (Beck Anxiety Index), 146 Balance anxiety disorders and, 533–535 biomechanics of, 87–89 defined, 87 developmental milestones of, 34–36 exercises, 585 function testing, 510 gravity alignment center, 89 gross motor skills and, 484 impact of rehabilitation, 584–589 interactions, between sensory and motor components, 98–100

motor control of, 92–94 muscles involved in, 95 perceived threat and, 533 psychological influences on, 531–533 senses of, 90–92 sensing position of, 89–92 stability limits, 88 frequency, 89 support base, 88 sway limits, 88–89 frequency, 89 voluntary movements and, 99–100 Balance Advantage system, 387, 389 Balance therapy, 479 balance training, 485 static/dynamic, 483–484 delivery of, 480 gaze stabilization training, 480–482 gross motor development and, 484–485 Baloh, Robert, 12 Bárány, Róbert, 7–8, 9, 10–12, 310 caloric test and, 257–259 Bárány Medal, 11 Bárány Society, 11, 521 defining terms, 629 International Classification of Vestibular Disorders and, 538, 618 macro saccadic oscillations defined by, 218 Ménièré’s disease and, 634 nystagmus defined by, 214 vestibular migraine and, 521 paroxysmia and, 636 Barbituates, vestibular dysfunction and, 307 Basic Symptom Inventory-53 (BSI-53), 146 Basilar-type migraine, 521 Basolateral ion channels, 29 BDI (Beck Depression Inventory), 146 BDNF (Brain-derived neurotrophic factor), 25 The Beasts and the Man’s Life, 3 Beck Anxiety Index (BAI), 146 Beck Depression Inventory (BDI), 146 Bedside assessment of vestibular system, 167–185 dynamic visual acuity test, 170–180 head shake, 172–176 horizontal head-impulse test, 170–172 sensory interaction of balance test, 182–185 spontaneous nystagmus, 167–170 valsalvan-induced nystagmus, 180–182 Bedside tests, described, 167 Behavioral response, to head motion, 30–31

Index 691

“Beitrage zur Lehre vom statischen Sinne,” 8 Beiträge zur näheren Kenntniß des Schwindels aus heautognostischen Daten, 7 Békésy, George von, Nobel Prize, 10–11 Benadryl, 310 vestibular dysfunction and, 307 Bench-to-bedside link, 10 Benign paroxysmal positional vertigo (BPPV), 111, 184, 382, 389 age and, 577, 579, 582, 585–586 behavioral outcomes, 531 Brandt-Daroff exercise and, 551 characteristics of, 225 clinical presentation of, 228–233 diagnosis of, 230 Dix-Hallpike and roll test and, 466, 555 dizziness handicap inventory and, 560 habituation training and, 483 head trauma and, 132 head-shake test and, 176 Ménièré’s disease, 133 migraine and, 133 nystagmus and, 250–252 otoconia movement and, 131 paroxysmal vertigo in children, 479 pediatric, 458, 473 pediatric, 466, 473 posterior canal occlusion for, 502–503 semicircular canal occlusion and, 501 recurrent vertigo of childhood, 521 semicircular canals (SCCs) and, 226 singular neurectomy for, 502 studies, 227 surgical management of, 502 testing, 225, 229–233 treatment of, 234–250, 490 utricular origin of, 227 VBT (Vestibular balance therapy) and, 483 vertigo and, 129 benign paroxysmal, 473 vestibular migraine and, 496 neuronitis and, 539 Benzodiazepines, 489 vestibular dysfunction and, 307 Beta-blockers, vestibular migraine and, 497 Bilateral impairments, sinusoidal harmonic acceleration, 324 vestibular lesions compensation after, 120–121

effects of, 112 vestibular system hypofunction, 178 weakness, interpretation/clinical significance of, 275 Bilateral vestibular hypofunction (BVH), 584 Bilateral vestibular loss (BVL), 519 failure, test patterns, 605–606 video head impulse test, 338–340 Binocular cameras, monocular cameras versus, 302, 304 Biomechanical constraints, 566 Bithermal caloric test pediatric, 468 procedure, 262 directional preponderance, 267–269 Blood glucose levels, lightheadedness and, 129 supply, vestibular system, 72 Blurred vision, vestibular abnormalities and, 520 Body coordination, gross motor skills and, 484–485 movement coordination of, 97 integration of, head movements and, 99 Bone-conducted vibration, 401–403 Bony labyrinth, 69, 71 Booth lighting, rotational chair enclosure, 296–298 BOR (Bruininks-Oseretsky Test of Motor Proficiency), 471 BOT-2 (Bruininks-Oseretsky Test of Motor Proficiency II), 460, 484 Bow and Lean test, 233 BPPV (Benign paroxysmal positional vertigo), 111, 129, 184, 382, 389 age and, 577, 579, 582, 585–586 behavioral outcomes, 531 Brandt-Daroff exercise and, 551 characteristics of, 225 clinical presentation of, 228–233 diagnosis of, 230 Dix-Hallpike and roll test and, 555 dizziness handicap inventory and, 560 habituation training and, 483 head trauma and, 132 shake test and, 176 Ménièré’s disease, 133 migraine and, 133 otoconia movement and, 131 pediatric, 466, 473 positional nystagmus and, 250–252 testing, 225 vertigo, benign paroxysmal, 473

692

Balance Function Assessment and Management

BPPV (Benign paroxysmal positional vertigo)  (continued) posterior canal occlusion for, 502–503 semicircular canal occlusion and, 501 procedures for, 502 semicircular canals (SCCs) and, 226 singular neurectomy for, 502 studies, 227 surgical management of, 502 testing for, 229–233 treatment of, 234–250, 490 utricular origin of, 227 VBT (Vestibular balance therapy) and, 483 vestibular migraine and, 496 neuronitis and, 538–539 Brain Chiari malformation of, 526 vestibular dysfunction and, 582 Brain-derived neurotrophic factor (BDNF), 25 Brainstem, 55 eye movements and, 48 saccades eye movement and, excitatory burst neurons, 55–57 Branchio-oto-renal (BOR), 471 Brandt-Daroff exercise and, benign paroxysmal positional vertigo (BPPV) and, 551 Breuer, Josef, 6, 9, 12 criticizes Róbert Bárány, 11 Brisk maneuver, 237–238 Bruininks-Oseretsky Test of Motor Proficiency II (BOT-2), 460, 484 Bruns nystagmus, acoustic neuroma and, 526 BSI-53 (Basic Symptom Inventory-53), 146 BVH (Bilateral vestibular hypofunction), 584 BVL (Bilateral vestibular loss), 519 video head impulse test, patient results, 338–340

C Caffeine, vestibular migraine and, 497 Calcium channel blockers, vestibular migraine and, 497 Calibration test, rotational testing and, 310 Caloric hyperactivity, 276 irrigations, 257, 260–261 order of, 262–263 pediatric, 468 recalibration before each, 262 tolerance of, 260 waiting period between, 263 performing the, test, 261–264 physiologic artifacts and, 269–271

responses analysis of, 264–269 monothermal, 269 profile, 265 total, 266 stimulation, 12, 257–259 technical errors, 269–271 test limitations of, 259–260 position, 258 unilateral weakness, 266–267 Caloric test, 597 abnormalities of, 277, 279 considerations in, test, 262–264 ice water, 277–278 interpretation of findings, test, 271–277 interpretation/clinical significance of bilateral weakness, 275 failure of fixation suppression, 276–277 hyperactive responses, 275–276 unilateral caloric weakness, 272–274 limitations of, test, 259–260 minimum age of patients in, test, 264 in neonates, 34 pediatric, 468 in perforated ear, 278 specialized, 277–278 test parameters, normative values for, 271–272 Cameras, binocular versus monocular, 302, 304 Canalith repositioning procedure (CRP), 235, 242–245 eye movements measured by, 262 Canalithiasis, 129 Canaliths, 227, 233–236, 243, 245 canalithiasis with, 247 displaced otoconia, 236 forced prolonged positioning and, 245 Canal-ocular reflexes, 50, 52–53 anxiety disorders and, 534 Carbamazepine vestibular dysfunction and, 307 vestibular migraine and, 497 Cardiovascular disease, 524 Case examples CDP (Computerized dynamic posturography) challenging, 617–626 motor control test, 389–391 sensory Organization Test (SOT), 378–382 SOT interpretations, 378–382 Catastrophic thinking, about dizziness, 537 Cawthrone-Cooksey exercises, 549–551, 585 CDP (Computerized dynamic posturography), 35, 554, 566, 583 adaptation test, 388–389

Index 693

described, 365 composite equilibrium scores, 372 minimum physical requirements, 367 motor control test, 382–388 case examples, 389–391 older adults score and, 560 patient instructions, 367 results, for asymptomatic population, 368–369 SOT interpretations, case examples, 378–382 testing interpretation, sensory organization, 369–382 operator administration, 367–368 preparation for, 367 Center of gravity (COG) adaptation results presentation, 388 alignment, 372, 375 balance and, 87, 88 examples of, 93 motor control test and, 382 active force latency, 385–387 active force strength, 387–388 protocol, 384–385 posture control and, 365 slow support surface, 388 rotations, 388 Central impairments, sinusoidal harmonic acceleration, 324–326 positional nystagmus, 250–252, 251 vertigo, 127, 251, 252 vestibular disorders, from peripheral vestibular disorders differentiating, 519 vestibular integration dysfunction cerebral palsy and, 479 in children, 479 vestibular lesions compensation after, 121 effects of, 112 vestibular structures/pathways, 50–55 vestibular system, 76–78 Central nervous system (CNS) axon guidance mechanisms and, 26 unilateral peripheral vestibular abnormality and, compensation for, 520 Centrifuge, psychiatric, 8, 10 Cerebellar artery, 72 clamping, 116 degeneration, 525 flocculonodular lobe, 77 stroke, pediatric, 473 syndromes, 67

tumors, vertigo and, 127 Cerebellopontine angle tumors, vertigo and, 127 Cerebellum, 50 central vestibular system and, 77 influences on gaze, 64–68 Cerebral palsy, central vestibular integration dysfunction and, 479 Cerebrovascular system, vertigo and, 128 Cervical spine, nystagmus and, 226 Cervical VEMP (cVEMP), 400, 597 amplitude normalization, 412–414 analysis/normative data amplitude, 417–418 latency, 418–419 threshold, 419 measurement parameters, effect of age on, 414–417 pathways of, 400–401 pediatric, 467–468 recording variables, 407–408 amplification/filtering, 408 response description, 400 stimulus frequency, 405 gating/duration, 407 intensity, 405–406 monaural/binaural, 407 rate, 406–407 variables, 401–407 subject variables, 408–417 biofeedback, 410–412 EMG activity/monitoring, 408–410 patient self-monitoring, 410–412 tuning, effect of age on, 417 see also Vestibular evoked myogenic potentials (VEMPs) Cervicogenic dizziness, 226 nystagmus, 226 Cervico-ocular reflex (COR), 157 CHABA (Committee on Hearing, Bioacoustics, and Biomechanics), 262 CHARGE (Coloboma-heart-atresia-growth retardationgenital-ear) syndrome, 460 Charité-Hospital, 8 Cheese, vestibular migraine and, 497 Chemotherapeutic agents, vestibular dysfunction and, 307 Chiari malformation, 526 Children benign paroxysmal vertigo in, 479 benign recurrent vertigo and, 521 examination of, 462–463 rotational testing of, 287

694

Balance Function Assessment and Management

Children  (continued) vestibular dysfunction in, 479 vestibular migraine, 479 Chocolate, vestibular migraine and, 497 Chronic gaze-evoked nystagmus, 211 Circulating fan, rotational chair enclosure, 296–298 Cisplatin, vestibular dysfunction and, 307 Clinical diagnosis, rotation, absence of, 8 Clinical Test of Sensory Interaction and Balance (CTSIB), 182, 566 vestibular rehabilitation and, 562 Clinical Test of Sensory Interaction and Balance (mCTSI B), modified, 556, 565 Clonazepam, 489 vestibular migraine and, 491 Closed-loop water irrigation, 260 CM (Cochlear microphone), 440 CMV (Congenital cytomegalovirus), 470 CNS (Central nervous system), axon guidance mechanisms and, 26 Cocaine, vestibular dysfunction and, 307 Cochlea, formation of, 20–22 Cochlear artery, 72 concussion, 524 endolymphatic shun, 509 Cochlear microphone (CM), 440 Cochleogram, 439 COG (Center of gravity) adaptation results presentation, 388 alignment, 372, 375 balance and, 87, 88 examples of, 93 motor control test and, 382 active force latency, 385–387 active force strength, 387–388 protocol, 384–385 posture control and, 365 slow support surface rotations, 388 Cognitive impact, vestibular disorders and, 82–83 Coloboma, infrared light and, 306 Coloboma-heart-atresia-growth retardation-genital-ear (CHARGE) syndrome, 460 Committee on Hearing, Bioacoustics, and Biomechanics (CHABA), 262 Compazine®, 236 Compensation for unilateral peripheral vestibular abnormality and, 520 vestibular, 105, 112–122, 167 anticholinergics and, 492 assessment of, 510

benzodiazepines and, 491 described, 520 lower extremity weakness and, 555 patient satisfaction and, 516 postoperative, 514 recovery and, 552–553 rotational testing and, 283 vestibular neuritis and, 501 VOR and, 353 Computer, rotational chair, 301–302 Computerized dynamic posturography (CDP), 35, 554, 566, 583 adaptation test, 388–389 described, 365 composite equilibrium scores, 372 minimum physical requirements, 367 motor control test, 382–388 case examples, 389–391 older adults score and, 560 patient instructions, 367 results, for asymptomatic population, 368–369 SOT interpretations, case examples, 378–382 testing interpretation, sensory organization, 369–382 operator administration, 367–368 preparation for, 367 Concentration, vestibular dysfunction and, 582 Concussion, 524, 527 symptoms of, 524 Congenital cytomegalovirus (CMV), 470 muscular torticollis, 479 nystagmus, 218 Conjugate eye movements, 47 Connexin 26 mutations, 471 Console, rotational chair, 301–302 Constant–varying cupular deflection, 312 Contaract lens replacement surgery, infrared light and, 306 Convergence, defined, 47 Coordinated movements, biomechanics of, 94–95 Cordes, Emil, 529 Corneoretinal potential (CRP), 189–190 Coronary heart disease, presyncope/syncope and, 128 Cortical saccadic abnormalities, 58 Couch, rotation, 8 Country and City of Cork Lunatic Asylum, 8 Cox, Joseph Mason, 8 Cranial nerve III, 49 IV, 49 VI, 48

Index 695

VIII, 69, 71 “Cretan Labyrinthos,” 5 CRP (Canalith repositioning procedure), 242–245 eye movements measured by, 262 CRP (Corneoretinal potential), measuring, 189–190 Crum-Brown, Alexander, 6, 9 CTSIB (Clinical Test of Sensory Interaction and Balance), 182, 566 vestibular rehabilitation and, 562–564 Cupula, endolymph and, 108 Cupulolithiasis, 129 cVEMP (Cervical VEMP), 400 amplitude normalization, 412–414 analysis/normative data amplitude, 417–418 latency, 418–419 threshold, 419 measurement parameters, effect of age on, 414–417 pathways of, 400–401 pediatric, 467–468 recording variables, 407–408 amplification/filtering, 408 response description, 400 stimulus frequency, 405 gating/duration, 407 intensity, 405–406 monaural/binaural, 407 rate, 406–407 variables, 401–407 subject variables, 408–417 biofeedback, 410–412 EMG activity/monitoring, 408–410 patient self-monitoring, 410–412 tuning, effect of age on, 417 see also Vestibular evoked myogenic potentials (VEMPs) Cytomegalovirus, 470

D Darwin, Charles, 1–2 Darwin, Erasmus, 2–3, 4, 6, 12 rotation and, 8 Darwin, Robert Waring, 2, 4 DBS (Dizziness Belief Scale), 149 De Anima Brutorum quae Hominis Vitals ac Sentitiva Exercitationes Duae, 3 de la Mettrie, Julien Offray, 3 de Nó, Rafeal Lorente, 11 Deiter’s nucleus, 53, 71, 76, 401 Demyelinating disease, 520, 526–527

Depression defined, 47 Ménièré’s disease and, 539 stress and, 536 “Destined for Distinguished Oblivion: The Scientific Writings of William Charles Wells,” 12 Developmental coordination disorder, 479 Dextrocycloversion, defined, 47 Dextroversion, defined, 47 DFI (Dizzy Factor Inventory), 149 DGI (Dynamic Gait Index), 157, 567, 583–584, 585 DHI (Dizziness Handicap Inventory), 148, 540–541, 559–560 rotation testing and, 306 self-report tools, 154–157 use of, 159 vestibular exercise program and, 557 vestibular rehabilitation and, 559, 585 DHI-S (Dizziness Handicap Inventory-Screening Version), 156 Diabetes, lightheadedness and, 129 Diagnoses, multiple, possibility of, 132–134 Diagnosis clinical, rotation, absence of, 8 Diagnostic and Statistical Manual of Mental Disorders (DSM-III), 530 Diazepam, 489, 491 DIE (Dynamic illegible E), 178 test, 178 Die Agoraphobie, 529 Diet, Ménièré’s disease and, 493 Differentiation, hair cell, 22 Dilantin, vestibular dysfunction and, 307 DiNA (Dizziness Needs Assessment), 149 Direction changing nystagmus, pediatric, 467 fixed, 211 gaze-evoked nystagmus, 211 pediatric positional nystagmus, 467 Disequilibrium, described, 128 Disjunctive eye movements, 47 Diuretics Ménièré’s disease and, 493 vestibular dysfunction and, 307 Divergence, defined, 47 Dix-Hallpike and roll test, 226, 229–233, 473 benign paroxysmal positional vertigo (BPPV) and, 555 panic disorders and, 535 pediatric, 466 vestibular exercise program and, 557 Dizziness 19th century descriptions of, 530 acoustic neuroma and, 526

696

Balance Function Assessment and Management

Dizziness  (continued) concussion and, 527 defined, 127 diagnostic categories, 521–527 cerebrovascular disease, 524 chiari malformation, 526 demyelinating disease, 526–527 head trauma and, 524–525 mal de debarquement syndrome, 527 neurodegenerative disease and, 525–526 vestibular migraine, 521–524 fear of falling and, 588 postural-perceptual, persistent, 537–538 psychiatric morbidity in, diagnosis/treatment of, 540–542 psychological factors, 535–537 twentieth century syndromes of nonvertiginous, 530 twenty-first century interactive model, 537–539 types of, 521 see also Vertigo Dizziness Belief Scale (DBS), 149 Dizziness Handicap Inventory (DHI), 148, 540–541 rotation testing and, 306 self-report tools, 154–157 use of, 159–162 vestibular exercise program and, 557 vestibular rehabilitation and, 559–560, 585 Dizziness Handicap Inventory-Screening Version (SHI-S) (DHI), 156 Dizziness Needs Assessment (DiNA), 149 Dizziness-related quality of life (DRQoL) described, 143 measurement tools general/disease specific, 145, 146–151 selecting, 144 self-report tools, 151–159 Dizzy Factor Inventory (DFI), 149 DLPN (Dorsolateral pontine nuclei), 61, 63 Dorsal vermis, role of, 66 Dorsolateral pontine nuclei (DLPN), 61 Down-beating nystagmus, 181, 228 Drop attacks, Ménièré’s disease and, 130–131 DRQoL (Dizziness-related quality of life) described, 143 measurement tools general/disease specific, 145, 146–151 selecting, 144–145 self-report tools, 151–159 Dual-tasking, 549, 582 DVA (Dynamic visual acuity), 176, 180, 480 assessment, 555 risk of falling and, 583

test, 170–180 VOR (Vestibulo-ocular reflex) and, 480 Dyazide, Ménièré’s disease and, 493 Dynamic balance, defined, 483 compensation, 113, 118–120 posturography, 121, 326, 458, 534 computerized, 35, 554, 566, 583 older adults computerized score and, 560 SOT included, 540 systems, 105 Dynamic Gait Index (DGI), 157, 567, 585 Dynamic illegible E (DIE), 178 test, 179 Dynamic visual acuity (DVA), 176, 180, 480 assessment, 555 risk of falling and, 583 test, 170–180 VOR (Vestibulo-ocular reflex) and, 480 Dyssynchrony, 471

E Ear hair cell, differentiation, 22 pressure, Ménièré’s disease and, 130 Early Treatment Diabetic Retinopathy Study (ETDRS), 176 Earth vertical axis rotation around, 286 rotational chair, 288, 290 EBNs (Excitatory burst neurons), 57, 197 ECochG (Electrocochleography), 439 diagnostic applications of, 448–453 neurophysiology of, 440 rationale/principle of, parameters, 447–448 recording methods, 440–446 parameters, 446 stimulating parameters, 444–446 semicircular canal dehiscence, 449–453 semicircular canal dehiscence repair, intraoperative applications of, 453–454 EEV (European Evaluation of Vertigo), 147 Efferent innervation, 27 neurons, 22, 25 system, 75–76 Effexor, vestibular migraine and, 497 Einstein, Albert, Theory of General Relativity, 9 Elavil, vestibular dysfunction and, 307 Electrocochleography (ECochG) diagnostic applications of, 448–453 discussed, 439

Index 697

neurophysiology of, 440 rationale/principle of, 447–448 recording methods, 440–446 parameters, 446 stimulating parameters, 444–446 semicircular canal dehiscence, 449–453 semicircular canal dehiscence repair, intraoperative applications of, 453–454 Electrode placement, oVEMP, 426–427 Electronystagmography (ENG), 189–192, 260 Electro-oculography (EOG), 189–192, 284 Elevation, defined, 47 Elicited nystagmus, 228 Embryonic development, 15 End organs, vestibular, innervation of, 25–27 Endolymph, 69, 401, 493, 605 cupula and, 108 flow, in semicircular canals (SCCs), 73 flute frequency and, 399 labyrinth and, 106 mastoidectomy and, 508 otolith organs and, 74 sac surgery and, 509 semicircular canals (SCCs), 71–72 Endolymphatic duct, 71 hydrops, 106 sac procedures, 508–509 ENG (Electronystagmography), 189–192, 260 Enhanced with fixation removed, gaze-evoked nystagmus, 211 EOG (Electro-oculography), 189–192, 284 Epidermoid cysts, vertigo and, 127 Epley, John, 235 Epley maneuver, reverse, 240 EQ-5D (European Quality of Life Scale), 146 EquiTest™, 566 Erasmus Wells Debate, Visual vertigo, 4–5 Essays upon Single Vision with Two Eyes: Together with Experiments and Observations on Several Other Subjects in Optics, 4, 5 ETDRS (Early Treatment Diabetic Retinopathy Study), 176 Ethacrynic acid, vestibular dysfunction and, 307 Ethanol, vestibular dysfunction and, 307 European Evaluation of Vertigo (EEV), 147 European Quality of Life Scale (EQ-5D), 146 Examination, office, pediatric, 462–463 Excitatory burst neurons (EBNs), 57, 197 Excyclovergence, defined, 47 Experiences sur les canaux semicirculaires de l’oreille dans les mammifères, 7

Experiences sur les canaux semicirculaires de l’oreille dans les oiseaux, 7 Extorsion, defined, 47 Extraocular muscles, 45 actions/innervation of, 45–47 Eye-hand coordination, gross motor skills and, 484–485 Eye movement anatomic scheme for synthesis of signals, 51 following focal lesion, 111 functional classes of, 43–45 nomenclature for, 47 nystagmus, 45 optokinetic system, 43, 44 pathways of, 45–50 saccades, 34, 44 smooth pursuit system, 43, 45 vergence system, 43, 45 vestibular system, 44 visual fixation, 43–44 Eye movement recording gaze stability tracking, 208–220 analysis parameters, 208–210 interpretation of, 210–220 saccade intrusions/oscillations, 217–220 optokinetic nystagmus, 220–222 protocol, 210 pursuit tracking and, 202–222 analysis parameters, 203–205 fixed-velocity pursuit, 205–206 sinusoidal target, 205 technical considerations, 202–203 smooth pursuit tracking and, 202–222 techniques, 189–193 infrared video, 192–193 Eyelids, infrared light and, 306 Eyeliner, infrared light and, 306

F Facial nerve schwannomas, vertigo and, 127 Failure of fixation suppression, 276–277 Fall risk effect of age on, 586 impact of fear and, 587–588 progressive corrective lenses and, 520 Falls Efficacy Scale, 158 International, 158, 588 Fan, rotational chair enclosure, 296–298 Fastigial oculomotor region, 65 role of, 66 “Father of Otolith Function Testing,” 9 Fear of falling (FOF), 587–588

698

Balance Function Assessment and Management

Fetal period, 15 FI (Fixation index), 269 Fishponds Private Lunatic Asylum, 8 Five Times Sit to Stand Test (FTSST), 157 Fixation index (FI), 269 Flourdens, Jean Pierre, 6–7, 12 Flunarizine, vestibular migraine and, 497 Foam posturography, 562–563 Focal lesion, eye movements following, 111 FOF (Fear of falling), 587–588 Forced prolonged positioning (FPP), 245 FPP (Forced prolonged positioning), 245 Frame-rate goggles, 328 Free-floating otoconia, 129 Frenzel goggles, 181, 229, 558 Friedreich’s ataxia, 525 vertigo and, 127 FTSST (Five Times Sit to Stand Test), 157 Functional gait disorders, 535 reach, 561–562 Functional Gait Assessment, 484

G GABA (γ-aminobutyric acid), 491 Gabapentin, vestibular migraine and, 497 GAD-7 (Generalized Anxiety Disorder Scale), 541 Gain asymmetry, 222, 269, 275, 341 described, 315 VOR asymmetries, 343 interpretation, 316–319 response, 315–316 video head impulse test, 340–343 Gait age and, 583 assessment of, 566–567 Dynamic Gait Index (DGI), 157, 567 speed, 566 exercises, 585 instability, lateral medullary syndrome and, 524 Galen, Aelius, 5 Gastrulation, process of, 15–16 Gate instability, acoustic neuroma and, 526 Gaze cerebellar influences on, 64–68 effects, oVEMP, 427–428 evoked nystagmus, 61 acoustic neuroma and, 526 characteristics of, 211 eye, evoked nystagmus, 524

shifting, gaze stability training, 481–482 testing, pediatric, 466–467 Gaze stability, 194 exercises, 585 testing, 208–220, 480–482 analysis parameters, 208–210 interpretation of, 210–220 tracking, eye movement recording, saccade intrusions/oscillations, 217–220 training exercises, 481 gaze shifting, 481–482 remembered targets, 482 vestibular hypofunction and, 482 X1 (Times one) viewing, 480–481 X2(Times two) viewing, 481 Gaze stabilization test (GST), 580, 583–584 General Health Questionnaire (GHQ-12), 146 Generalized Anxiety Disorder Scale (GAD-7), 541 Gentamicin ototoxicity, video head impulse test and, 354 vestibular dysfunction and, 307 vestibulotoxicity, 106 The Gentleman’s Magazine, 5 Geotropic nystagmus, Gufoni maneuver for, 245, 246 German measles, 470 GHQ-12 (General Health Questionnaire), 146 GJB2, 471 Glaucoma, narrow angle, anticholinergics, 492 Goggles, video-oculography, 287, 288 calibration test and, 310 components of, 306 described, 302–306 eye movement recording and, 463–464 patient setup and, 308 rotational chair and, 288, 299 test enclosure and, 291 testing and, 302–306 Golgi tendon organs, 182 Graviceptive pathways, 54 Gravity alignment, center of gravity alignment, 371 fixed strategy, 97 Griffith, Coleman, 6 Gross motor body coordination and, delay, vestibular system and, 459–460 development, VBT and, 484–485 skills, balance and, 484 Group exercises, 550 Grundlinien der Lehre von den Bewegungsempfindungen, 8 GST (Gaze stabilization test), 580, 583–584

Index 699

Gufoni maneuver, 245, 246 for apogeotropic nystagmus, 247

H Habituation training, 483 VBT (Vestibular balance therapy) and, 483 as a treatment, 585 HADS (Hospital Anxiety and Depression Scale), 132, 146, 541 Hair cells, 69 afferent physiology and, 74 differentiation, 22 dysfunction, 106 stimulating, 28 transduction channels, 28 response to, 29–30 Haldol, vestibular dysfunction and, 307 Hallaran, William Saunders, 8 “Hallaran’s Circulating Swing,” 8 Hallpike, Charles Skinner, 11 Harmonic acceleration sinusoidal abnormalities associated with, 329 acceleration response, 320–321 bilateral impairments, 324 central impairments, 324–326 rotational testing, 311–326 site-of-lesion abnormalities, 330 unilateral peripheral impairments, 321–324 Harness, safety, rotational chair, 298–299 Head impulse goggles, 337 impulse test, 555 horizontal, 170–172, 173 motion, behavioral response to, 30–31 movement coordination of, 97 integration of, body movements and, 99 sensory effects of body and, 98–99 vestibular response to, 106–109 rest, rotational chair, 296 restraints, rotational chair, 298–301 rotation, 11 around earth axis, 286 nystagmus and, 8 shake test, 172–176 benign paroxysmal positional vertigo (BPPV) and, 176 shaking nystagmus, 172 stimulating hair cells, 28 thrust test, 462

trauma, 524–525 vestibular dysfunction, 479 velocity sensor, video head impulse test, 345–346 vestibular disorders and, 552 Head impulse paradigm (HIMP) tests, 336 Hearing loss Ménièré’s disease, 130 preservation of residual, 512 vertigo and, 130 Heart disease, presyncope/syncope and, 128 Hennebert’s sign, 180, 181, 504 Hering’s law of equal innervation, 46 Heschel’s gyrus, 77 Hetzig, Julius Eduard, criticizes Róbert Bárány, 11 HIMP (Head impulse paradigm) tests, 336 Hip, movement strategy and, 96 Hippocrates of Kos, 1 An Historical Survey of Vestibular Equilibration, 6 Horizontal head-impulse test, 170–172, 173 nystagmus, 181 Horizontal semicircular canal BPPV with apogeotropic nystagmus, 247–250 with geotropic nystagmus, 242–247 forced prolonged positioning and, 245 outcomes, 245 particle repositioning maneuvers, 242–245 Horn, Anton Ludwig Ernst, 8 Hospital Anxiety and Depression Scale (HADS), 132, 146, 541 HSN (Head-shaking nystagmus), 172 Hydrochlorothiazide, Ménièré’s disease and, 493 Hyperactive responses, to caloric tests, 275–276 Hypermetric saccades, 202 Hypometric saccades, 202

I IBN (Inhibitory burst neurons), 57 Ice water caloric test, 277–278 ICF (International Classification of Functioning Disability and Health), 144 definitions, 144 ICIDH (International Classification of Impairments, Disabilities, and Handicaps), 144 ICVD (International Classification for Vestibular Disorders), 214 Idiopathic sclerosis, adolescent, 479 IGSB (Intraganglionic spiral bundle), 27 IHS, 2018 (International Classification of Headache Disorders), 131 INC (Interstitial nucleus of Cajal), 57, 215 Incyclovergence, defined, 47

700

Balance Function Assessment and Management

Industrial solvents, vestibular dysfunction and, 307 Infantile Nystagmus, 218 Infants, examination of, office, 462–463 Infections hair cell dysfunction and, 106 vestibular nerve dysfunction and, 106 Inferior, 46 cerebellar artery, 72 oblique, 45, 47 rectus, 45, 47 Inferior vestibular nucleus (IVN), 76 Inflammation, vertigo and, 130 Infrared goggles, 346, 555 inability to fit, 327 light, use of, 304–306 recording techniques, 192–193 video monitor, patient, 295–296 Infrared videonystagmography (VNG), 189 eye movements measured by, 262 goggles, 168, 173, 181 Inhibitory burst neurons (IBN), 57 Inner ear, formation of, 17 Innervation efferent, development of, 27 patterns, 598–599 of vestibular end organs, 25–27 INO (Internuclear ophthalmoplegia), 49 International Classification for Vestibular Disorders (ICVD), 214 International Classification of Diseases, 458 International Classification of Functioning Disability and Health (ICF), 144 definitions, 144 International Classification of Headache Disorders (IHS, 2018), 131 International Classification of Impairments, Disabilities, and Handicaps (ICIDH), 144 International Headache Society, 131, 521 Internuclear connections, 50 Internuclear ophthalmoplegia (INO), 49 Interstitial nucleus, 198, 215 of medial longitudinal fasciculus, 55 of vestibular nerve, 76–77 Interstitial nucleus of Cajal (INC), 57, 215 Interstitial nucleus of the vestibular nerve (INVN), 76–77 Intorsion, defined, 47 Intracranial pathology, identification of, 511 Intraganglionic spiral bundle (IGSB), 27 Intratympanic gentamicin, 495

Ménièré’s disease and aminoglycosides, 495 vasodilators steroids, 494–495 Investigations of Rhythmic Nystagmus and Its Accompanying Manifestations Arising from the Vestibular Apparatus of the Ear, 10 INVN (Interstitial nucleus of the vestibular nerve), 76–77 Ipsilateral limb dysmetria, lateral medullary syndrome and, 524 Ipsilateral vestibulospinal tract (VST), 76 IVN (Inferior vestibular nucleus), 76

K Karolinska Institute, on Róbert Bárány, 11 Kidney disease, sulfa medications and, 493 Kinocilium, 24 Klonopin, 489

L Laboratory testing pediatric vestibular system, 463–469 recording techniques, 463 rotational chair, 463–465 Labyrinth, 69 Labyrinthectomy, 512 Labyrinthine artery, 72 concussion, 106, 524 membrane, endolymphatic hydrops and, 106 unstable disease, poor compensation versus, 509–511 Labyrinthitis, 106 pediatric, 458 symptoms, 492 Large vestibular aqueduct syndrome (LVAS), 471–472 Lasix, vestibular dysfunction and, 307 Lateral, 47 rectus, 45 signs of medullary syndrome, 524 Lateral geniculate nucleus (LGN), 61 Lateral vestibular nucleus (LVN), 53, 71, 76, 401 Lateral vestibulospinal tract (LVST), 77, 184, 579 The Laws of Organic Life, 2, 4 LED goggles, 328, 346 Lempert maneuver, 242–245 Levocycloversion, defined, 47 Levoversion, defined, 47 LGN (Lateral geniculate nucleus), 61 Liberatory maneuver, 237–238 Lifestyle changes, vertigo and, 132

Index 701

Lightheadedness described, 128–129 dizziness and, 521 Limits of stability (LOS), 88 Limits of sway, 88–89 Linear slow component, gaze-evoked nystagmus, 211 Lipomas, vertigo and, 127 Lithium, vestibular dysfunction and, 307 LLBN (Long-lead burst neurons), 57–58 Localization, auditory, 5 LogMar scale, 180 Long-lead burst neurons (LLBN), 57–58 Lorazepam, 489, 491 LOS (Limits of stability), 88 LVAS (Large vestibular aqueduct syndrome), 471–472 LVN (Lateral vestibular nucleus), 53, 71, 76, 401 LVST (Lateral vestibulospinal tract), 77, 184, 579

M Mach, Ernst Josef, 6, 12 criticizes Róbert Bárány, 11 rotational chair, 9 Macro saccadic oscillations, 218 square-wave jerks, 218 Maculae, 71 Macular degeneration, infrared light and, 306 Mal de debarquement syndrome, 527 Marijuana, vestibular dysfunction and, 307 Mascara, infrared light and, 304–306 Mastoidectomy, 508 Maxzide, Ménièré’s disease and, 493 mCTSIB (Modified Clinical Test of Sensory Interaction on Balance), 182–183, 556, 565 static balance and, 483–484 MD-POSI (Ménière’s Disease Patient-Oriented Severity Index), 150 Measles, 472 Meclizine, 491 impaired compensation and, 520 vestibular dysfunction and, 307 Media rectus, 45, 46 Medial longitudinal fasciculus (MLF), 48 unilateral inactivation of, 49 Medial longitudinal fasciculus (riMLF), 198 Medial rectus, 47 Medial superior temporal (MST) cortex, 61 Medial vestibular nucleus (MVN ), 61, 71, 76, 184, 215, 582 Medical Faculty of the Karolinska Institute, on Róbert Bárány, 11

Medical Outcomes Study Short form (SF-36), 146 Medicinal slumber, 8 Membranous labyrinth, 69, 71 Ménièré’s disease, 106, 439, 447, 582 anxiety and, 539 benign paroxysmal positional vertigo (BPPV) and_ Copy, 133 BPPV and, 226 depression and, 539 Diazepam and, 491 drop attacks and, 130–131 ear pressure and, 130 ECochG (Electrocochleography) in, 448–450 gaze-evoked nystagmus, 214 intratympanic gentamicin (ITG) dosages for, 354 management of, 496 medications for, 489 oral steroids and, 493–494 pediatric, 458, 472 stress and, 536 surgical management of, 508 test patterns, 601, 603 tinnitus and, 131 treatment of, 492–496 dietary modification, 493 diuretics, 493 intratympanic aminoglycosides and, 495 intratympanic steroids, 494–495 oral steroids, 493 vasodilators, 494 vertigo and, 129 hearing loss and, 130 video head impulse test and, 354–355 VOR gain and, 352 Ménièré’s Disease Patient-Oriented Severity Index (MD-POSI), 150 Meningioma, vertigo and, 127 Meningitis, 472 Mental exercises, 549 Metabolic disorders, lightheadedness and, 129 Metastatic tumors, vertigo and, 127 Methadone, vestibular dysfunction and, 307 Methyphendiate, vestibular dysfunction and, 307 MFES (Modified Falls Efficacy Scale), 147 Microdrift, eye, 44 Micromedical, Inc., 287 Microsaccades, eye, 44 Microtremor, eye, 43 Middle temporal cortex, 61 Migraine, 131, 521–524 benign paroxysmal positional vertigo (BPPV) and, 496 BPPV and, 133, 226

702

Balance Function Assessment and Management

Migraine  (continued) clonazepam and, 491 described, 521 diagnostic criteria for, 521 flow chart, 522 exacerbating factors, 132 medications for, 489 pediatric, 458, 479 stress and, 536 test patterns, 603–605 treatment of, 496–497 vertigo and, 130, 539 MLF (Medial longitudinal fasciculus), 48 unilateral inactivation of, 49 Modified Clinical Test of Sensory Interaction on Balance (MCTSIB), 182–183 static balance and, 483–484 Modified Falls Efficacy Scale (MFES), 147 Mondini malformation, 471–472 Monitor, infrared, patient, 295–296 Monocular cameras, binocular cameras versus, 302 eye movements, 47 Monothermal caloric responses, analysis of, 269 testing, 263–264 Morphogenesis, 15–16 Morphological polarization vector (MPV), 24 Motion Sensitivity Quotient (MSQ), 147 Motion sickness, 76–77, 81–82, 489–492, 521 medications for, 490–491 psychiatric causes of, 521 vestibular disorders and, 552 Motor control, of balance, 92–94 Motor control test active force response recordings, 385 computerized dynamic posturography horizontal support surface, 382–384 protocol, 384–385 computerized dynamic posturography (CDP), 382–388 presentation of results, 385–387 active force latency, 385–387 active force strength, 387 real-time display, 385 weight symmetry, 385 results, normal sample, 387–388 Motors, rotational chair, 292 Movement anatomy of, 92 automatic, 93–94 coordination of, 94–97 postural, 94, 96

body, coordination of, 97 coordinated, biomechanics of, 94–95 head, coordination of, 97 physiology of, 92 strategies ankle, 96 hip, 96 postural, 97, 98 stretch reflex, 93 system properties, 94 vertigo and, 131–132 volitional, 93–94 “The Moving Tablet of the Eye: The Origins of Modern Eye Movement Research,” 12 MPV (Morphological polarization vector), 24 MS (Multiple sclerosis), vertigo and, 127 MSQ (Motion Sensitivity Quotient), 147 MST (Medial superior temporal) cortex, 61 Multiple diagnoses, possibility of, 132–134 Multiple sclerosis (MS), vertigo and, 127 Multisensory integration, vestibular system function and, 81–82 Mumps, 472 MVN (Medial vestibular nucleus), 61, 71, 76, 184, 215

N N1 (Action potential). See Action potential (AP) Narrow angle glaucoma, anticholinergics, 492 National Institutes of Health Toolbox for the Assessment of Neurological and Behavioral Function, 180 Nausea peripheral vestibular disorders and, 519, 520 vestibular disorders and, 552 Neonates, caloric testing in, 34 Nerve palsies, abducens nucleus and, 49 Neural firing, afferent physiology and, 74–75 Neuritis, vestibular compensation and, 501 Neuro Kinetics, Inc. (NKI), 287 Neurocardiogenic syncope, 128 Neurodegenerative disease, 520, 525–526 Neurofibromatosis type 2 (NF2), 472 Neuromuscular system, age effects on, 581 Neurons, statoacoustic ganglion, 25 Neurontin, vestibular migraine and, 497 Neuroticism, anxiety disorders and, 535 Neurotologic illnesses, psychiatric complications of, 538–539 Neurotologic Test Center Suite (NOTC), 287 Neurotoxic agents, nerve fibers and, 106 Neurotrophins, 25 NF2 (Neurofibromatosis type 2), 472 Nicotine, vestibular dysfunction and, 307

Index 703

Nintendo Wii Fit, 587 NKI (Neuro Kinetics, Inc.), 287 Nó, Rafeal Lorente de, 11 Nobel Prize George von Békésy, 10 Róbert Bárány, 7–8, 10–11 Noise, vertigo and, 131–132 Nonsyndromic deafness, GJB2, 471 Nonvertiginous dizziness chronic, 539 twentieth century syndromes, 530 Nortriptyline, vestibular migraine and, 497 NOTC (Neurotologic Test Center Suite), 287 NPH-MVN (Nucleus propositus hypoglossi and adjacent medial vestibular nucleus), 61 NRTP (Nucleus reticularis tegmenti pontis), 58, 61, 63 Nucleus propositus hypoglossi and adjacent medial vestibular nucleus (NPH-MVN), 61 Nucleus reticularis tegmenti pontis (NRTP), 58, 61, 63 NutraSweet, vestibular migraine and, 497 Nylen, Carl O., 11 Nystagmus, 2, 45 acoustic neuroma and, 526 central positional, 250–252 described, 167 enhanced with head-shake test, gaze-evoked nystagmus, 211 head rotation and, 5-6, 8 horizontal, 181 periodic alternating, 55 positional, benign paroxysmal positional vertigo (BPPV) and, 250–252 slow-phase velocity (SPV), 264, 265–266 fixation index, 269 valsalvan-induced, 180–182 vestibular, examination to identify, 167–170

O Obsessive compulsive disorder, lightheadedness and, 128 Ocular flutter, 57, 218 motor nuclei, 50 nuclei/nerves, 48 rotational testing and, 310 pursuit, lateral medullary syndrome and, 524 tilt reaction, 53 Ocular motility testing, 193–222 saccade testing, 194–202 parameters for, 195–196 Ocular motor neurons (OMN), 55

Ocular vestibular-evoked myogenic potential (oVEMP), 400, 421–431, 597 description of response, 421 pathway, 421 pediatric, 467–468 recording variables, 426–427 stimulus age effects on, 428–431 duration, 423–424 frequency, 422–423 gaze effects, 427–428 intensity, 423 rate, 423 stimulus, 423 subject factors, 427–431 variables, 421–422 test results superior semicircular canal dehiscence (SSCD), 431–432 vestibular neuritis and, 433 Oculomotor nerve, 49 “Of Vertigo,” 2 Offending labyrinth, identifying the, 511 Office examination, pediatric, 462–463 Off-Vertical-Axis-Rotation (OVAR), 287 OKAN (Optokinetic after nystagmus), 220 OKN (Optokinetic) nystagmus parameters for analysis, 222 testing interpretation, 222 pediatric, 462 system, 43, 44 to age 7, 466 OMN (Ocular motor neurons), 55 Omnipause neurons, 57 “On the Law which has Regulated the Introduction of New Species,” 1 One-and-a-half syndrome, 49 Opiates, vestibular dysfunction and, 307 Opsoclonus flutter, 57 Optokinetic eye movements, 43, 44 nystagmus, 194, 220–222 parameters for analysis, 222 testing interpretation, 222 pediatric, 462 system, 43, 44 to age 7, 466 Optokinetic after nystagmus (OKAN), 54, 220 Oral steroids, Ménièré’s disease and, 493–494 Orbital muscle, gross anatomy of, 45 On the Origin of Species, 1, 2 On the Sense of Rotation and the Anatomy and Physiology of the Semicircular Canals of the Internal Ear, 8

704

Balance Function Assessment and Management

“On the Tendencies of Varieties to Depart Indefinitely From the Original Type,” 1 Orthostatic hypotension defined, 128 drop attacks and, 131 presyncope/syncope and, 128 Oscillopsia, defined, 176 Otago balance rehabilitation program, 587 Otic capsule, 69 formation of placode, 17–18 vesicle, 18 Otoconial crystals, 28, 71, 111, 429 BPPV and, 129 displaced, 227 free-floating, 129 otolith organs and, 74 vertigo and, 502 membrane, 24, 28, 74 Otocyst anteroventral regions of, 20 undifferentiated cells, 29 Otolith crystals, 74 ocular reflexes, 53–54 anxiety disorders and, 534 organs, 69 afferent physiology and, 72, 74, 75 described, 71 vestibular system anatomy and, 71 Otosclerosis, BPPV and, 226 Ototoxic drug use, pediatric, 472 OVAR (Off-Vertical-Axis-Rotation), 287 oVEMP (Ocular vestibular-evoked myogenic potential), 400, 421–431 description of response, 421 pathway, 421 pediatric, 467–468 recording variables, 426–427 stimulus age effects on, 428–431 duration, 423–424 frequency, 422–423 gaze effects, 427–428 intensity, 423 rate, 423 subject factors, 427–431 variables, 421–422 test results superior semicircular canal dehiscence (SSCD), 431–432 vestibular neuritis and, 433

P Pamelor, vestibular dysfunction and, 307 Panic attacks, 521 disorder alprazolam and, 491 dizziness/vertigo and, 536 stress and, 536 PANQOL (Penn Acoustic Neuroma Quality of Life Scale), 150 Paramedian pontine reticular formation (PPRF), 55 Parieto-temporo-occipital cortex, 61 Parkinson’s disease, 525 Particle repositioning maneuvers, 235, 240–241 procedure, 235–237 Patient clinician talk-back system, rotational chair, 294–295 setup, rotational testing, 306–308 Patient Health Questionnaire (PHQ-9), 541 Patient Intentions Questionnaire (PIQ), 146 Patterns innervation, 598–599 reproduceable, case examples, 606–616 vascular perfusion, 599–600 pDHI-PC (Pediatric Dizziness Handicap Inventory for Patient Caregivers), 151 PDMS (Peabody Developmental Motor Scales), VBT (Vestibular balance therapy) and, 480 Peabody Developmental Motor Scales (PDMS), VBT (Vestibular balance therapy) and, 480 Pediatric migraine and, 479 patients, rotational testing of, 287 vestibular dysfunction, 479 vestibular migraine, 479 Pediatric Dizziness Handicap Inventory for Patient Caregivers (pDHI-PC), 151 Pediatric Vestibular Symptom Questionnaire (PVSQ), 151 Pediatric vestibular system caloric irrigations, 468 development of, 457–458, 459–461 gross motor development, 459–460 vestibulocollic reflex, 459 vestibulo-ocular reflex [VOR], 459 vestibulospinal reflex, 459 disorders acquired, 472–473 auditory neuropathy, 471 benign paroxysmal positional vertigo (BPPV) and, 473

Index 705

benign paroxysmal vertigo, 473 cerebellar stroke, 473 cytomegalovirus, 470 GJB2, 471 in utero, 470–472 large vestibular aqueduct syndrome, 471–472 measles, 472 Ménièré’s disease, 458, 472 meningitis, 472 mumps, 472 neurofibromatosis type 2, 472 ototoxic drug use, 472 rubella, 470 semicircular canal dehiscence, 472 Usher syndrome, 470–471 Waardenburg syndrome, 471 Dix-Hallpike and roll test, 466 evaluation of, 461–469 clinical presentation, 461–462 history, 461–462 office examination, 462–463 gaze testing, 466–467 laboratory testing, 463–469 recording techniques, 463 rotational chair, 463–465 OKN to age 7, 466 positional testing, 466–467 postural control assessment, 465–466 pursuit tracking, 466 random saccade, 466 sensory Organization Test (SOT), 465–466 VEMPs (Vestibular evoked myogenic potentials), 467–468 video head impulse test, 468–469 Pediatric Visually Induced Dizziness Questionnaire (PVID), 151 Pendred syndrome, 471–472 Penn Acoustic Neuroma Quality of Life Scale (PANQOL), 150 Percent canal paresis, 267 reduced vestibular respons, 266–267 Perforated ear, caloric test in, 278 Perilymph, 69 labyrinth and, 106 Perilymphatic fistula, 132, 180, 182, 252, 501, 509 repair of, 503–504 Peripheral vertigo, 127 Peripheral vestibular abnormalities described, 105 medications for, 489 lesions, compensation of, 287 pediatric, loss, 459–460

Peripheral vestibular system disorders, central vestibular disorders differentiating from, 519 at birth, 457 Persistent Postural-Perceptual Dizziness (PPPD), 143 CSD superseded by, 538 defined, 532 neuroticism and, 536 Phenergan®, 236 vestibular dysfunction and, 307 Phenytoin, vestibular dysfunction and, 307 Phobias, lightheadedness and, 128 Phobic postural vertigo (PPV), 531, 537–538 PHQ (PRIME-MD Patient Health Questionnaire), 146, 541 Physical Self-Efficacy Scale, 158 Physiologic artifacts, caloric responses and, 269–271 PIQ (Patient Intentions Questionnaire), 146 PIVC (Posterior insula), 77 Placode, otic, formation of, 17–18 Platform posturography, 525 Plato, 1 Platzschwindel, 529 Politzer, Ádám, criticizes Róbert Bárány, 11 Pons, 61 Porterfield, William, 3 Post concussion vestibular dysfunction, 479 rotation nystagmus, 5 Positional nystagmus, 225–226 benign paroxysmal positional vertigo (BPPV) and, 250–252 interpretation of, 226 pediatric, 467 semicircular canals (SCCs) and, 226 test battery, purpose of, 225 testing, pediatric, 466–467 Positioning nystagmus clinical significance of, 225–226 tests for, 226–227 test, diagnosis of BPPV and, 230–231 Posterior canal occlusion, for BPPV, 502–503 fossa, dizziness/vertigo and, 524 parietal cortex, 61 Posterior insula (PIVC), 77 Posterior semicircular canal BPPV, treatment of, 234–240 occlusion BPPV (Benign paroxysmal positional vertigo) and, 501 procedures for, 502

706

Balance Function Assessment and Management

Post-traumatic stress disorder (PTSD), lightheadedness and, 128 Posttraumatic vertigo, pediatric, 458 Postural control assessment, pediatric, 465–466 system age effects on, 582–583 age-related changes in, 578–583 attentional demands on, 582–583 VOR and, 583–584 Postural movements automatic, 94 coordination of, 94–97 strategies, 98 selecting, 97 Postural orthostatic tachycardia, 128 Postural orthostatic tachycardia syndrome (POTS), presyncope/syncope and, 128 Postural responses automatic, 383 discrete measurement of, 366 value of, 366–367 Posture control, performance measures of, 365–366 “Posture-first” principle, 82 Posturography, 35, 470, 510 dynamic, 121, 326, 458, 534 computerized, 35, 554, 560, 566, 583 SOT included, 540 foam, 562–563 platform, 525 POTS (Postural orthostatic tachycardia syndrome), presyncope/syncope and, 128 PPPD (Persistent postural perceptual dizziness), 143 CSD superseded by, 538 defined, 532 neuroticism and, 536 PPRF (Paramedian pontine reticular formation), 55 PPV (Phobic postural vertigo), 531, 537–538 Pressure changes, vertigo and, 131–132 Presyncope, described, 128 PRIME-MD Patient Health Questionnaire (PHQ), 146 Prince Carl of Sweden, George von Békésy and, 10 PRMs (Particle repositioning maneuvers), 235 Processed meats, vestibular migraine and, 497 Progressive supranuclear palsy, 525 Projector, 292 rotational chair, 294 Prone-on-elbows position, 245 Prosensory patches delamination/formation of, 20 formation of, 18 Prostate hypertrophy, anticholinergics, 492

Prozac, vestibular dysfunction and, 307 Psychiatric centrifuge, 8, 10 illness, mental notes and, 540 screening tools, 540–541 Psychiatric morbidity diagnosis/treatment of, 540–543 medications, 542 psychotherapy, 542 vestibular rehabilitation, 542 in dizziness, diagnosis/treatment of, 540–542 Ptosis, infrared light and, 306 Pulmonary edema, anticholinergics, 492 Purkyneˇ, Jan Evangelista, 6–7, 8 Pursuit tracking eye movement recording and, 202–222 analysis parameters, 203–205 fixed-velocity pursuit, 205–206 sinusoidal target, 205 technical considerations, 202–203 pediatric, 462, 466 PVID (Pediatric Visually Induced Dizziness Questionnaire), 151 PVSQ (Pediatric Vestibular Symptom Questionnaire), 151

Q Quinine, vestibular dysfunction and, 307

R Random saccade, 466 Real-time display, of results, 372 Rebound Nystagmus, 214 Receptors, vestibular, 25 Recherches expérimentales sur les propriétés et les fonctions du système nerveux dans les animaux vertébrés, 7 Rectus muscles, 45 Recording eye movements, gaze stability tracking, 208–220 analysis parameters, 208–210 interpretation of, 210–220 saccade intrusions/oscillations, 217–220 optokinetic nystagmus, 220–222 protocol, 210 pursuit tracking and, 202–222 analysis parameters, 203–205 fixed-velocity pursuit, 205–206 sinusoidal target, 205 technical considerations, 202–203 smooth pursuit tracking and, 202–222

Index 707

Red wine, vestibular migraine and, 497 Reflex testing, vestibular, 35 Reflexive eye movement, 197 Rehabilitation age and outcomes, 586 assessing progress in, 559–561 balance confidence scale activities, 560–561 daily living scale activities, 561 Dizziness Handicap Inventory (DHI), 559–560 subjective assessments, 559 balance standing measures, 561–566 elements of, 584–586 exercise program, 555–557 gait assessment, 566–567 groups that improved after, 556 history of, 549–552 impact of, 584–589 individual vs. group, 588–589 negative predictive factors, 553 new technologies impact on, 586–587 selected cases, 557–558 theoretical considerations, 552–554 compensation and recovery, 552–553 therapeutic trial of, 510–511 Remembered targets, gaze stability training, 482 Restraints, head, rotational chair, 298–301 Reticular formation (RF), 77 Reticulospinal tract (RST), 77, 184, 459 Retina, 189 Retinal slip, 277 RF (Reticular formation), 77 riMLF (Rostral interstitial nucleus of the medial longitudinal fasciculus), 55, 57, 198 Ritalin, vestibular dysfunction and, 307 Rocking sensation, dizziness and, 521 Roll test, 252 described, 466 for horizontal SCC BPPV, 232 supine, 473 Romberg position, 561 Rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF), 55 Rotary chair test, 597 Rotation, 8–9 absence of, in clinical diagnosis, 8 couch, 8 Rotational vertebral artery syndrome, 524 Rotational chair, 10, 287–306 children and, 462, 463–465 components of, 288–302 booth lighting, 296–298 circulating fan, 296–298

computer, 301–302 electrical console, 301–302 enclosure, 291 head restraints, 298–301 headrest, 296 infrared patient video monitor, 295–296 motor projector, 292, 294 motors, 292 patient-clinician talk-back system, 294–295 safety harness, 298–299 software, 301–302 earth vertical axis, 288, 290 Ernst Josef Mach, 9 test, 115–116, 597 Rotational testing advantages, 326–328 calibration test, test preparation, 308 limitations of, 328 ocular motor test, 310 patient setup, 306–308 principles of, 284–285 protocols, 311 rotational chair, 287–306 advantages, 327–328 booth lighting, 296–297 calibration test, 308–310 circulating fan, 296–297 components of, 288–290 computer, 301–302 console, 301–302 enclosure, 291 goggles, 302–306 head restraints, 298–301 headrest, 296 infrared video monitor, 295–296 limitations of, 328 motors, 292–294 ocular motor test, 310 patient-clinician talk-back system, 294–295 patent setup, 306–308 physiological response during, 312–326 pre-appointment fundamentals, 306 protocols, 310–311 safety harness, 298 sinusoidal harmonic acceleration, 311–312 software, 301–302 rotational properties by frequency, 312 sinusoidal harmonic acceleration (SHA), 311–312 interpretation, 320–326 parameters, 315–319 physiological response during, 312–315 VOR (Vestibulo-ocular reflex) phase, 319–320 slow/fast phase, nystagmus and, 313

708

Balance Function Assessment and Management

Rotational testing  (continued) test distribution, 284 preparation, 306–311 protocols, 310–311 suite, 291 vestibular compensation and, 283, 286 of vestibular system, 283–285 clinical indications for, 285–286 patient population for, 286–287 principles of, 284–285 rotational chair, 287–306 test preparation, 306–311 video-oculography goggles for, 302–306 vestibulo-ocular reflex [VOR] symmetry, 320 symmetry interpretation, 320 Rotations, slow support surface, 388 RST (Reticulospinal tract), 77, 184, 459 Rubella, 470

S Saccade testing, 194–202 abnormalities of, 199 accuracy, 196 abnormalities of, 199 interpretation of, 196–202 latency, 196 abnormalities of, 199 parameters for, 195–196 patterns, 600–601 pediatric, 462 velocity and, 195–196 Saccades abnormally fast, 202 defined, 466 random, 466 Saccades eye movements, 34, 43 brainstem control of, 55–57 control of, 55–60 cortical, 58, 60 excitatory burst neurons, 55, 57 inhibitory burst neurons, 57 long-lead burst neurons, 57–58 omnipause neurons, 57 superior colliculus, 58 neural integrator physiology of, 60 VOR gain and, 343 Saccadic lateropulsion, lateral medullary syndrome and, 524 pulse disorders of, 62

generator, 59 Saccular macula, pulse generator, 71 Saccule, described, 71 Safety harness, rotational chair, 298–299 Salicylates, vestibular dysfunction and, 307 Salt, Ménièré’s disease and, 493 SC (Superior colliculus), 58 Scarpa’s ganglion, 71, 401, 429, 514 SCCs (Semicircular canals), 50, 52–53, 69 afferent physiology and, 72 assessing functional state of, 334 described, 70–71 elicited nystagmus in BPPV, 228 endolymph flow in, 73 excitatory projections from, 52 positional nystagmus and, 226 primary function of, 167 schematic view of, 334 vestibular system anatomy and, 70–71 Schwannomas, vertigo and, 127 Scleral search coils, eye movement recording and, 192 Sclerosis, idiopathic adolescent, 479 Scopolamine, 491 vestibular dysfunction and, 307 SCV (Slow component velocity), 219 Sedatives, vestibular dysfunction and, 307 Sedentary lifestyle, 520 Selective serotonin reuptake inhibitor (SSRI), 534 Semicircular canals (SCCs), 50, 52–53, 69 afferent physiology and, 72 assessing functional state of, 334 dehiscence described, 70–71 elicited nystagmus in BPPV, 228 endolymph flow in, 73 excitatory projections from, 52 hydrodynamic theory of function of, 9 positional nystagmus and, 226 primary function of, 167 schematic view of, 334 vestibular system anatomy and, 70–71 Semont maneuver, 237–238 Sense of Coherence Scale (SOC), 146 Sensorimotor performance, pathways related to, 523 Sensorineural hearing loss MCTSIB and, 484 Ménièré’s disease and, 493 vertigo and, 130 vestibular hypofunction and, 480 without vestibular testing, 479 Sensors, vestibular, development/maturation of, 27–30 Sensory interaction of balance test, 182–185

Index 709

neurons, 25 organization analysis, 372 patches, 18, 20, 22 Sensory organization test (SOT), 35, 369–382, 525 ankle versus hip movements, 371–372 case examples, 378–382 center of gravity alignment, 371 equilibrium scores, 370–371 pediatric, 465–466 presentation of results, 372 protocol, 370 psychiatric comorbidity and, 540 repeatability of, 375–376 results of normal sample, 372–375 sensory conditions, 369–370 six conditions, 564 stability limits, volitional reduction in, 376–378 static balance and, 483 VBT (Vestibular balance therapy) and, 480 vestibular deficits and, 534 Serotonin reuptake inhibitors, vestibular migraine and, 497 Severity of motion sensitivity (SMD), 534 SF-36 (Medical Outcomes Study Short form), 146 SHA (sinusoidal harmonic acceleration) acceleration response, 320–321 bilateral impairments, 324 central impairments, 324–326 clinical summary, 326 rotational testing, 311–312 parameters, 315–319 physiological response during, 312–315 VOR (Vestibulo-ocular reflex) phase, 319–320 unilateral peripheral impairments, 321–324 SHIMP (Suppression head impulse) temp, 336 Short Form Medical Outcomes, vestibular rehabilitation and, 559 Sickness Impact Profile (SIP), 146 Side-lying position, 245, 247 test, 230, 231 Single leg standing, 561 Singular neurectomy, for BPPV, 502 Sinusoidal harmonic acceleration abnormalities associated with, 329 acceleration response, 320–321 bilateral impairments, 324 central impairments, 324–326 rotational testing, 311–312 interpretation, 320–326 parameters, 315–319 physiological response during, 312–315 VOR (Vestibulo-ocular reflex) phase, 319–320

site-of-lesion abnormalities, 330 unilateral peripheral impairments, 321–324 SIP (Sickness Impact Profile), 146 Sixth sense, 3–4, 8 Skull taps, 403–404 Slow component velocity (SCV), 219 Slow-phase velocity (SPV) nystagmus, 264, 265–266 fixation index, 269 Slumber, medicinal, 8 SMD (Severity of motion sensitivity), 534 SMD (Space motion discomfort), 531 Smooth pursuit system, 43, 45, 61, 63–64 abnormalities, 64 Smooth pursuit tracking, 194, 276 eye movement recording and, 202–222 fixed-velocity pursuit, 205–206 sinusoidal target, 205 interpretations of, 206–208 pediatric, 457 pursuit tracking and analysis parameters, 203–205 technical considerations, 202–203 SN (Spontaneous nystagmus), 167 bedside assessment of, 169–170 SOC (Sense of Coherence Scale), 146 Social phobias, lightheadedness and, 128 Sodium, Ménièré’s disease and, 493 Software, rotational chair, 301–302 Solvents, vestibular dysfunction and, 307 Somatosensory effectiveness, for balance, 484 input, balance and, 91 system, age effects on, 581 “Some New Methods for Functional Testing of the Vestibular Apparatus and the Cerebellum,” 10 SOT (Sensory organization test), 35, 369–382, 525 ankle versus hip movements, 371–372 case examples, 378–382 center of gravity alignment, 371 equilibrium scores, 370–371 composite, 372 pediatric, 465–466 presentation of results, 372 protocol, 370 psychiatric comorbidity and, 540 repeatability, of results, 375–376 results of normal sample, 372–375 sensory conditions, 369–370 six conditions, 564 stability limits, volitional reduction in, 376–378 static balance and, 483 strategic analysis, 374–375

710

Balance Function Assessment and Management

SOT (Sensory organization test)  (continued) VBT (Vestibular balance therapy) and, 480 vestibular deficits and, 534 Sound amplification, superior semicircular canal dehiscence (SSCD), 131 SP (Summating potential), 440 Space motion discomfort (SMD), 531 Spatial navigation, vestibular dysfunction and, 582 orientation, vestibular system function and, 81 Spine, nystagmus and, 226 Spinocerebellar ataxia, 525 atrophy, 525 degeneration, 525 Spitzer, Alexander, criticizes Róbert Bárány, 11 Spontaneous nystagmus (SN), 167 bedside assessment of, 169–170 Spontaneous vestibular discharge patterns, 32–33 SPV (Slow-phase velocity) nystagmus, 264, 265–266 fixation index, 269 Square-wave jerks, 217 macro, 218 SSCD (Superior semicircular canal dehiscence), 431–432, 449 amplification of sound and, 131 drop attacks and, 131 syndrome, 450 test patterns, 605 vertigo and, 129, 130 SSRI (Selective serotonin reuptake inhibitor), 534 Stability, limits of, 88 STAI (State-Trait Anxiety Inventory), 146 State-Trait Anxiety Inventory (STAI), 146 Static balance defined, 483 tests, 483–484 compensation, 113, 114–115, 117–118 positional testing, pediatric, 467 posturography, 534 symptoms, 105 Statoacoustic ganglion neurons, 25 Stereocilia, 72 Stereociliary bundles, vestibular, 24 Steroids, Ménièré’s disease and, 493 Stimulants, vestibular dysfunction and, 307 Strategic analysis, computerized organization test, 374–375 Strength, gross motor skills and, 484 Streptomycin, vestibular dysfunction and, 307 Stretch reflex movement, 93 Styrene, vestibular dysfunction and, 307

Sulfa medications, Ménièré’s disease and, 493 Summating potential (SP), 440 Superior canal dehiscence, 180–182, 252, 420, 451, 453 diagnosis of, 432 repair of, 454 cerebellar artery, 72 oblique, 45, 47 rectus, 45, 46, 47 Superior colliculus (SC), 58 Superior semicircular canal dehiscence (SSCD), 431–432, 449 amplification of sound and, 131 drop attacks and, 131 repair of, 504–507 syndrome, 450 test patterns, 603–605 vertigo and, 129, 130 Superior vestibular nucleus (SVN ), 71, 76 Suppression head impulse (SHIMP) test, 336 Supranuclear progressive palsy, 525 saccadic palsies, 57 Surgical management of vertigo ablative vestibular surgery, 509, 515 cochlear endolymphatic shunt, 509 endolymphatic sac procedures, 508–509 labyrinthectomy, 509 Ménièré’s disease, 508 patient selection, 509 perilymphatic fistula repair, 503–504 postoperative care, 514, 516 posterior canal occlusion, 502–503 rationale for, 501–502 singular neurectomy for BPPV, 502 superior semicircular canal dehiscence (SSCD) repair, 504–507 vertigo and, test results, 511 vestibular neurectomy, 512–514 SVN (Superior vestibular nucleus), 71, 76 caloric responses profile, 265 Sway limits of, 88–89 oscillation cycle, 89 Swimming sensation, dizziness and, 521 Syncope, described, 128 Syndromic hearing loss, Pendred syndrome, 471 Systemic aminoglycosides, Ménièré’s disease and, 495

T Tandem Romberg, 561 Tatler, Benjamin, 12

Index 711

Tegretol vestibular dysfunction and, 307 vestibular migraine and, 497 Tenon’s capsule, 45 Tenormin, vestibular migraine and, 497 Test impaired structures, 598 patterns, 598 preparation, rotational testing, 306–311 protocols, rotational testing and, 310–311 Thalamocortical projections, 77–78 Thalamus, pulvinar of, 77 Theory of General Relativity, 9 Thiazide diuretics, Ménièré’s disease and, 493 Timed Up to Go (TUG) test, 157, 585 Tinnitus, Ménièré’s disease and, 131 Tobacco, vestibular dysfunction and, 307 Toddlers benign paroxysmal vertigo in, 479 benign recurrent vertigo and, 521 examination of, 462–463 rotational testing of, 287 vestibular dysfunction in, 479 vestibular migraine, 479 Toluene, vestibular dysfunction and, 307 Topamax, vestibular migraine and, 497 Topiramate, vestibular migraine and, 497 Top-shelf vertigo, 228 Torque motor OVAR and, 287 rotational chair, 288, 292, 298, 302, 328 head restraints, 298 Torsional nystagmus, 181, 228 Trait anxiety, 533 Traité du Vertige, 3 Tranquilizers, vestibular dysfunction and, 307 Transderm Scop, 492 Transdermal scopolamine, 492 Transduction channels, 28–29 hair cells, 28 response to, 29–30 Trauma, hair cell dysfunction and, 106 Treaty of Vertigo, 3 Triamterene, Ménièré’s disease and, 493 Triangle Completion Task, 582 Trichoroethylene, vestibular dysfunction and, 307 Tricyclic antidepressant nortriptyline, vestibular migraine and, 497 vestibular dysfunction and, 307 Trigeminal neuromas, vertigo and, 127 Trochlear Nerve, 49 Trunk-fixed strategy, 97

TUG (Timed Up to Go) test, 157, 567, 585 Tumors, vertigo and, 127 Two-Minute Walking test, 158

U “Über die Funktion der Bogengänge des Ohrlabyrinthes,” 8 “Über die Funktion der Bogengnge des Ohrlabyrinthes,” 8 UCLA-DQ (UCLA Dizziness Questionnaire), 149 Undifferentiated otocyst cells, 29 Unilateral caloric weakness, 266–267 interpretation/clinical significance of, 272–274 inactivation of MLF, 49 peripheral impairment, sinusoidal harmonic acceleration, 321–324 peripheral vestibular abnormality and, compensation for, 520 vestibular lesions, 109–112 compensation after, 113–120 vestibulopathy, 81 Unilateral vestibular hypofunction (UVH), 584 “Untersuchungen ueber den vom Vestibularapparat des Ohres reflektorisch ausgelösten rhythmischen Nystagmus und seine Begleiterscheinungen,” 10 «Up and Go» test, timed, 567 Up-beating nystagmus spontaneous, 250 vertical, 181 Usher syndrome, 470–471 Utricle described, 71 test patterns, 600–601 Utricular macula, 71

V VACU (Acute attack of vertigo” subscale), 154 Valium, 489 vestibular dysfunction and, 307 Valproic acid, vestibular migraine and, 497 Valsalvan induced nystagmus, 180–182 test, 182 Valsalvan, Antonio Mario, 180 Valsalvan maneuver (VM), 180, 252, 504 VAP (Vestibular Activities and Participation), 149 Vascular disease, 520 perfusion patterns, 599–600

712

Balance Function Assessment and Management

Vasodilators, Ménièré’s disease and, 494 Vasovagal syncope, 128 VBT (Vestibular balance therapy), 479 balance training, static/dynamic, 483–484 balance training for, 485 delivery of, 480 gaze stabilization training, 480–482 gross motor development and, 484–485 habituation training, 483 VCR (Vestibulocollic reflex), 80 pediatric, development of, 80 VDAL (Vestibular Disorders Activities of Daily Living), 148, 158–159, 561 vestibular rehabilitation and, 559 VDI (Vestibular Disability Index), 150 VEDGE (Vestibular Evidence Database to Guide Effectiveness), 167 head-impulse test and, 172 Velocity step testing (VST), 310 Velocity storage mechanism (VSM), 54–55, 108 VEMPs (Vestibular evoked myogenic potentials), 11–12, 260 history of, 399–400 pediatric, 467–468 significance of, 399–400 see also Cervical VEMP (cVEMP) Venlafaxine, vestibular migraine and, 497 Vergence system, 43, 45 Vertebrobasilar insufficiency, 524 system, vertigo and, 128 Vertical gaze-evoked nystagmus, 215 semicircular canals, video head impulse test of, 349–353 Vertigo, 489–492 19th century descriptions of, 530 associated events/symptoms, 130–132 case history characteristics of sensation, 126–129 components of, 126–132 importance of taking, 125–126 central positional, 252 concussion and, 527 defined, 126–127, 458 by Aristotle, 1 diagnostic categories, 521–527 acoustic neuroma, 526 cerebrovascular disease, 524 chiari malformation, 526 demyelinating disease, 526–527 head trauma and, 524–525 mal de debarquement syndrome, 527

neurodegenerative disease and, 525–526 vestibular migraine, 521–524 exacerbating factors, 131–132 hearing loss and, 130 medications for, 489–492, 490–491 Ménièré’s disease and, 493 pediatric, 458 prevalence of, 125 psychiatric factors, 521 psychological factors, 535–537 surgical management of ablative vestibular surgery, 509, 515 cochlear endolymphatic shunt, 509 endolymphatic sac procedures, 508–509 labyrinthectomy, 509 Ménièré’s disease, 508 patient selection, 509 perilymphatic fistula repair, 503–504 post operative care, 514, 516 posterior canal occlusion, 502–503 rationale for, 501–502 singular neurectomy for BPPV, 502 superior semicircular canal dehiscence (SSCD) repair, 504–507 vestibular neurectomy, 512–514 time course of attacks, 129–130 twenty-first century interactive model, 537–539 vestibular disorders and, 552 migraine and, 539 system, link between, 5–8 system and, 529 see also Dizziness Vertigo: Five Physician Scientists and the Quest for a Cure, 12 Vertigo Handicap Questionnaire (VHQ), 148 Vertigo of short duration” subscale (VSH), 154 Vertigo Symptom Scale (VSS), 147, 151, 152–153, 561 vestibular rehabilitation and, 559 Vesicle, otic, formation of, 18 Vestibular acute crisis, treatment of, 492 afferent neurite terminals, 26 neurons, 22 compensation, 105, 112–122, 167 anticholinergics and, 492 assessment of, 510 benzodiazepines and, 491 described, 520 lower extremity weakness and, 555 patient satisfaction and, 516 postoperative, 514 recovery and, 552–553

Index 713

rotational testing and, 283 vestibular neuritis and, 501 VOR and, 353 dysfunction, in children, 479 effectiveness, for balance, 484 end organs, innervation of, 25–27 evaluation patient history, 554–555 physical examination, 555 evoked myogenic potentials, 521 function development of, 28 developmental milestones of, 34–36 physiological origins of, 597–598 ganglion, 50 hypofunction, 479 gaze stability training and, 482 gross motor skills and, 484 MCTSIB and, 484 sensorineural hearing loss and, 480 input, balance and, 91 loss, gross motor delay and, 459–460 nerve, 50, 71 infections and, 106 interstitial nucleus of, 76–77 vestibular system anatomy and, 71 neurectomy, 512–514 neuritis, 106, 433 symptoms, 492 test patterns, 601, 602 vertigo and, 130 vestibular compensation and, 501 video head impulse test, 343–345 neuronitis BPPV (Benign paroxysmal positional vertigo), 539 pediatric, 458 nuclei, 50 nystagmus examination to identify, 167–170 lateral medullary syndrome and, 524 ocular reflex arc, 11 peripheral. see Peripheral vestibular physiology, 8–9 receptors, 25 reflexes, 78–80 testing, 35 rotational chair, 8, 10 schwannoma, 106 vertigo and, 127, 526 sensors, development/maturation of, 27–30 spontaneous discharge, 32–33 stereociliary bundles, 22 structures/pathways, 50–55

suppressants vestibular dysfunction and, 307 vestibular migraine and, 497 tests, 262 anatomy and, 597 patterns, 600–603 vascular migraine, 603–605 Vestibular Activities and Participation (VAP), 149 Vestibular balance therapy (VBT), 479 balance training, 485 static/dynamic, 483–484 delivery of, 480 gaze stabilization training, 480–482 gross motor development and, 484–485 Vestibular Disability Index (VDI), 150 Vestibular Disorders Activities of Daily Living (VADL), 148, 158–159, 561 vestibular rehabilitation and, 559 Vestibular Evidence Database to Guide Effectiveness (VEDGE), 167 Vestibular evoked myogenic potentials (VEMPs), 11–12, 260 history of, 399–400 pediatric, 467–468 significance of, 399–400 see also Cervical VEMP (cVEMP) Vestibular lesions compensation after bilateral, 120–121 central, 121 unilateral, 113–120 described, 106–112 effects of bilateral, 112 central organization of, 112 unilateral, 109–112 Vestibular migraine, 131, 521–524 benign paroxysmal positional vertigo (BPPV) and, 496 clonazepam and, 491 described, 521 diagnostic criteria for, 521 flow chart, 522 exacerbating factors, 132 medications for, 489 pediatric, 458, 479 stress and, 536 test patterns, 603–605 treatment of, 496–497 vertigo and, 130, 539 Vestibular nuclei, nuclei, 76–77 Vestibular nucleus (VN), 71, 77 rebalancing activity, 520

714

Balance Function Assessment and Management

Vestibular rehabilitation age and outcomes, 586 assessing progress in, 559–561 balance confidence scale activities, 560–561 daily living scale activities, 561 Dizziness Handicap Inventory (DHI), 559–560 subjective assessments, 559 balance standing measures, 561–566 elements of, 584–586 exercise program, 555–557 gait assessment, 566–567 groups that improved after, 556 history of, 549–552 impact of, 584–589 individual vs. group, 588–589 negative predictive factors, 553 new technologies impact on, 586–587 selected cases, 557–558 theoretical considerations, 552–554 compensation and recovery, 552–553 therapeutic trial of, 510–511 Vestibular Rehabilitation Benefit Questionnaire (VRBQ), 150 Vestibular sensory-evoked potentials (VSEPs), 11–12 Vestibular suppression, 489–492 medications for, 489–492 anticholinergics, 492 antihistamines, 491 benzodiazepines, 489 Vestibular system, 43 afferent physiology, 72–75 hair cells, 74 neural firing, 74–75 otolith organs and, 72, 74, 75 semicircular canals (SCCs), 72 age effects on, 578–580 autonomic system and, 78 bedside assessment of, 167–185 dynamic visual acuity test, 170–180 head shake, 172–176 horizontal head-impulse test, 170–172 sensory interaction of balance test, 182–185 spontaneous nystagmus, 167–170 valsalvan-induced nystagmus, 180–182 central, 76–78 described, 69 function of, 80–83 pediatric caloric irrigations, 468 development of, 457–458, 459–461 developmental changes, 460–461 disorders, 469–473

Dix-Hallpike and roll test, 466 evaluation of, 461–469 gaze testing, 466–467 optokinetic (OKN) nystagmus, 466 positional testing, 466–467 postural control assessment, 465–466 pursuit tracking, 466 random saccade, 466 sensory Organization Test (SOT), 465–466 VEMPs (Vestibular evoked myogenic potentials), 467–468 video head impulse test, 468–469 peripheral anatomy, 69–72 blood supply, 72 otolith organs and, 71 semicircular canals (SCCs), 70–71 vestibular nerve, 71 rotational testing of, 283–285 children, 287 clinical indications for, 285–286 patient population for, 286–287 pediatric, 287 principles of, 284–285 rotational chair, 287–306 video-oculography goggles for, 302–306 vertigo, link between, 5–8 vestibular reflexes and, 78–80 vestibulocollic reflex and, 80 vestibulo-ocular reflex and, 79–80 vestibulospinal reflex, 80 Vestibulo-cerebellum, 64, 77 role of, 65 Vestibulocochlear nerve, 69 Vestibulocollic reflex (VCR), 80 pediatric, development of, 459 Vestibulo-ocular reflex [VOR], 5, 44, 79–80, 459 analysis of, 315–320 at birth, 457 central organization of otolith-ocular reflexes, 53–54 velocity storage mechanism, 53–54 dynamic visual acuity test and, 480 function of, 50 gain hex plot, 351–352 interpreting results, 352 repeatability, 352–353 measurement of, 189 phase, 316 interpretation, 316–320 postural control and, 583–584 response

Index 715

calorics, 34–35 gain, 315–316 interpretation, 316–319 role of, 106–109 rotational testing, 319–320 semicircular canals (SCCs) and, 167 suppression, 353 symmetry, 320 vestibular compensation and, 353 video head impulse test, asymmetries, 343 “Vestibulo-Ocular Reflex Arc,” 11 Vestibulopathy, unilateral, 81 Vestibulospinal reflex, 80 pediatric, 459 vHIT (Video head impulse test), 597 advantages of, 353 bilateral vestibular loss, patient results, 339–340 calibration, 347–348 compensation, vestibular, 343–345 conducting, 345–349 overview of, 345 patient position, 346 cutoffs for patients, 345 described, 333–337 eye, optimizing image of, 347 gain, normal, 345 gentamicin ototoxicity and, 354 glasses, fitting the, 347 head impulse paradigm, suppression, 355–358 impulse testing, 260 sensor, 345–346 image, 346, 347 optimizing, 347 impulses, number of, 348–349 instructions, 348 Ménièré’s disease and, 354–355 new developments, 358 pediatric, 468–469 results, examples of, 337–340 sensitivity/specificity of, 353–354 validation of, 337 vertical semicircular canals, 349–353 vestibular neuritis and, 343–345 VOR gain asymmetries, 343 hex plot, 351–352 interpreting results, 352 repeatability, 352–353 vHIT (Video head impulse testing), 260 VHQ (Vertigo Handicap Questionnaire), 148 VID (Visually induced dizziness), 531, 538

Video head impulse test (vHIT), 260, 597 advantages of, 353 bilateral vestibular loss, patient results, 339–340 calibration, 347–348 compensation, vestibular, 343–345 conducting, 345–349 overview of, 345 patient position, 345–349 cutoffs for patients, 345 described, 333–337 eye, optimizing image of, 347 gain, normal, 345 glasses, fitting the, 347 head impulse paradigm, suppression, 355–358 head velocity sensor, 345–346 image, 346, 347 optimizing, 347 impulses, number of, 348–349 instructions, 348 Ménièré’s disease and, 354–355 new developments, 358 pediatric, 468–469 results, examples of, 337–340 sensitivity/specificity of, 353–354 validation of, 337 vertical semicircular canals, 349–353 vestibular neuritis and, 343–345 VOR gain, 340–343 asymmetries, 343 hex plot, 351–352 interpreting results, 352 repeatability, 352–353 Video-oculography (VOG), 189 goggles, 287, 288 calibration test and, 310 components of, 306 described, 302–306 eye movement recording and, 463–464 patient setup and, 308 rotational chair and, 288, 299 rotational test enclosure and, 291 rotational testing and, 302–306 video monitor and, 296 Vienna Medical Faculty Academic Senate, charges Róbert Bárány, 11 Viral inflammation, vertigo and, 130 Vision balance and, 92 vestibular abnormalities and, 520 vestibular disorders and, 552 Visual, 531 after-images, visual vertigo and, 3–4

716

Balance Function Assessment and Management

Visual  (continued) effectiveness, for balance, 484 fixation, 43–44 system, age effects on, 580–581 vertigo Erasmus Wells Debate, 4–5 visual after-images and, 3–4 see also Vertigo Visual Analog Scale, 561, 586 Visual vertigo, acuity test, dynamic, 170–180 Visual Vertigo Analog Scale (VVAS), 147 vestibular rehabilitation and, 559 Visually induced dizziness (VID), 531, 538 VM (Valsalvan maneuver), 180, 252, 504 VN (Vestibular nucleus), 71, 77 VNG (Infrared videonystagmography), 189 eye movements measured by, 262 goggles, 168, 173, 181 VOG (Video-oculography), 189 Volitional movement system, 93–94 Voltage-gated channels, 29 Voluntary flutter, 218 movements automatic postural movements and, 100 balance and, 99–100 properties of, 100 Vomiting peripheral vestibular disorders and, 519, 520 vestibular disorders and, 552 von Békésy, George, Nobel Prize, 10–11 von Héthárs, Heinrich Neumann, criticizes Róbert Bárány, 11 von Wenusch, F.R., 8 VOR (Vestibulo-ocular reflex), 79–80 analysis of, 315–320 at birth, 457 central organization of, 50–55 canal-ocular reflexes, 50, 52–53 otolith-ocular reflexes, 53–54 velocity storage mechanism, 53–54 dynamic visual acuity test and, 480 function of, 50 gain hex plot, 351–352 interpreting results, 352 repeatability, 352–353 measurement of, 189 pediatric, development of, 459 phase, 316 interpretation, 316–319 postural control and, 583–584

response gain, 315–316 interpretation, 316–319 responses to calorics, 34–35 role of, 106–109 rotational testing, 319–320 symmetry, 320 symmetry interpretation, 320 semicircular canals (SCCs) and, 167 suppression, 353 symmetry, 320 vestibular compensation and, 353 video head impulse test, asymmetries, 44, 343 VRBQ (Vestibular Rehabilitation Benefit Questionnaire), 150 VSEPs (Vestibular sensory-evoked potentials), 11–12 VSH (Vertigo of short duration” subscale), 154 VSM (Velocity storage mechanism), 54–55, 108 VSS (Vertigo Symptom Scale), 147, 151, 152–153, 561 vestibular rehabilitation and, 559 VST (Ipsilateral vestibulospinal tract), 76 VST (Velocity step testing), 310 VVAS (Visual Vertigo Analog Scale), 147

W Waardenburg syndrome, 471 Wade, Nicholas, 12 Walking, vestibular disorders and, 552 Wallace, Alfred Russel, 1 Wallenberg syndrome, 67–68, 524 Water (closed loop) irrigation, 260 (open-loop) irrigation, 260 Ways of Coping, 146 Weather, vertigo and, 132 Weaver, Ernst Glen, 439 Wells, William Charles, 2–4, 7, 12 Wenusch, F. R. von, 8 Westphal, Carl, 529 WHO (World Health Organization) DRQoL classification scheme, 143 ICIDH, 144 WHO-DAS II (World Health Organization Disability Assessment Schedule II), 146 WHOQoL-Brief (World Health Organization Quality of Life–Brief), 146 Willis, Thomas, 3 Wine, vestibular migraine and, 497 World Health Organization Disability Assessment Schedule II (WHO-DAS II), 146

Index 717

World Health Organization Quality of Life– Brief (WHOQoL-Brief), 146 World Health Organization (WHO) DRQoL classification scheme, 143 ICIDH, 144

X X1 (Times one) viewing, 480–481 X2 (Times two) viewing, 481 Xanax, 489 vestibular dysfunction and, 307 Xylene, vestibular dysfunction and, 307

Y Yeshiva University, 439

Z Zone of non-proliferation, 20–22 Zone of non-proliferation (ZNP), 20–22 Zoonomia, 2–6, 8

Γ γ-aminobutyric acid (GABA), 491