Developmental Cognitive Neuroscience: An Introduction [5 ed.] 1119904692, 9781119904694

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Developmental Cognitive Neuroscience

Developmental Cognitive Neuroscience An Introduction

Fifth Edition

Michelle de Haan, Iroise Dumontheil, and Mark H. Johnson

This edition first published 2023 © 2023 John Wiley & Sons Ltd Edition History Blackwell Publishers Ltd (1e, 1997); Blackwell Publishing Ltd (2e, 2005); John Wiley & Sons, Ltd (3e, 2011); John Wiley & Sons, Ltd (4e, 2015) All rights 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, photocopying, recording or otherwise, except as permitted by law. Advice on how to obtain permission to reuse material from this title is available at http://www.wiley.com/go/permissions. The right of Michelle de Haan, Iroise Dumontheil, and Mark H. Johnson to be identified as the authors of this work has been asserted in accordance with law. Registered Offices John Wiley & Sons, Inc., 111 River Street, Hoboken, NJ 07030, USA John Wiley & Sons Ltd, The Atrium, Southern Gate, Chichester, West Sussex, PO19 8SQ, UK For details of our global editorial offices, customer services, and more information about Wiley products visit us at www.wiley.com. Wiley also publishes its books in a variety of electronic formats and by print-­on-­demand. Some content that appears in standard print versions of this book may not be available in other formats. Trademarks: Wiley and the Wiley logo are trademarks or registered trademarks of John Wiley & Sons, Inc. and/or its affiliates in the United States and other countries and may not be used without written permission. All other trademarks are the property of their respective owners. John Wiley & Sons, Inc. is not associated with any product or vendor mentioned in this book. Limit of Liability/Disclaimer of Warranty While the publisher and authors have used their best efforts in preparing this work, they make no representations or warranties with respect to the accuracy or completeness of the contents of this work and specifically disclaim all warranties, including without limitation any implied warranties of merchantability or fitness for a particular purpose. No warranty may be created or extended by sales representatives, written sales materials or promotional statements for this work. The fact that an organization, website, or product is referred to in this work as a citation and/or potential source of further information does not mean that the publisher and authors endorse the information or services the organization, website, or product may provide or recommendations it may make. This work is sold with the understanding that the publisher is not engaged in rendering professional services. The advice and strategies contained herein may not be suitable for your situation. You should consult with a specialist where appropriate. Further, readers should be aware that websites listed in this work may have changed or disappeared between when this work was written and when it is read. Neither the publisher nor authors shall be liable for any loss of profit or any other commercial damages, including but not limited to special, incidental, consequential, or other damages. Library of Congress Cataloging-­in-­Publication Data Names: de Haan, Michelle, 1969– author. | Dumontheil, Iroise,   author. | Johnson, Mark H. (Mark Henry), 1960– author. Title: Developmental cognitive neuroscience : an introduction / Michelle de Haan,   Iroise Dumontheil, and Mark H. Johnson. Description: Fifth edition. | Hoboken, NJ, USA : John Wiley & Sons, Inc.,   2023. | Revised edition of: Developmental cognitive neuroscience / Mark   H. Johnson and Michelle de Haan. Fourth edition. 2015. | Includes   bibliographical references and index. Identifiers: LCCN 2022056812 (print) | LCCN 2022056813 (ebook) | ISBN   9781119904694 (Paperback) | ISBN 9781119904700 (ePDF) | ISBN   9781119904717 (epub) Subjects: LCSH: Cognitive neuroscience. | Developmental psychology. Classification: LCC QP360.5 .J64 2023 (print) | LCC QP360.5 (ebook) | DDC   612.8/233­–dc23/eng/20221222 LC record available at https://lccn.loc.gov/2022056812 LC ebook record available at https://lccn.loc.gov/2022056813 Cover Design: Wiley Cover Image: Courtesy of Danyal Akarca, Alexa Mousley, Alicja Monaghan, Sofia Carozza and Duncan Astle Set in 9.5/12.5pt STIXTwoText by Straive, Pondicherry, India

To our parents, who provided both our nature and our nuture.

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Contents List of Figures  x List of Tables  xvii List of Abbreviations  xviii Preface to the First Edition  xx Preface to the Fifth Edition  xxii About the Companion Website  xxiii 1 The Biology of Change  1 ­Viewpoints on Development  1 ­Analyzing Development  5 ­Why Take a Cognitive Neuroscience Approach to Development?  6 ­Why Take a Developmental Approach to Cognitive Neuroscience?  7 ­The Cause of Developmental Change  8 ­Three Viewpoints on Human Functional Brain Development  10 ­Interactive Specialization  11 ­Looking Forward  12 2 Methods and Populations  14 ­Introduction  14 ­Behavioral and Cognitive Tasks  15 ­Assessing Brain Function in Development  16 ­Observing Brain Structure in Development  18 ­Animal Studies and Genetics  19 ­Neurodiversity and Developmental Disorders  20 ­Atypically Developing Brains  22 ­Sensory and Environmental Variations  25 ­Familial Risk Populations  26 3 From Gene to Brain  28 ­The History of the Gene  28 ­Principles of Gene Function  29 ­Genetics and Developmental Cognitive Neuroscience  32 ­The Epigenome  36 ­The FOXP2 Gene  36

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Contents

4 Building a Brain  39 ­An Overview of Primate Brain Anatomy  40 ­Prenatal Brain Development  43 ­Postnatal Brain Development  46 ­The Development of Cortical Areas: Protomap or Protocortex?  53 ­Differential Development of Human Cortex  61 ­Postnatal Brain Development: Adolescence  64 ­Postnatal Brain Development: The Hippocampus and Subcortical Structures  65 ­Neurotransmitters and Neuromodulators  66 ­What Makes a Brain Human?  69 ­General Summary and Conclusions  70 5 Vision, Orienting, and Attention  71 ­The Development of Vision  71 ­The Development of Visual Orienting  76 ­Saccade Planning  86 ­Visual Attention  89 ­General Summary and Conclusions  95 6 Perceiving and Acting in a World of Objects  97 ­The Dorsal and Ventral Visual Pathways  98 ­Hidden Objects  101 ­Neural Oscillations and Object Processing  105 ­General Summary and Conclusions  106 7 Perceiving and Acting on the Social World  107 ­The Social Brain  107 ­Face Recognition  109 ­Brain Development and Face Recognition in Humans  113 ­Perceiving and Acting on the Eyes  120 ­Understanding and Predicting the Behavior of Others  123 ­The Atypical Social Brain  127 ­General Summary and Conclusions  131 8 Learning and Long-­Term Memory  133 ­Development of Explicit Memory  135 ­Implicit Memory  143 ­General Summary and Conclusions  145 9 Language 147 ­Introduction  147 ­Are Some Parts of Cortex Critical for Language Acquisition?  149 ­Neural Basis of Speech Processing in Infants  155 ­Influence of Experience on Brain Language Processing  156 ­Neural Correlates of Typical and Atypical Language Acquisition  158 ­General Summary and Conclusions  161

Contents

10 Prefrontal Cortex, Executive Functions, and Decision-­Making  163 ­Introduction  164 ­Prefrontal Cortex and Object Permanence  164 ­Prefrontal Cortex and Executive Functions Development During Adolescence  166 ­Social Decision-­Making and Self-­Regulation During Adolescence  170 ­Prefrontal Cortex, Skill Learning, and Interactive Specialization  173 ­General Summary and Conclusions  177 11 Educational Neuroscience  179 ­Numeracy  181 ­Literacy  185 ­Domain-­General Skills: Executive Functions and Processing Speed  186 ­Individual Differences and Training Interventions  189 ­Dyscalculia and Dyslexia  192 ­General Summary and Conclusions  195 12 Global and Cross-­Cultural Perspectives  197 ­Developmental Cognitive Neuroscience: Factors to Consider in Global, Cross-­Cultural Settings  198 ­Cognitive Neurosciences Approaches to Look at Commonalities Across Global/Cultural Settings  199 Infants’ Response to Novelty  199 Social Processing  200 Numeracy and Literacy  202 ­Developmental Cognitive Neuroscience: Examining Factors Affecting Similarities and Differences Among Global Settings and Cultures  203 Maternal Stress, Caregiving and Education and Brain Responses to Social Stimuli  203 Interactions Between Factors Predicting Individual Differences in Neurocognition  203 Brain Responses in the Context of Global-­Specific Risk  204 ­General Summary and Conclusions  204 13 Toward an Integrated Developmental Cognitive Neuroscience  206 ­Introduction  206 ­Three Viewpoints on Human Functional Brain Development  207 ­Interactive Specialization (IS)  209 ­Emerging Networks  213 ­Genes and Cognitive Development  217 ­Relations Between Brain Structure and Function in Development  218 ­Neuroconstructivism  219 ­Criticisms of Developmental Cognitive Neuroscience  221 ­Applications of Developmental Cognitive Neuroscience  223 ­Concluding Remarks  224 References  225 Index  282

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List of Figures Figures listed below without a page number appear in the color plate section. The color plate section appears between pages 136 and 137. Figure 1.1 Drawings such as this influenced a 17th-­century school of thought, the “spermists,” who believed that there was a complete preformed person in each male sperm and that development merely consisted of increasing size.  3 Figure 1.2 The epigenetic landscape of Waddington (1975).  9 Figure 2.1 An illustration of the relative strengths and weaknesses of different functional brain imaging methods used with infants and children. Figure 2.2 An infant wearing a high-­density ERP/EEG system (EGI Geodesic Sensor Net) during a study on the “mirror neuron system”. The sensor net consists of damp sponge contacts that rest gently on the scalp. Figure 2.3 Infants in (a) the UK, (b) Bangladesh, and (c) The Gambia engaged in functional near-­infrared spectroscopy studies. Light emitters and detectors are incorporated into the head caps. Figure 2.4 The expansion of myelinated fibers over early postnatal development as revealed by a new structural MRI technique. Figure 3.1 (a) The basic double helix structure of DNA in which two nucleotide strands coil around each other. (b) Detail showing how the two strands are linked by chemical bonds between the bases of nucleotides.  30 Figure 3.2 An illustration of the complex causal pathway between a genetic level defect and its consequences for behavior from Fragile-­X syndrome.  35 Figure 4.1 A simplified schematic diagram which illustrates that, despite its convoluted surface appearance (top), the cerebral cortex is a thin sheet (middle) composed of six layers (bottom). The convolutions in the cortex arise from a combination of growth patterns and the restricted space inside the skull. In general, differences between mammals involve the total area of the cortical sheet, and not its layered structure. Each of the layers possesses certain neuron types and characteristic input and projection patterns.  41 Figure 4.2 A typical cortical pyramidal cell. The apical dendrite is the long process that extends to the upper layers and may allow the cell to be influenced by other neurons. An axon projects to subcortical regions.  42 Figure 4.3 A sequence of drawings of the embryonic and fetal development of the human brain. The drawings of brains beneath those of 25–100 days are the same images

List of Figures

Figure 4.4 Figure 4.5 Figure 4.6

Figure 4.7 Figure 4.8

Figure 4.9

Figure 4.10

Figure 4.11

Figure 4.12

Figure 4.13

Figure 4.14

but drawn to the same scale as those in the row below. The forebrain, midbrain, and hindbrain originate as swellings at the head end of the neural tube. In primates, the convoluted cortex grows to cover the midbrain, hindbrain, and parts of the cerebellum. Prior to birth, neurons are generated in the developing brain at a rate of more than 250,000 per minute.  44 MRI structural scans of a 4-­month-­old infant (top) and a 12-­year-­old adolescent (below).  46 A drawing of the cellular structure of the human visual cortex based on Golgi stain preparations from Conel (1939–1967).  48 The sequence of axon myelination by an oligodendrocyte. (a–d) show the sequence of initial contact, then engulfing and surrounding the axon, followed by spiraling around the axon to form the final myelin sheath.  49 Resting state networks in a single representative infant. Rows A to E each show one resting state network at three axial sections. Figure illustrating the approximate timeline for some of the most important changes in human brain development, including the characteristic rise and fall of synaptic density. Graph showing the development of density of synapses in human primary visual cortex and resting glucose uptake in the occipital cortex as measured by PET. ICMRGlc is a measure of the local cerebral metabolic rates for glucose.  51 A color-­coded map of changes in cortical gray matter with development. The maps illustrate regional variations in decreases in gray matter density between the ages of 5 and 20 years. The brain maps (center panel) show prominent clusters where “superior” and “average” intelligence groups differ significantly in the trajectories of cortical development. The graphs show the developmental trajectories for these regions. The age of peak cortical thickness is arrowed for each of the three groups in each region. Cytoarchitectural map of the cerebral cortex. Some of the most important specific areas are as follows. Motor cortex: motor strip, area 4; pre-­motor area, area 6; frontal eye fields, area 8. Somatosensory cortex: areas 3, 1, 2. Visual cortex: areas 17, 18, 19. Auditory cortex: areas 41 and 42. Wernicke’s speech area: approximately area 22. Broca’s speech area: approximately area 44 (in the left hemisphere).  54 The radial unit model of Rakic (1987). Radial glial fibers span from the ventricular zone (VZ) to the cortical plate (CP) via a number of regions: the intermediate zone (IZ) and the subplate zone (SP). RG indicates a radial glial fiber, and MN a migrating neuron. Each MN traverses the IZ and SP zones that contain waiting terminals from the thalamic radiation (TR) and corticocortical afferents (CC). As described in the text, after entering the cortical plate, the neurons migrate past their predecessors to the marginal zone (MZ).  55 Patterning of areal units in somatosensory cortex. The pattern of “barrels” in the somatosensory cortex of rodents is an isomorphic representation of the geometric arrangement of vibrissae found on the animal’s face. Similar

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patterns are present in the brain stem and thalamic nuclei that relay inputs from the face to the barrel cortex.  60 Figure 4.15 PET images illustrating developmental changes in local cerebral metabolic rates for glucose (ICMRGlc) in the normal human infant with increasing age. Level 1 is a superior section, at the level of the cingulate gyrus. Level 2 is more inferior, at the level of caudate, putamen, and thalamus. Level 3 is an inferior section of the brain, at the level of cerebellum and inferior position of the temporal lobes. Gray scale is proportional to ICMRGlc, with black being highest. Images from all subjects are not shown on the same absolute gray scale of ICMRGlc; instead, images of each subject are shown with the full gray scale to maximize gray scale display of ICMRGlc at each age. (A) In the 5-­day-­old, ICMRGlc is highest in sensorimotor cortex, thalamus, cerebellar vermis (arrows), and brain stem (not shown). (B, C, D) ICMRGlc gradually increases in parietal, temporal, and calcarine cortices; basal ganglia; and cerebellar cortex (arrows), particularly during the second and third months. (E) In the frontal cortex, ICMRGlc increases first in the lateral prefrontal regions by approximately 6 months. (F) By approximately 8 months, ICMRGlc also increases in the medial aspects of the frontal cortex (arrows), as well as the dorsolateral occipital cortex. (G) By 1 year, the ICMRGlc pattern resembles that of adults (H).  63 Figure 5.1 Diagram of the developmental sequence of visual behavior (left of vertical line) and ventral-­and dorsal-­stream neural systems contributing to this (right of vertical line).  73 Figure 5.2 Simplified schematic diagram illustrating how projections from the two eyes form ocular dominance columns in the visual cortex. LGN, lateral geniculate nucleus.  74 Figure 5.3 (a) Afferents from both eyes synapse on the same cells in layer 4, thereby losing information about the eye of origin. (b) Afferents are segregated on the basis of eye origin (R and L), and consequently recipient cells in layer 4 may send their axons to cells outside of that layer so as to synapse on cells that may be disparity-­selective.  75 Figure 5.4 Diagram representing some of the main neural pathways and structures involved in visual orienting and attention. BS, brain stem; LGN, lateral geniculate nucleus; V1, V2, and V4, visual cortical areas; MT, middle temporal area; SC, superior colliculus; SN, substantia nigra; BG, basal ganglia.  78 Figure 5.5 Brain areas involved in stimulus-­driven and goa-­driven attention. Figure provide by Iroise Dumontheil.  82 Figure 5.6 The oculomotor delayed response task as designed for use with infants. Infant subjects face three computer screens on which brightly colored moving stimuli appear. At the start of each trial, a fixation stimulus appears on the central screen. Once the infant is looking at this stimulus, a cue is briefly flashed up on one of the two side screens. Following the briefly flashed cue, the central stimulus stays on for between 1 and 5 seconds, before presentation of two targets on the side screens. By measuring delayed looks to the cued location prior to the target onset, Gilmore and Johnson (1995) established that infants can retain information about the cued location for several seconds.  84

List of Figures

Figure 5.7 Grand-­average saccade-­locked potentials at the midline, parietal electrode in (a) 6-­month-­old infants, (b) 12-­month-­old infants, and (c) adults. The vertical bar marks the saccade onset, a spike potential (SP) is evident in adults and 12-­month-­olds, but not at 6 months.  85 Figure 5.8 Three types of saccades made by young infants in response to two targets briefly flashed as shown. (a) A “vector summation” saccade in which eye movement is directed between the two targets. (b) A “retinocentric” saccade in which the second saccade is directed to the location corresponding to the retinal error when the flash occurred. (c) An “egocentric” saccade which corresponds to the use of extra-­retinal information to plan the second saccade. Between birth and 6 months, infants shift from the first two types of response to the third.  87 Figure 5.9 Heart-­rate-­defined phases of sustained attention.  91 Figure 6.1 Major routes whereby retinal input reaches the dorsal and ventral streams. The diagram of the brain on the right of the figure shows the approximate routes of the projections from primary visual cortex to posterior parietal and the inferotemporal cortex, respectively. LGNd, lateral geniculate nucleus, pars dorsalis; Pulv, pulvinar; SC, superior colliculus.  98 Figure 6.2 A diagram showing the object processing model of Mareschal et al. Mareschal et al.  102 Figure 6.3 Gamma-­band EEG activity recorded from infants in the Kaufman, Csibra, and Johnson (2003a) experiment. (a) Time-­frequency analysis of the average EEG at three electrodes over the right temporal cortex (around T4) during the phase in which the tunnel was lifted showed higher activations when the object should have been below the tunnel. Black asterisks below the maps indicate a significant difference from baseline; red asterisks indicate a significant difference between conditions in the average gamma activity in 200 ms-­long bins. (b) A topographical map of the between-­condition difference of gamma-­band (20–60 Hz) activity during the occlusion-­related peak gamma activity (from –400 to –200 ms) revealed a right-­temporal focus. Circles signify right-­temporal electrode sites. Figure 7.1 Some of the regions involved in the human social brain network.  108 Figure 7.2 Data showing the extent of newborns’ head and eye turns in following a schematic face, a scrambled face, and a blank (unpatterned) stimulus.  110 Figure 7.3 A summary of human newborn and model responses to schematic images. The top row represents some of the schematic patterns presented to both newborns and the “retina” of the neural network model. The next two rows illustrate the lateral geniculate nucleus and visual cortex stages of the models processing. The bottom row indicates the output of the model, with the preferred stimuli being b, c, and d. The preferences of the model correspond well to the result obtained with newborn infants.  112 Figure 7.4 Key regions involved in face processing in adults.  114 Figure 7.5 Schematic illustration of the stimuli that might be optimal for eliciting a face-­related preference in human newborns. These hypothetical representations were created by integrating the results from several experiments with newborns.  116

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Figure 7.6 Differential activation for each stimulus category mapped onto an inflated brain: (a) ventral view and (b) a lateral view of the right hemisphere for all three age groups. In contrast to older groups, young children showed no face-­selective activation in face-­related areas. However, objects and buildings or navigation yielded similar patterns of selective activation at all ages. Abbreviations: FFA, fusiform face area; LO, lateral occipital object area; OFA, occipital face area; PPA, parahippocampal place area; STS, superior temporal sulcus. Figure 7.7 Example of the edited video image illustrating the stimulus for experiment 1 in Farroni et al. (2000). In this trial the stimulus target (the duck) appears on the side incongruent with the direction of gaze.  121 Figure 7.8 Results of the Farroni et al. 2002 preferential looking study with newborns. (a) Mean looking times (and standard error) spent at the two stimulus types. Newborns spent significantly more time looking at the face with direct gaze than looking at the face with averted gaze. (b) Mean number of orientations toward each type of stimulus. (v) Filled triangles indicate reference scores for the direct gaze over the averted gaze for each individual newborn. Open triangles indicate average preference scores.  122 Figure 8.1 Brain areas involved in memory. Figure provided by Iroise Dumontheil.  134 Figure 8.2 (a) Example of a 2-­step imitation task—­the actions are to put down the ramp, and roll the car down. (b) Example of the mobile conjugate reinforcement task, showing the baby with the ribbon attached to their leg, the mobile they can control, and the phone camera recording the session. Figure 8.3 Memory performance for Beth, Jon, and Kate on the Rey-­Osterrieh Complex Figure. Left column shows their normal copying of the figure, while the right column shows how much less they were able to recall after a 40-­minute delay compared to control participants.  141 Figure 9.1 (a) Some of the key structures involved in language processing. Top left: Schematic view of information flow from posterior sensory areas to frontal response areas through the inferior temporofrontal loop. The shaded regions show where brain damage causes fluent (Wernicke’s) and nonfluent (Broca’s) aphasia. These regions are conceptual rather than anatomical. Bottom left: The Sylvian fissure has been pulled out and down in the direction of the arrows to reveal the insula (I) and the auditory cortex (H, P) on the superior surface of the temporal lobe. The region of the frontal operculum indicated as F5 contains mirror neurons in the monkey. It is thought that these neurons play a crucial role in imitation learning. Right: Enlarged view of Heschl’s gyrus and planum temporal. (b) Dorsal and ventral language streams.  148 Figure 9.2 Cortical areas showing increases in blood oxygenation on fMRI when normal hearing adults read English sentences (top), when congenitally deaf native signers read English sentences (middle), and when congenitally deaf native signers view sentences in their native sign language (American Sign Language).  154 Figure 9.3 Covert language task: group average fMRI activation in the unaffected and affected members of the KE family. Activated regions are projected onto the

List of Figures

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Figure 11.1 Figure 11.2 Figure 11.3

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Figure 13.1

Figure 13.2

surface rendering of a typical 3D individual brain, displayed at a statistical threshold of p  children

association areas

children > young-adults

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primary sensory areas subcortical areas

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Figure 13.3  Developmental changes in inter-­regional functional connectivity. A graphical representation of developmental changes in functional connectivity along the posterior-­anterior and ventral-­dorsal axes of the brain highlighting higher sub-­cortical connectivity and lower paralimbic connectivity in children compared to young adults. Supekar et al., 2009. Reproduced with permission of the authors and of Public Library of Science, Biology.

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