Journal für Hirnforschung: Band 19, Heft 2 1978 [Reprint 2021 ed.] 9783112526729, 9783112526712

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ISSN 0021 - 8359

Heft2-1978 Band 19

J

O

U

T i l d i

für Hirnforschung Internationales Journal für Neurobiologie Begründet von Cécile und Oskar Vogt

Redaktion: J.Anthony, Paris A. Hopf, Düsseldorf W Kirsche, Berlin • J.Szentàgothai, Budapest WisaSekretär: J.Wenzel, Berlin

Akademie-Verlag • Berlin EVP 25,-M - 32105

Begründet von Cécile und Oskar Vogt Unter Mitwirkung des Cécile und Oskar Vogt Instituts für Hirnforschung in Düsseldorf und der Arbeitsgemeinschaft für vergleichende Neuroanatomie der Fédération mondiale de Neurologie (World Federation of Neurology)

Mitherausgeber: H . ADAM, Salzburg—Wien

O. S.

A D R I A N O W , Moskau J . A R I É N S K A P P E R S , Amsterdam E. C R O S B Y , Ann Arbor A. D E W U L F , Corbeck-Lo J . E S C O L A R , Zaragoza R. H A S S L E R , Frankfurt a. M. E. H E R Z O G , Santiago J . J A N S E N , Oslo J . K O N O R S K I , Warschau S T . K Ö R N Y E Y , Pécs M . M A R I N - P A D I L L A , Hanover-New J . M A R É A L A , Koéice H. A. M A T Z K E , Lawrence D . M I S K O L C Z Y , Tirgu Mures G . P I L L E R I , Waldau —Bern T. O G A W A , Tokyo

Le JOURNAL F Ü R HIRNFORSCHUNG publiera des études sur la morphologie normale (anatomie, histologie, cytologie, microscopie électronique, histochimie), sur le développement du système nerveux ainsi que des études anatomiques expérimentales. On acceptera aussi des travaux du caractère de la coopération entre des domaines différents à condition qu'ils contiennent des résultats morphologiques obtenus par les méthodes de la neuromorphologie et de la neurophysiologie ou de la neuropharmacologie et de la neurochimie. Les travaux doivent contenir des acquisitions nouvelles sur l'action réciproque entre la structure et la fonction. Des études neuropathologiques seront seulement acceptées quand elles contribuent à la conaissance des structures normales, des changements structurels ou de leur signification fonctionelle. Des études sur la localisation cérebrale de phénomènes expérimentaux ou cliniques d'excitation ou de déficit (doctrine des localisations) seront également publiées par le JOURNAL F Ü R HIRNFORSCHUNG. Une partie spéciale sera réservée à la neurobiologie comparée.

Hampshire

B . REXED, U p s a l a

H. S T E P H A N , Frankfurt a. M . W. J . C. V E R H A A R T , Leiden

Bezugsmöglichkeiten des ,,Journal für Hirnforschung".

F. W A L B E R G , Oslo K. G. W I N G S T R A N D , Kopenhagen E . W I N K E L M A N N , Leipzig W . W Ü N S C H E R , Berlin A . D . Z U R A B A S H V I L I , Tbilissi

— in der DDR an eine Buchhandlung oder an den AkademieVerlag, DDR - 108 Berlin, Leipziger Straße 3 - 4

M. VOGT, Cambridge

Im JOURNAL F Ü R HIRNFORSCHUNG werden Arbeiten aus dem Gesamtgebiet der normalen Morphologie (Anatomie, Histologie, Cytologie, Elektronenmikroskopie, Histochemie) und der Entwicklungsgeschichte des Nervensystems unter Einschluß experimentell-anatomischer Arbeiten veröffentlicht. Es werden auch Arbeiten multidisziplinären Charakters aufgenommen, sofern sie morphologische Ergebnisse beinhalten, die mit neuromorphologischen und neurophysiologischen oder neuropharmakologischen bzw. neurochemischen Methoden gewonnen wurden und einen Erkenntnisgewinn hinsichtlich der Wechselwirkung zwischen Struktur und Funktion beinhalten. Neuropathologische Arbeiten werden nur angenommen, wenn sie Beiträge zur normalen Struktur, den Strukturwandlungen oder deren funktionellen Bedeutungen enthalten. Zum Publikationsgebiet des JOURNAL F Ü R HIRNFORSCHUNG gehören auch Arbeiten, die sich mit der Zuordnung experimenteller Reiz- und Ausfallerscheinungen bzw. klinischen Symptomen zu bestimmten Strukturen des Gehirns („Lokalisationslehre") befassen. Als spezielles Publikationsgebiet ist die vergleichende Neurobiologie vorgesehen.

The JOURNAL F Ü R HIRNFORSCHUNG will publish studies on normal morphology (anatomy, histology, cytology. electron microscopy, histochemistry), on the development of the nervous system, as well experimental anatomical studies. Papers of multidisciplinary character will also be included so far as they contain morphological results which were obtained using neuromorphological and neurophysiological or neuropharmacological and neurochemical methods and provide further information on the interaction between structure and function. Neuropathological studies will only be published if they contribute to the knowledge of normal structures structurals changes or their functional significance. Papers dealing with the cerebral localization of experimental excitation and deficit phenomena or clinical symptoms (localization theory) will also be published by the J O U R N A L F Ü R HIRNFORSCHUNG. A special part of the publication is reserved for comparative neurobiology.

Bestellungen sind zu richten

— im sozialistischen Ausland an eine Buchhandlung für fremdsprachige Literatur oder an den zuständigen Postzeitungsvertrieb — in der B R D und Westberlin an eine Buchhandlung oder an die Auslieferungsstelle KUNST UND WISSEN, Erich Bieber, 7 Stuttgart 1, Wilhelmstraße 4 - 6 — in Österreich an den Globus-Buchvertrieb, 1201 Wien, Höchstädtplatz 3 — im übrigen Ausland an den Internationalen Buch- und Zeitschriftenhandel; den Buchexport, Volkseigener Außenhandelsbetrieb der Deutschen Demokratischen Republik, DDR - 701 Leipzig, Postfach 160, oder an den Akademie-Verlag, DDR - 108 Berlin, Leipziger Straße 3 bis 4

Journal für Hirnforschung Herausgeber: Im Auftrag des Akademie-Verlages von einem internationalen Wissenschaftlerkollektiv herausgegeben. Verlag: Akademie-Verlag, DDR -108 Berlin, Leipziger Straße 3 - 4 ; Fernruf: 2236 229 und 2236 221; Telex-Nr.: 114420; Bank: Staatsbank der DDR, Berlin, Kto.-Nr.: 6836-26-20712. Schriftleitung: Prof. Dr. W. Kirsche, Berlin. Wissenschaftlicher Sekretär: Dr. Jürgen Wenzel, Berlin. Veröffentlicht unter der Lizenznummer 1326 des Presseamtes beim Vorsitzenden des Ministerrates der Deutschen Demokratischen Republik. Gesamtherstellung: V E B Druckhaus „Maxim Gorki", DDR - 74 Altenburg. Erscheinungsweise: Das Journal für Hirnforschung erscheint jährlich in einem Band mit 6 Heften. Bezugspreis eines Bandes 180,— M zuzüglich Versandspesen (Preis für die DDR 1 5 0 , - M); Preis je Heft 3 0 , - M (Preis für die DDR 2 5 , - M). Bestellnummer dieses Heftes 1018/19/2. © 1978 by Akademie-Verlag Berlin. Printed in the German Democratic Republic. AN (EDV) 60315

ISSN 0 0 2 1 - 8 3 5 9 J . Hirnforsch. 19

(1978) 101-108

•

•

Journal

Internationales Journal für Neurobiologie

^jj y

Hirnforschung

Heft 2 • 1978 • Band 19

Aus dem Anatomischen Institut des Bereiches Medizin (Charite) der Humboldt-Universität zu Berlin (Direktor: Prof. Dr. sc. med. W. K I R S C H E )

Fluoreszenzhistochemische und neurohistologische Untersuchungen zur adrenergen Innervation des Cortex pyriformis der Ratte1'2 Herbert

DANNER

und Claus

PFISTER

Mit 5 Abbildungen (Eingegangen am 11. Juni 1977)

Summary: The pyriform region of normal adult rats was investigated by fluorescence histochemistry and Golgirapid-impregnation technique. Fluorescence microscopically noradrenaline and dopamine fibers could be described in typical arrangement and distribution. It is suggested that various Golgi-"beaded"-axons in the cortex pyriformis may be equivalent to the fluorescence histochemically demonstrated varicose catecholamine axons. This would raise the possibility of interpreting, in the Golgi impregnation technique, kinds of axons in a functional manner. Zusammenfassung: Die Regio pyriformis der normalen juvenilen Ratte wurde fluoreszenz-histochemisch und mittels der Golgi-Rapid-Imprägnations-Technik untersucht. Fluoreszenzoptisch konnten Noradrenalin- und Dopamin-Fasern in charakteristischer Anordnung und Verteilung dargestellt werden. Es wird vermutet, daß es sich bei den nach Golgi-Rapid-Imprägnation dargestellten unterschiedlichen varicösen Axonen im Cortex pyriformis um das Äquivalent zu den fluoreszenzhistochemisch nachweisbaren CatecholaminAxonen handelt. Damit bestünde die Möglichkeit, bestimmte Axontypen in der Golgi-Rapid-Darstellung funktionell zu interpretieren.

Einleitung

handlung n a c h F A L C K und H I L L A R P ( F A L C K et al.

Mit Hilfe der hochsensitiven G l y o x y l s ä u r e - T e c h n i k

1 9 6 2 ; F U X E et al. 1 9 7 0 ; BJÖRKLUND et al. 1972) er-

n a c h LiNDVALLet al. (1974 a) ist es möglich, Catechol-

hobenen B e f u n d e hinsichtlich der catecholaminergen

aminfasern in ihrem g e s a m t e n Verlauf bis zu ihrem

I n n e r v a t i o n des Cortex cerebri k o n n t e n präzisiert und

T e r m i n a t i o n s g e b i e t zu verfolgen u n d morphologisch

erweitert werden ( L I N D V A L L and B J Ö R K L U N D 1 9 7 4 b ;

dopaminerge

B E R G E R et al. 1974).

Axone

deutlich

von

noradrenergen

A x o n e n zu unterscheiden ( L I N D V A L L and B J Ö R K L U N D 1 9 7 4 a). Die 1 2

D a es die G l y o x y l s ä u r e - T e c h n i k n a c h

LINDVALL

et al. (1974 a) ermöglicht, Noradrenalin- u n d Dopn a c h Anwendung

der

Paraformaldehyd-Be-

aminfasern m i t Sicherheit zu erkennen u n d zu ver-

Mit dankenswerter Unterstützung durch einen Forschungsauftrag des Ministeriums für Wissenschaft und Technik der DDR. Herrn Prof. Dr. J . Szentagothai zur Vollendung des 65. Lebensjahres mit herzlichen Glückwünschen gewidmet.

Hirnforschung, Bd. 19, Heft 2

8

102

Danner, H „ und C. Pfister

Abb. 1. Catecholamin-Innervation des Cortex pyriformis (Fissura rhinalis) der Ratte. Äußere corticale Schichten; vorwiegend Noradrenalin-Fasern. Abb.-Maßstab: 380:1

folgen (LINDVALL and B J Ö R K L U N D 1974b; B E R G E R et al. 1974, 1976), war es naheliegend, derartig fluoreszenzhistochemisch definierbare Axontypen mit Axonen ähnlicher Morphologie nach Golgi-Imprägnations-Darstellung zu vergleichen.

2. Golgi-Rapid-Imprägnations-Technik nach V A L V E R D E (1970) Zur Untersuchung gelangten 6 unbehandelte Ratten beiderlei Geschlechts im Alter von 6 — 8 Wochen. Schnittdicke: 200 (xm. Die Mikrophotos wurden mit der Kleinbildkamera E x a k t a R T L 1000 angefertigt. Filmmaterial: ORWO N P 27 bzw. N P 15

Befunde

Material und Methode 1. Glyoxylsäure-Technik nach L I N D V A L L et al. (1974a): Zur Untersuchung gelangten 12 männliche, unbehandelte Ratten im Alter von 10 — 12 Wochen. Herstellung von Hirnserienschnitten am Vibratom® (Oxford Instruments, California). 1 Schnittdicke: 25 — 35 [¿m. Die Kontrolle auf Spezifität der Reaktion erfolgte a) durch Applikation 3 Stunden);

Autofluoreszierende Granula und Gefäßendothelien waren leicht an ihrer organge-gelben Fluoreszenzfarbe erkennbar.

von

Reserpin

(5 mg/kg,

i. p„

b) durch Weglassen der Glyoxylsäure-Gasbehandlung. Untersuchung der Schnitte nach Eindecken in Entellan® (MERCK) mit dem Fluoreszenzmikroskop FLUOVAL® ( V E B Carl Zeiss, Jena) bei Auflichtfluoreszenz unter Verwendung eines Kardioid-Kondensors. Erregerfilter: B G 12/4 g; Sperrfilter OG 1. Die Catecholaminfasern zeigten unter den angegebenen Bedingungen eine charakteristische blau-grüne Fluoreszenz. 1 Diese Arbeiten wurden am Biological Research Center der Ungarischen Akademie der Wissenschaften in Szeged ausgeführt. Für ständige freundliche Unterstützung sei besonders Dr. F. J o o , K . M O H A C Z I und Dr. I . T O T H gedankt.

1. Corticale Strukturen (Regio pyriformis, Übergangsgebiet an der Fissura rhinalis) nach Glyoxylsäure-Behandlung Der pyriforme Cortex zeigt im Fluoreszenzbild ein ausgeprägtes adrenerges Innervationsmuster (Abb. 1, 2). Die einzelnen Rindenschichten sind nicht gleichmäßig innerviert, vielmehr sind deutliche Unterschiede sowohl hinsichtlich der allgemeinen Innervationsdichte wie auch der speziellen Axonmorphologie sichtbar. Zumindest zwei differente Axontypen sind zu unterscheiden: a) Axone mit relativ dicken, knöpfförmigen, gleichmäßig angeordneten Varicositäten Axone dieses Typs sind in allen Schichten des Cortex darstellbar, sie steigen von den tiefen Anteilen in leicht kurvenförmigen Verläufen zur pialen Oberfläche auf, nehmen in den medialen Laminae eine häufig vertikale Richtung (Abb. 3a, c; 4a), um in den oberflächlichen Schichten (LI) mehr oder minder parallel zur Oberfläche zu verlaufen. Die Fasern

Adrenerge Innervation des Cortex pyriformis 103

Abb. 2. Catecholamin-Innervation des Cortex pyriformis (Fissura rhinalis) der Ratte. Tiefere corticale Schichten; überwiegend Dopamin-Fasern. Abb.-Maßstab: 380:1

dieses Typs haben ihre größte Dichte im Stratum moleculare. Zwischen den Varicositäten sind deutlich fluoreszierende intervaricöse Abschnitte erkennbar.

b) Axone mit relativ kleinen, rundlich bis oval erscheinenden, unregelmäßig angeordneten Varicositäten Für die Fasern dieses Typs ist charakteristisch, daß sie als Einzelfaser weniger deutlich darstellbar sind und in ihren Afferenzgebieten plexusartige Endverzweigungsmuster bilden. Sie durchsetzen die Laminae nicht gleichmäßig, sondern sind in der weitaus größten Dichte in den tieferen corticalen Schichten lokalisiert, während sie im Stratum moleculare nur in geringer Zahl vertreten sind (Abb. 2). Die Cortices der reserpinierten Tiere zeigten, von

104

Danner, H„ und C. Pfister

jEiagijf '

*

ir

*

Jf « „ SP - fL.


'

S

cO'

p

'

..

v

Pbm

(II)

* n,

Dorsal tegmental area located ventral and lateral to the periaqueductal gray matter

Subcoeruleus complex (SCC). The SCC (Fig. 8-9 ~10) extends from the level of LC to the "BARRINGTON nucleus". The SCC is composed of neurons which show strong MAO activity and of other neurons which do not show MAO activity. HRP injections into the spinal cord or cerebellum labeled, in the SCC, medium

Fig. 7. Dark-field photomicrograph of H R P positive neurons in the pbl and pbm following injection into the LH. x 100

to large sized and multipolar shaped neurons showing strong MAO activity (Fig. 6 a and b). In the case of cerebellum injections, several neurons which did not show MAO activity were also labeled in this area. Although HRP injection into the hypothalamus in this study failed to label MAO-positive neurons in the SCC and other pontine regions, these results should be "false-negative", since histofluorescence analysis clearly showed that these neurons also send their

172

Tohyama, M., K. Satoh, T. Sakumoto, Y. Kimoto, Y. Takahashi, K. Yamamoto and T. Itakura

Fig. 8 (1—4). Schematic representation of the organization and projections of the neurons in the dorsal tegmental area.

axons to innervate the hypothalamus FUXE,

1971;

OLSON

and

FUXE,

1972;

(OLSON MAEDA

and et

SHIMIZU, 1 9 7 2 ; SAKUMOTO e t a l „ 1 9 7 7 ) .

Reticular formation rostromedial to SCC (R). Injection of HRP into the spinal cord also gave evidence that neurons in the reticular formation (R) situated slightly rostromedial to the SCC also send their axons to the spinal cord. These neurons do not stain for MAO activity. Cell group I of Meessen and Olszewski. Cell group 1 of MEESSEN and OLSZEWSKI lies just ventrolateral to the fasciculus longitudinalis medialis at the level of the caudal pole of the nTD (Fig. 1-9). This nucleus is characterized by its densely arranged medium sized

cells. Following injection of HRP into the cerebellum, a large number of these cells were labeled. Nuclei parabrachialis lateralis (pbl) and medialis (pbm). Following injection of HRP into the medial part of the hypothalamus (POM and AH), a large number of labeled neurons were found in the pbl. This neuronal group is composed of small cells and extends from the rostral pole of the "BARRINGTON nucleus" to the caudal part of the decussation of the SCP (Fig. 7). These HRP labeled neurons fused rostrally with small sized HRP containing neurons situated just medial to the VM at the mid-point of the nVT. When HRP was injected into the POL or LH, on the other hand, a moderate number of HRP posi-

Dorsal tegmental area of the rat

tive neurons were found in the pbm at the level of the rostral pole of the "BARRINGTON nucleus". Furthermore injection of H R P into various hypothalamic areas resulted in labeling several mantle cells of the SCP at the caudal level of its decussation, while after injection of H R P into nts a cluster of labeled neurons occured in the nucleus reticularis pontis oralis just ventral to the SCP at the level of the caudal end of the nTV. This H R P labeled cell group contains mainly small cells. No H R P labeled neurons, however, were found in the pbl and pbm ( T A K A H A S H I et al., in preparation).

173

Organization and projection of the neurons in the dorsal tegmental area at the LC level are schematically drawn in Fig. 8. Discussion In the cytoarchitectonic study, cell bodies which show a characteristic arrangement are readily identified as a nucleus such as the LC, nRD, nTV, nTD, and VM in the dorsal tegmental area. In other parts of the dorsal tegmental area, however, cells are more loosely arranged so that the identification of any nucleus

174

Tohyama, M., K. Satoh, T. Sakumoto, Y. Kimoto, Y. Takahashi, K. Yamamoto and T. Itakura

group is difficult when based only upon the cytoarchitectonic characteristic of the nucleus. On this point, the present study indicates that the combination of retrograde tracer techniques, such as the HRP and histochemical techniques, such as MAO staining is a useful tool for this kind of investigation. The present study gives evidence that the dorsal tegmental area can be subdivided into various neuronal groups. We will mainly discuss some of these neuronal groups. The present findings indicate that a cluster of medium sized cells (which lies in the PGM lateral to the nRD and medial to the VM) (nucleus periaqueductus ventralis mesencephali (nPVM)) give rise to widespread ascending projections like the neurons of the LC and nRD. But it should be emphasized that this group of cells is composed exclusively of nonnoradrenergic neurons. The present study also provides evidence that the TLD can be subdivided into three components: TLDG, TLDP, and PB. Medium sized cells in the TLD (TLDG) (Figs. 1 and 8), which lies just rostromedial to the LC, innervates monosynaptically the cerebral cortex, hypothalamus and the PT (Fig. 8-4 ~6). On the other hand, small sized cells in the TLD (TLDP) innervate mainly the AH, while neurons in the peri-BARRINGTON area (PB) innervate mainly the LH (Fig. 8-4 ~8). It should be noted that the LC and SC (which contain NA), and the PVM and "BARRINGTON nucleus" (which do not contain NA) both innervate the spinal cord. It should be also noted that the neurons in the SC are composed of NA and non-NA neurons, and both types of neurons have a similar projection pattern. In the present study, neurons of the "BARRINGTON nucleus" were intensively labeled by the HRP when the animals were pretreated by 6-hydroxydopa. The "BARRINGTON nucleus" was first described b y BARRINGTON (1925) i n t h e c a t a s t h e ' p o n t i n e m i c -

turition reflex center', since the bilateral destruction at the dorsal tegmental area of the cat resulted in an urinary retention. Many subsequent electrophysiological and morphological studies concerning the central control of micturition have been reported (BORS a n d KOMMAR, 1 9 7 1 ; KURU, 1 9 6 5 ; LANGWORTHY e t al., 1 9 4 0 ; ROUSSEL e t al., 1976), b u t p r e c i s e locali-

zation of this nucleus remained to be determined. Recently SATOH identified the "BARRINGTON nucleus" in the TLD by lesion experiments in the rat (1976). In this study we have demonstrated the monosynaptic fiber connections to the spinal cord from this nucleus as well as from the LC. It is of great interest to note that the amount of HRP transported through the axons to the perikaryon of this nucleus remarkably increased by pretreatment of 6-hydroxy-

dopa. This observation might indicate that central NA systems also share in the control of the micturition reflex, but that the main control of this function is played by "BARRINGTON nucleus" which does not contain NA. Possible interactions between NA and non-NA neuronal system have been suggested previously (JOUVET, 1972). The present findings together with some previous electromicroscopic studies (KODA and BLOOM, 1 9 7 7 ; ITAKURA et al., 1 9 7 7 ; MAEDA et al., in press; SAKUMOTO et al., 1977) are also in favor of possible interactions among different neurotransmitter systems. This paper is dedicated to Prof. Nobuo SHIMIZU, who retired from the Osaka University Medical School on May 31, 1976.

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coeruleus noradrenaline neuron: The cerebellar innervation. Brain Research 28, 1 6 5 - 1 8 1 (1971). OLSON, L . , and K . F U X E : Further mapping out of central noradrenaline neuron system: Projections of the "subcoeruleus" area. Brain Research 43, 289 — 295 (1972). O N G , H., C. R. C R E V E L I N G and J . D A R Y : The synthesis of 2,4,5-trihydroxy-phenylalamin(6 hydroxydopa). A centrally active norepinephrine deeping agent. J . med. Chem. 12, 4 5 8 - 4 6 1 (1969). R O U S S E L , B., J . F. P U J O R , et M. J O U V E T : Effects des lesion du tegmentum ponti pontique sur les etats de sommeil chez le rat. Arch. ital. Biol. 114, 1 8 8 - 2 0 9 (1976). R O U S S Y , G . , et M . M O S I N G E R : Traite de neuroendocrinologie. Manson (1946). S A C H S , CH., and J . J O N S S O N : Selective 6-hydroxydopa induced degeneration of central and peripheral noradrenaline neurons. Brain Research 40, 563 — 568 (1972). S A C H S , C H . , G . J O N S S O N and K . F U X E : Mapping of central noradrenaline pathways with 6-hydroxydopa. Brain Research 63, 2 4 9 - 2 6 1 (1973).

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and

Afferent fiber connections from lower brain stem with special reference to noradrenergic neuron system. J . Hirnforsch. 1 9 , 8 5 - 1 0 0 (1978). K I V I E T , J . , and H. G. J . M. K U Y P E R S : Subcortical afferents to frontal lobe in the rhesus monkey studied by means of retrograde horseradish peroxidase transport. Brain Research 85, 2 6 1 - 2 6 6 (1975). K O D A , L. Y., and F. E. B L O O M : A light and electron microscopic study of noradrenergic terminals in the rat dentate gyrus. Brain Research 120, 3 2 7 - 3 3 5 (1977). L A N G W O R T H Y , O. R., L . C. K O L B and L . G. L E W I S : Physiology of micturition. Baltimore, (1940). N . SHIMIZU:

LEGER, L.,

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A. KASHIBA,

M . TOHYAMA,

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T . ITA-

and N . S H I M I Z U : Aminergic terminals and their contacts demonstrated by in situ fixation of endogeneous monoamine with potassium permanganate. Brain Research in press. KURA

MAEDA, T . , C. PIN, D . SALVERT, M . LIGIER a n d M .

JOUVET:

Les neurones contenant des catecholamine du tegmentum pontique et leur voies de projection chez le chat. Brain Research 57, 1 1 9 - 1 5 2 (1973). M A E D A , T . , et N . S H I M I Z U : Projection ascendante du locus coeruleus et d'autres neurones aminergiques au niveau du prosencephale du rat. Brain Research 36, 19 — 35 (1972). M E E S S E N , H., and J . O L S Z E W K I : " A cytoarchitectonic atlas of the rhombencephalon of the rabbit. Karger, Basel. (1948). M O R I N , F . : An experimental studies of the hypothalamic connections in the guinea pig. J . Domp. Neurol. 92, 91 bis 115 (1950). O L S O N , L . , and K . F U X E : On the projection from the locus

D . SALVERT, L . L E G E R a n d M .

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VET: Afferent projections to the cat locus coeruleus as visualized by the horseradish peroxidase technique. Brain Research 120, 1 - 2 1 (1976).

SAKUMOTO, T . ,

M . TOHYAMA,

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T . ITAKURA,

T.

KINUGASA, T . TANIZAWA, K . YAMAMOTO, K . KURACHI a n d

N. S H I M I Z U : Fine structure of noradrenaline terminals in the inner layer of the median eminence of the rat. J . Hirnforsch., in press. SAKUMOTO, T . ,

M . TOHYAMA,

K . SATOH

and

N . SHIMIZU:

Afferent fiber connections from lower brain stem to hypothalamus with special reference to noradrenaline neuron system. Exp. Brain Res. 30 (1977) in press. S A T O H , K . : Experimental morphological studies on the micturition reflex center in the pontine tegmentum in the rat. Brain and nerve 29, 63 — 71 (1976). (in japanese). SATOH, K . , M . TOHYAMA,

K . YAMAMOTO, T . SAKUMOTO

and

N. S H I M I Z U : Noradrenaline innervation of the spinal cord by the horseradish peroxidase method combined with monoamine oxidasej staining.® E x p . J Brain Res. 30, 1 7 5 - 1 8 6 (1977). S H I M I Z U , N., N. M O R I K A W A and K. O K A D A : Histochemical studies of monoamine oxidase of the brain of rodents. Z. Zellforsch. 49, 3 8 9 - 4 0 0 (1959). SHIMIZU, N . ,

S. OHNISHI,

M . TOHYAMA

and

T . MAEDA :

SHIMIZU, N . ,

S . OHNISHI,

M . TOHYAMA

and

T. MAEDA:

Demonstration of ascending projection from locus coeruleus by degeneration silver method. Exp. Brain Res. 20, 1 8 1 - 1 9 2 (1974).

Demonstration of ascending projection of amine neurons in the brain stem by degeneration silver method. 10th Int. Cond. Anat. (Abstract) 135 (1975). SHIMIZU, N.: Morphology of locus coeruleus. From the memorial book of the retirement of Prof. SHIMIZU from Osaka Univ. Med. School 1977, in japanese. T A B E R , T . : The cytoarchitecture of the brain stem of the cat. I Brain stem nuclei of the cat. J . Comp. Neurol. 116, 1 6 1 - 1 8 7 (1961). T O H Y A M A , M.: Comparative anatomy of the cerebellar catecholamine innervation from teleosts to mammals. J . Hirnforsch. 17, 4 3 - 6 0 (1976). TOHYAMA, M . ,

T . MAEDA,

A. KASHIBA

and

N . SHIMIZU:

Fluorescence and electron microscopic analysis of axonal change of coerulo-cortical noradrenaline neuron system following destruction of locus coeruleus and administra-

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tion og 6-hydroxydopa. Med. J . Osaka Univ. 24, 205 bis 221 (1974). T O H Y A M A , M., T. M A E D A and N. S H I M I Z U : Detailed noradrenaline pathways of locus coeruleus neuron to the cerebral cortex with use of 6-hydroxydopa. Brain Research 79, 1 3 9 - 1 4 4 (1974). TOHYAMA, M . ,

K . SATOH,

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Possible interaction between noradrenergic and nonnoradrenergic neuron system. Acta Anat. nippon., (Abstract), in Japanese, in press. U N G E R S T E D T , U . : Stereotaxic mappings of the monoamine pathways in the r a t brain. Acta Physiol. Scan., Suppl. 367, 1 - 4 8 (1971).

: Reticular formation of the pons and medulla oblongata. A golgi study. J . Comp. Neurol. 116, 71 — 99 (1961).

VALVERDE, F .

Address: D r . M . TOHYAMA

Department of Neuroanatomy Institute of Higher Nervous Activity Osaka University Medical School 3 - 5 7 Nakanoshima 4 chome Kitaku Osaka 530 Japan

J . Hirnforsch. 19 (1978) 177-187

Paul-Flechsig-Institute of Brain Research, Department of Neuroanatomy, Karl-Marx-University Leipzig, German Democratic Republic (Head: Prof. Dr. sc. med. E . W I N K E L M A N N )

Phylogenetical changes and functional specializations in the dorsal lateral geniculate nucleus (dLGN) of mammals1-2-3 By Kurt

BRAUER,

Wilfried

SCHOBER

and Ernst

WINKELMANN

With 16 figurs (Received 2 nd August 1977) Summary: Depending on their visual specialization and their place in the zoological system the mammalian species show some peculiarities in the morphology of the dorsal lateral geniculate nucleus (dLGN). The lamination of dLGN can be find in mammals with a highly developed visual system and a proportionally big part of ipsilaterally projecting retinogeniculate fibres. Number and sequence of ipsi- and contralaterally innervated laminae varies between species of different taxonomical categories. Hence these features depend on phylogenetical trends which could be traced back to the beginning of the "mammalian radiation" in the cretaceous period and the earliest tertiary. Ancestral conditions may be found in mammals with an unlaminated dLGN and a medially located ipsilaterally innervated part. I t may be registrated that a cytoarchitectonical separation of laminae (concerning the ipsi- and contralateral innervation) is the secondary step after fibre anatomical separation. The most primitive status may be realized in mammals having a zone of mixed ipsi- and contralateral fibre input. Some conclusions are made with regard to the suitability of lab mammals for generalization of results in the dLGN morphology. Zusammenfassung: In Abhängigkeit von ihrer visuellen Spezialisation und ihrem Platz im zoologischen System weisen die Säugetierarten einige Besonderheiten im Bau des dorsalen Kerns des Corpus geniculatum laterale (dLGN) auf. Eine Laminierung des dLGN wird bei Säugern mit einem hoch entwickelten visuellen System und einem vergleichsweise großen Anteil ipsilateral projizierender retinogeniculärer Fasern angetroffen. Anzahl und Reihenfolge ipsi- und contralateral innervierter Laminae variieren zwischen Species, die unterschiedlichen taxonomischen Kategorien angehören. Daraus folgt, daß diese Merkmale von phylogenetischen Trends abhängig sind, welche bis zum Beginn der "Säuger-Radiation" in der Kreidezeit und dem frühesten Tertiär zurückverfolgt werden könnten. Ancestrale Bedingungen zeigen möglicherweise Säugetiere mit einem unlaminierten dLGN und einem medial lokalisierten ipsilateral innervierten Anteil. Es kann festgestellt werden, daß die cytoarchitektonische Abgrenzung der Laminae als sekundärer Schritt der faseranatomischen — in bezug auf die ipsi- und contralaterale Innervierung — folgt. Das primitivste Stadium wird bei Säugetieren anzutreffen sein, bei denen eine Zone gemischten ipsi- und contralateralen Inputs existiert. Es wurden einige Schlußfolgerungen über die Eignung von Labortieren für eine Verallgemeinerung von morphologischen Befunden am dLGN gezogen.

Introduction Numerous comparative investigations concerning the mammalian dorsal lateral geniculate nucleus (dLGN) indicate so much differences in morphological characteristic properties rarely to observe in any other subcortical structure. There axe not only considerable size differences in the dLGN of various species, but also specific peculiarities in its histological structure about which a lot of literature has been published. These findings are based in the first line on Nissl1 Sponsored by a grant of the Ministry of Science and Technology of the GDR 2 Prof. Dr. J. Szentdgothai dedicated with the best wishes to the 65. birthday 3 The authors wish to thank Mrs. M A T T H E S and Dr. B I G L for critical reading the english text.

and fibre-preparations. Investigators utilize as most important characteristics size and shape of nerve cell somata, the presence or absence of their laminar arrangement as well as especially during the last years — the demonstration of an ipsi — or contralateral afferentiation for characterizing the laminae or for the proof of lamination if the latter cannot be vizualized by the Nissl-method. Comparing the dLGN structure in various orders or species it may be of importance to ask for the causes of these striking differences. We will try to find some references or answers in this paper and by the way to the usefulness of some lab mammals for experiments concerning the visual system, too. dLGN structure of various mammals The following review of the most important characteristics will include only placental mammals since —

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on the one hand — the homologies of the "LGNa" and "LGNb" of Monotremata are not completly settled (CAMPBELL and HAYHOW 1 9 7 1 ) and — on the other — the Marsupialia investigated until now show relations which are mainly in accordance with those of basal and speciallized placental mammals (HAYHOW, 1 9 6 7 , CAMPBELL 1 9 7 2 ) .

A detailed investigation of the homologous structures of the dLGN in other vertebrates is available by EBBESSON ( 1 9 7 2 ) .

Insectívora (fig. 1, 2) This order includes numerous olfactory orientating species with highly reduced visual system but also species, where the eye is developed rather good. But there are also a few tree-living forms with a good organized visual system. While we do not have any results on moles and shrews representing insectivores with poor developed visual apparatus, the dLGN of hedgehog (Erinaceus europaeus) a species having a better developed visual system has been investigated (fig. 1). No cytoarchitectonic lamination could be observed. After enucleation the medial and dorsal sections of the ipsilateral dLGN show a sharply outlined islelike area with degenerating terminals. These areas are degeneration-free on the contralateral side (CAMPBELL 1 9 7 2 ) . This fact can be considered as primitive stage of a beginning lamination which was already concluded from fibre-anatomical studies but could not yet be shown cytoarchitectonically (CAMPBELL 1 9 7 2 ) .

One of the insectivores with highly developed visual system is the tree-shrew (Tupaia) (fig. 2). In the dLGN six laminae may be detected cytoarchitectonically as well as after degeneration of retinal fibres (GLICKSTEIN 1 9 6 2 , CAMPBELL 1 9 7 2 , HUBEL 1 9 7 5 ) . According to the widely accepted enumeration of laminae from lateral to medial, used for the laminated dLGN, the laminae 1, 3, 4 and 5 receive a contralateral input and only laminae 2 and 6 an ipsilateral one. According to H U B E L (1975) there are differences in the projection of these laminae onto different cortical layers. Chiroptera (fig. 3, 4) Our material as well as the investigations of PENTNEY and COTTER ( 1 9 7 6 ) show that the dLGN of bats who orientate primarily acoustically is well developed. Nevertheless it does not show any lamination or a subdivision in different cell regions (fig. 3). Regarding the termination zone of ipsilateral fibres no studies are available. Unfortunately, no results for the Macrochiroptera who orientate mainly optically are published in lite-

rature. After analyzing own preparations we can now say there may exist cytoarchitectonically a lamination in the dLGN (fig. 4). Primates (fig. 5, 6, 7, 8) Members of this order dispose of laminated dLGN. The lamination is already visible cytoarchitectonically. Regarding the number of laminae of various species opinions are partly contradictory. HASSLER ( 1 9 6 7 ) described four laminae at Callithrix, Aotes, Saimiri and Tarsius, but at prosimians he found six (fig. 5). JONES (1966) who investigated Aotes, agrees with HASSLER (fig. 6). Contrary to HASSLER, CAMPOSORTEGA and HAYHOW (1970) as well as TIGGES and TIGGES ( 1 9 7 0 ) indicate a seventh lamina at Galago, a prosimian. At Cebus and Macaca also seven, at Papio even nine laminae are distinguished (CAMPOSORTEGA a n d HAYHOW 1 9 7 0 ) . CAMPBELL ( 1 9 7 2 ) des-

cribes in Saimiri a seventh lamina too (0), but he found six at the prosimian Nycticebus. At Galago and Nycticebus it is unanimously stated that laminae 2, 3 and 4 get input from ipsilateral, laminae 1, 5 and 6 from contralateral retina (CAMPOSORTEGA a n d HAYHOW 1 9 7 0 , CAMPBELL 1 9 7 2 , TIGGES a n d TIGGES 1 9 7 0 ) .

According to JONES ( 1 9 6 6 ) the two inner laminae contrary to the dorsal and ventral adjacent outer laminae of Aotes are innervated ipsilaterally. CAMPOS-ORTEGA and GLEES ( 1 9 6 7 ) as well as CAMPBELL ( 1 9 7 2 ) described in Saimiri 6 laminae after fibredegeneration whereas cytoarchitectonically only 4 laminae can be distinguished. WONG-RILEY ( 1 9 7 2 ) and TIGGES and O'STEEN ( 1 9 7 4 ) also indicate six laminae for Saimiri and mention that the distribution of optic fibres is the same as in rhesus monkeys and men, i.e. the laminae 1, 4 and 6 are contralaterally innervated, laminae 2, 3 and 5 ipsilaterally. Compared with that Hylobates, a pongide-like species, has only 4 laminae (KANAGASUNTHERAM and KRISHNAMURTI

Fig. 1. Erinaceus europaeus (hedgehog); left LGN; coronal section, Cresylviolet and Luxol-fast-blue stained, x 50; dLGN = dorsal lateral geniculate nucleus; vLGN = ventral lateral geniculate nucleus. Fig. 2. Tupaia glis (tree shrew); left LGN; coronal section, Cresylviolet and Luxol-fast-blue stained, x 50; 1 — 6 = laminae 1 — 6 of dLGN. Fig. 3. Artibeus jamaicensis (fruit-vampire); left dLGN, coronal section, Cresylviolet stained, x 30. Fig. 4. Pteropus giganteus (flying fox); left LGN, coronal section, Cresylviolet stained, x 50; 1 — 3 = laminae 1 — 3 of dLGN.

The dorsal lateral geniculate nucleus of mammals

Fig. 1 - 4

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Fig. 5. Galago crassicaudatus (giant galago); left dLGN, coronal section, Cresylviolet and Luxol-fast-blue, x 25; 1 - 6 = laminae 1 — 6 of the dLGN. Fig. 6. Aotes trivirgatus (owl monkey), left dLGN, coronal section, Cresylviolet and Luxol-fast-blue; x 25; 1 — 4 = laminae 1 — 4 of the dLGN. Fig. 7. Macaca mulatta (rhesus monkey), left dLGN, coronal section, Cresylviolet and Luxol-fast-blue; x 25; 1 — 6 = laminae 1 — 6 of the dLGN Fig. 8. Pan troglodytes (chimpanzee), left dLGN coronal section; x 25; 1 —6 = laminae 1 — 6 of the dLGN.

1970). Detailed investigations in the projection of the dLGN to the visual cortex of the rhesus monkey showed that the individual laminae project on differ e n t s u b l a y e r s of l a y e r I V (HUBEL a n d WIESEL 1972).

KAAS et al. (1972) suggest that all primates except the prosimians dispose of 4 laminae only, of which especially the parvocellular but in some cases also the magnocellular laminae form so-called "leaflets". The latter, however, do not correspond to true laminae. These authors take into consideration that also the prosimians — as well as other primates — ascend from ancestors with 4 laminae. The supply of the "central" laminae with ipsilateral retinal input points to a possible relationship to basal insectivores (Erinaceus). Lagomorpha (fig. 9, 10) The hare-like animals are mammals with well developed visual apparatus. For that reason the dLGN occupies a relatively greater volume as, for instance,

The dorsal lateral geniculate nucleus of mammals

18Í

Fig. 9. Oryctolagus cuniculus (rabbit), left LGN, coronal in most of the myomorphic rodents. ROSE (1935) action, Cresylviolet and Luxol-fast-blue, x 25; ex., ß = sub- did not indicate any lamination in the rabbits dLGN nuclei a and ß of the dLGN.

but discriminated four "subnuclei" (