Intrinsic Neuronal Organization of the Vestibular Nuclear Complex in the cat: A Golgi study

106 Pages·1968·4.423 MB·English

by  Eivinn Hauglie-Hanssen (auth.)

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Prof. Dr. A. BRODAL, Universitetet i Oslo, Anatomisk Institutt, Karl Johans Gate 47
(Domus Media), Oslo 1/Norwegen.
Prof. W. HILD, Department of Anatomy, The University of Texas Medical Branch,
Galveston, Texas 77550 (USA).
Prof. Dr. R. ORTMANN, Anatomisches Institut der Universitat, 5 Koln-Lindenthal,
Lindenb urg.
Prof. Dr. T. H. SOHIEBLER, Anatomisches Institut der Universitat, KoellikerstraBe 6,
87 Wiirzburg.
Prof. Dr. G. Ti:iNDURY, Direktion der Anatomie, GloriastraBe 19, CH-8006 Ziirich.
Prof. Dr. E. WoLFF, College de France, Laboratoire d'Embryologie Experimentale,
49 his Avenue de la belle Gabrielle, Nogent-sur-Mame 94/France.
Ergebnisse der Anatomie und Entwicklungsgeschichte
Advances in Anatomy, Embryology and Cell Biology
Revues d 'anatomie et de morphologie experimentale
40.5
Editores
A. Brodal, Oslo · W. Hild, Galveston · R. Ortmann, Koln
T. H. Schiebler, Wilrzburg · G. Tondury, Zurich · E. Wolff, Paris
Eivinn Hauglie-Hanssen
Intrinsic Neuronal Organization
of the Vestibular Nuclear Complex
in the Cat
A Golgi Study
With 46 Figures
Springer-Verlag Berlin Heidelberg GmbH 1968
Eivinn Hauglie-Hamsen, Anatomical Imtitute, University of Oslo
Karl Joham gt. 47, Oslo 1, Norway
ISBN 978-3-662-23469-3 ISBN 978-3-662-25528-5 (eBook)
DOI 10.1007/978-3-662-25528-5
Alle Rechte vorbehalten. Kein Tell dleses Buches darf ohne schrlftliche Genehmigung des Springer-Verlages
Springer-Verlag Berlin Heidelberg GmbH.
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© by Springer-Verlag Berlin Heidelberg 1968. Library of Congress Catalog Card Number 64-20582
Originally published by Springer-Verlag in 1968
Titel-Nr. 6958.
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auch ohne besondere Kennzeichnung nicht zu der Annahme, dall solche Namen im Sinne der Warenzeichen-und
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Contents
I. Introduction . . . . 7
II. Material and Methods 11
1. Golgi Preparations 11
2. Material of Reference 12
III. Observations . . . . . 13
1. The Vestibular Nuclear Complex as seen in Thionine Stained (Nissl)
and Silver Impregnated Sections (Bodian) . . . . . . . . . 13
2. The Vestibular Nuclear Complex as seen in Golgi Preparations 20
A. Nerve Cells in the Vestibular Nuclear Complex . 20
a) The Lateral Vestibular Nucleus . 27
b) The Superior Vestibular Nucleus . . 33
c) The Medial Vestibular Nucleus. . . 35
d) The Descending Vestibular Nucleus. 36
e) The Interstitial Nucleus of the Vestibular Nerve 40
f) The Group x . 41
g) The Group z . . . . . . . . . . . 41
h) The Group y. . . . . . . . . . . 42
B. Branching Patterns of Afferent Fibres. 42
a) Primary Vestibular Fibres . 45
b) Cere bello-vestibular Fibres. . . . . 50
Hook Bundle . . . . . . . . . . 51
Ipsilateral Cerebella-vestibular Fibres. 54
c) Spina-vestibular Fibres . . . . . . . 55
d) Reticula-vestibular Fibres . . . . . . 57
e) Descending Fibres from Higher Levels of the Brain . 58
C. Axon Terminals and Interneuronal Contacts 59
a) Axo-somatic Contacts. . . . 61
b) Axo-dendro-somatic Contacts 65
c) Axo-dendritic Contacts . . . 69
IV. Discussion . . . . . . . . . . . . 69
1. Comments on Material and Methods . 69
2. Delimitation and Subdivision of the Vestibular Nuclear Complex 71
3. Intrinsic Organization of the Vestibular Nuclear Complex 73
a) Neuronal Architecture . . . . . . . . . . . . . . . 73
b) Aspects of Dendritic and Axonal Distribution . . . . . 75
c) Distribution and Branching Patterns of Afferent Fibres . 80
d) Terminal Fibres and Interneuronal Contacts. . . . . . 87
6 Abbreviations
V. Summary and Conclusions. 95
References . . 97
Subject Index . . . . . . . . 103
Abbreviations
B.c., Br.c. Brachium conjunctivum (Superior cerebellar peduncle)
Ger. Cerebellum
O.r. Restiform body (Inferior cerebellar peduncle)
D Descending (inferior) vestibular nucleus
d.ac.s. Dorsal acoustic stria
I Cell group f in the descending vestibular nucleus
F Fastigial nucleus
F.l.m. Medial longitudinal fasciculus
Flocc. Flocculus
g Group rich in glia cells, caudal to the medial vestibular nucleus
H.b. Hook bundle of Russell (Uncinate fascicle)
i.e. Nucleus intercalatus (Staderini)
L Lateral vestibular nucleus (of Deiters)
l Lateral group (middle-sized cells) of lateral vestibular nucleus
Li Lingula of the cerebellum
M Medial vestibular nucleus
N.c. Cochlear nuclei
N.c.d. Dorsal cochlear nucleus
N.c.v. Ventral cochlear nucleus
N.cu.e. External (accessory) cuneate nucleus
N.f.c. Cuneate nucleus
N.j.g. Gracile nucleus
N.i. Nucleus interpositus cerebelli
N.i.n. VIII Interstitial nucleus of vestibular nerve
N.m.X,X Dorsal motor (parasympathetic) nucleus of vagus
N.m.XII, XII Motor nucleus of hypoglossal nerve
N.mea. V Mesencephalic nucleus of trigeminal nerve
N.pr. V, V Principal sensory nucleus of trigeminal nerve
N.pr.h., p.h. Nucleus praepositus hypoglossi
N.tr.s. Nucleus of solitary tract
N.tr.sp. V Nucleus of spinal tract of trigeminal nerve
N. V, VII, VIII, IX Cranial nerves V, VII, VIII, IX
Ol.i. Inferior olive
Ol.s. Superior olive
Ret. Reticular formation
s Superior vestibular nucleus (of Bechterew)
Sv Supravestibular nucleus
Tr.s. Solitary tract
Tr.sp. V, Tr.sp.n. V. Spinal tract of trigeminal nerve
Ventr.IV Fourth ventricle
X Cell group lateral to the descending vestibular nucleus
y Cell group dorsal to the restiform body
z Cell group dorsal to the caudal part of the descending vestibular
nucleus
"I know well that in the realm of science
that which is obstinately looked for is
usually found; but when that which is not
looked for establishes a frequent distri
bution and appears in all clearness it
finally arouses the attention which was
most distracted and most preoccupied
with other problems." - SANTIAGO
RAMON Y CAJAL (Neuron Theory or Reti
cular Theory? Madrid 1954, p. 98).
I. Introduction
Nervous impulses from the vestibular receptors have profound and widespread
influences on body functions. Since any signal from the vestibular labyrinths is
transmitted to the vestibular nuclei, these hold a strategic position among those
structures which are related to vestibular function. The vestibular nuclei are
supplied by nerve fibres from numerous other sources as well, including the
cerebellum, higher levels of the brain stem, and the spinal cord. Integration of
nervous impulses must therefore be assumed to take place within their territories.
However, the anatomical basis of these integrative processes is still insufficiently
known.
According to recent analyses of the organization of the vestibular nuclear
complex (see BRODAL, PoMPEIANO and WALBERG, 1962), various cell groups can
be distinguished, differing in their cytoarchitecture as well as in their fibre connec
tions, and probably representing more or less specific functional units. Most
authors have subdivided the vestibular complex into four major nuclei: the
superior (angular nucleus, nucleus of Bechterew), the lateral (nucleus of Deiters),
the medial (dorsal vestibular nucleus of Schwalbe), and the descending (spinal
nucleus, inferior nucleus) vestibular nuclei. BRODAL and PoMPEIANO (1957 a) in a
study of the normal cytoarchitecture and topography of the vestibular nuclei in
the cat, in addition to the four classical nuclei, distinguished some small cell groups
closely related to the former (f, l, x, y, z, g, nucleus supravestibularis, and the
interstitial nucleus of the vestibular nerve of Cajal). Within the four main nuclei
regional differences in size and shape of the nerve cells were noted.
Investigations on the fibre connections of the vestibular nuclear complex have
warranted a subdivision even more specific than is obtained on the basis of cyto
architectonic studies only. The various contingents of efferent fibres from the
vestibular complex arise from more or less restricted parts which do not always
coincide with those deliminated on the basis of cytoarchitecture. The vestibulo
spinal tract takes origin exclusively from nerve cells in the lateral nucleus (PoM
PEIANO and BRODAL, 1957 a). Fibres in the medial longitudinal fasciculus, descend
ing from the vestibular complex, arise in the medial vestibular nucleus (see
NYBERG-HANSEN, 1964) and apparently also in the descending nucleus (see PoM
PEIANO and BRODAL, 1957 a, for a review of the literature; WILSON, WYLIE and
8 E. IIAUGLIE-HANSSEN:
MARco, 1967). Fibres projecting to the cerebellum (secondary vestibulo-cerebellar
fibres) originate largely in certain regions of the descending nucleus and the group x
(BRODAL and ToRVIK, 1957). Fibres ascending in the brain stem appear to arise
from all four vestibular nuclei as well as from the cell group x and the interstitial
nucleus of the vestibular nerve (BRODAL and PoMPEIANO, 1957b). There are,
furthermore, fibres from the vestibular nuclei to the reticular formation (CAJAL,
1896, 1909; HELD, 1923; LoRENTE DE N6, 1933b; ScHEIBEL and ScHEIBEL, 1958;
LADPLI and BRODAL, 1968), and fibres passing in a centrifugal direction in the
vestibular nerve (LEIDLER, 1914; PETROFF, 1955; RASMUSSEN and GACEK, 1958;
GACEK, 1960; Rossr and CoRTESINA, 1962), but information on the sites of origin
of these fibres is sparse.
The various contingents of afferent fibres to the vestibular complex do not end
diffusely all over the complex, but have their particular sites of termination.
Although the primary vestibular fibres reach all four vestibular nuclei, there are
in all of them certain regions which are free from vestibular afferents (WALBERG,
BowSHER and BRODAL, 1958). It appears, furthermore, from an analysis of
LORENTO DE N6's (1926, 1931, 1933a) findings in a Golgi study in mice (see
BRODAL, PoMPEIANO and WALBERG, 1962) that fibres from the utricle, the saccule,
and the semicircular ducts end to some extent in different subdivisions of the
vestibular complex (see also STEIN and CARPENTER, 1967). Spino-vestibular fibres
terminate in restricted parts of the descending and medial nuclei and in the dorsa
caudal parts of the lateral nucleus (PoMPEIANO and BRODAL, 1957 b; BRODAL and
ANGAUT, 1967). Cortical (vermal) cerebello-vestibular fibres terminate largely in
the dorsal parts of the lateral and descending nuclei (WALBERG and JANSEN, 1961).
A differentiated pattern of termination of vestibular afferents from the flocculo
nodular lobe and the uvula has recently been demonstrated (ANGAUT and BRODAL,
1967). Fibres from the fastigial nuclei to the vestibular complex are crossed and
uncrossed; the former contingent, originating in the caudal part of the contra
lateral fastigial nucleus, end mainly in the ventrolateral parts of the lateral and
the descending nuclei; the latter contingent, arising in the rostral part of the
ipsilateral fastigial nucleus, terminates largely in those parts of the vestibular
complex not supplied by the former (WALBERG, POMPEIANO, BRODAL and JANSEN,
1962).
Evidence is established of a somatotopical organization of the pathways from
the cerebellar vermal cortex and the fastigial nuclei, via the lateral vestibular
nucleus to the spinal cord (see BRODAL, PoMPEIANO and WALBERG, 1962). PoM
PEIANO and BRODAL (1957 a) demonstrated anatomically within the lateral
nucleus a "neck and forelimb region", a "trunk region", and a "hindlimb region".
This topography was confirmed in physiological experiments by PoMPEIANO (1960)
and in degeneration studies following lesions of the nucleus by NYBERG-HANSEN
and MAsciTTI (1964). In physiological studies employing microelectrode tech
niques the somatotopical organization has also been confirmed (ITo, HoNGO,
YosHIDA, OKADA and 0BATA, 1964; WILSON, KATo, PETERSON and WYLIE, 1967).
A satisfactory understanding of the anatomical and functional organization of
the vestibular nuclear complex demands knowledge not only concerning its cyto
architecture and fibre connections with other aieas. Information on possible mutual
interconnections by means of dendrites or axons between the various subdivisions
Vestibular Nuclear Organization 9
of the complex is indispensable, since integration of various afferent impulses is
presumably a main function of this nuclear complex. The presence in the vestibular
nuclei of cells with long and radiating dendrites has been demonstrated in Golgi
material by several authors {CAJAL, 1896, 1909; LORENTE DE N6, 1927; MANNEN,
1965; ZHUKOVA, 1965). CAJ.AL, in mice, found nerve cells in the lateral nucleus
with long dendrites extending into the medial and the descending vestibular nuclei.
MANNEN {1965) described, in kittens, dendrites extending beyond the borders of
all the vestibular nuclei. LORENTO DE N6 {1933b) demonstrated, in mice, cells
with branching axons within various nuclei of the vestibular complex. However,
no detailed mapping has been made by these authors of the dendritic and axonal
distribution within the various parts of the vestibular complex. Furthermore, no
correlation has been made between such distributions and recent observations
concerning the restricted terminal areas in the vestibular complex of its afferent
fibre contingents.
The structural differentiation of the vestibular receptor cells and the spatial
distribution and orientation of different types of these cells within the sensory
epithelia {see SPOENDLIN, 1964; WERSALL and LUNDQUIST, 1966; ENGSTROM,
LINDEMAN and ADES, 1966) suggest that a specificity is maintained in the central
vestibular connections as well, as do also the effects of stimulation of vestibular
receptors. In view of such a possible specificity, the mode of branching and
distribution within the vestibular complex of the individual afferent fibres in the
various afferent contingents is deemed to be of considerable interest. The branching
pattern of the primary vestibular fibres demonstrated in previous Golgi studies
{CAJ.AL, 1896, 1909; LORENTE DE N6, 1933a) indicates transmission of nervous
impulses by each one of these fibres to cells widely scattered in different parts of
the vestibular complex. Few details, however, are reported concerning the branch
ing patterns of individual fibres belonging to other afferent contingents to the
vestibular complex.
The employment of refined electrophysiological techniques in the studies of
nerve cell interaction, has stimulated the interest in the morphology of synaptic
interrelations. A scrutiny of the literature, however, reveals only sparse information
concerning the finer anatomy of the interneuronal contacts in the vestibular
nuclei. In a Golgi material from kittens, newborn and a few days old, CAJAL
{1896, 1909) described and illustrated cells in the lateral vestibular nucleus sur
rounded by a dense plexus of fine nerve fibres almost forming baskets around the
perikarya, and he especially pointed to the abundance of fine fibres along the cell
processes. Furthermore, CAJ.AL noted that the individual fibres in the pericellular
networks had numerous short and strongly varicose branches, each with a small
terminal thickening closely attached to the surface of the cell. Experimental
anatomical studies of afferent fibres to the vestibular complex {see BRODAL,
PoMPEIANO and W .ALBERG, 1962) have produced evidence of contacts by means of
boutons in all the regions studied. Contacts were, in general, observed on perikarya
as well as on dendrites. Furthermore, these studies suggest that fibres belonging to
different contingents of afferents may end on cells of different sizes.
From the account given above it will be evident that there is a demand for
further knowledge of many aspects of the minute anatomy of the vestibular
nuclear complex. The regional differences in cytoarchitecture, as well as in fibre