Connections and oculomotor projections of the superior vestibular nucleus and cell group ‘y’

Attempts were made to determine brainstem and cerebellar afferent and efferent projections of the superior vestibular nucleus (SVN) and cell group 'y' ('y') in the cat using axoplasmic tracers. Injections of HRP, WGA-HRP and [3H]amino acids were made into SVN and 'y' using two different infratentorial stereotaxic approaches. Controls were provided by unilateral HRP injections involving the oculomotor nuclear complex (OMC), the interstitial nucleus of Cajal (INC) and the deep cerebellar nuclei (DCN). Large injections of SVN almost invariably involved 'y' and dorsal parts of the lateral vestibular nucleus (LVN). Smaller injections involved central and ventral peripheral parts of SVN. Discrete injections of 'y' involved small dorsal parts of LVN. Afferents to SVN are derived mainly from the vestibular nuclei (VN) and parts of the vestibulocerebellum. SVN receives afferents: bilaterally from caudal portions of the medial (MVN) and inferior (IVN) vestibular nuclei and 'y'; contralaterally from ventral and lateral parts of SVN and rostral MVN; and ipsilaterally from the nodulus, uvula and medial parts of the flocculus. Purkinje cells (PC) in medial parts of the flocculus project to central regions of SVN, while PC in the nodulus and uvula appear to project mainly to dorsal peripheral regions of SVN. SVN receives sparse projections from the ipsilateral INC, the contralateral central cervical nucleus (CCN) and virtually no projections from the reticular formation. SVN projects via the medial longitudinal fasciculus (MLF) to the ipsilateral trochlear nucleus (TN), the inferior rectus subdivision of the OMC, the INC, the nucleus of Darkschewitsch (ND) and the rostral interstitial nucleus of the MLF (RiMLF). Contralateral projections of SVN cross in the ventral tegmentum caudal to most of the decussating fibers of the superior cerebellar peduncle and terminate in the dorsal rim of the TN and the superior rectus and inferior oblique subdivisions of the OMC; sparse crossed projections enter the INC and the ND. Cerebellar projections of SVN end as mossy fibers in the ipsilateral nodulus, uvula and in medial parts of the flocculus bilaterally. Retrograde transport from unilateral injections of the OMC indicate that afferents from SVN arise ipsilaterally from central and dorsal regions and contralaterally from dorsal peripheral regions. Ventral cell group 'y' receives small numbers of afferent fibers from caudal central parts of the ipsilateral flocculus. No fibers from ventral 'y' could be traced to other vestibular nuclei, the OMC or the cerebellum.(ABSTRACT TRUNCATED AT 400 WORDS)

[1]  E. Tarlov Organization of vestibulo-oculomotor projections in the cat. , 1970, Brain research.

[2]  A. Fuchs,et al.  Contribution of y group of vestibular nuclei and dentate nucleus of cerebellum to generation of vertical smooth eye movements. , 1982, Journal of neurophysiology.

[3]  D. Robinson Eye movements evoked by collicular stimulation in the alert monkey. , 1972, Vision research.

[4]  A. Graybiel,et al.  Some afferent connections of the oculomotor complex in the cat: an experimental study with tracer techniques. , 1974, Brain research.

[5]  A. Weiss,et al.  Vestibular projections to the nuclei of the extraocular muscles. Degeneration resulting from discrete partial lesions of the vestibular nuclei in the monkey. , 1966, The American journal of anatomy.

[6]  C. Winkler Anatomie du système nerveux , 1918 .

[7]  Yu Sato,et al.  Neuronal pathway from floccular caudal zone contributing to vertical eye movements in cats—role of group y nucleus of vestibular nuclei , 1984, Brain Research.

[8]  Yu Sato,et al.  Afferent projections from the brainstem to the three floccular zones in cats. II. Mossy fiber projections , 1983, Brain Research.

[9]  M. Carpenter,et al.  Study of methods foe producing experimental lesions of the central nervous system with special reference to stereo‐taxic technique , 1952 .

[10]  G. Korte,et al.  The brainstem projection of the vestibular nerve in the cat , 1979, The Journal of comparative neurology.

[11]  S. Highstein,et al.  The superior vestibular nucleus: An intracellular hrp study in the cat. II. Non‐vestibulo‐ocular neurons , 1983, The Journal of comparative neurology.

[12]  M. Mesulam,et al.  Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. , 1978, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[13]  A. Brodal Anatomy of the vestibuloreticular connections and possible 'ascending' vestibular pathways from the reticular formation. , 1972, Progress in brain research.

[14]  D. Sparks,et al.  Corollary discharge provides accurate eye position information to the oculomotor system. , 1983, Science.

[15]  U. Büttner,et al.  Vestibular projections to the monkey thalamus: An autoradiographic study , 1979, Brain Research.

[16]  R. Gacek Location of trochlear vestibuloocular neurons in the cat , 1979, Experimental Neurology.

[17]  Y. Uchino,et al.  Branching pattern and properties of vertical- and horizontal-related excitatory vestibuloocular neurons in the cat. , 1982, Journal of neurophysiology.

[18]  A. Brodal,et al.  Anatomy of the Vestibular Nuclei and their Connections , 1974 .

[19]  O. Pompeiano,et al.  Identification of cerebellar corticovestibular neurons retrogradely labeled with horseradish peroxidase , 1979, Neuroscience.

[20]  N. Mizuno,et al.  Direct projections from the Ediger-Westphal nucleus to the cerebellum and spinal cord in the cat: An HRP study , 1978, Neuroscience Letters.

[21]  M. Carpenter,et al.  Distribution of primary vestibular fibers in the brainstem and cerebellum of the monkey , 1984, Brain Research.

[22]  M. Carpenter The dorsal trigeminal tract in the rhesus monkey. , 1957, Journal of anatomy.

[23]  W. Precht,et al.  Changes in the vertical vestibulo-ocular reflex due to kainic acid lesions of the interstitial nucleus of Cajal , 1979, Neuroscience Letters.

[24]  K. Tanimura,et al.  Microelectrode study on the subnuclei of the oculomotor nucleus in the cat. , 1974, Brain research.

[25]  W. Precht,et al.  Synaptic organization of frontal eye field and vestibular afferents to interstitial nucleus of Cajal in the cat. , 1980, Journal of neurophysiology.

[26]  D. Robinson,et al.  Eye movements evoked by cerebellar stimulation in the alert monkey. , 1973, Journal of neurophysiology.

[27]  Yu Sato,et al.  Zonal organization of the floccular Purkinje cells projecting to the vestibular nucleus in cats , 1982, Brain Research.

[28]  C. Markham,et al.  Effect of stimulation of interstitial nucleus of Cajal on vestibular unit activity in the cat. , 1966, Journal of neurophysiology.

[29]  R. Gacek Anatomical demonstration of the vestibulo‐ocular projections in the cat , 1971, Acta oto-laryngologica. Supplementum.

[30]  W. Mehler,et al.  The intrinsic organization of the vestibular complex: evidence for internuclear connevtivity , 1983, Brain Research.

[31]  M. Carpenter,et al.  Accessory oculomotor nuclei in the monkey. , 1970, Journal fur Hirnforschung.

[32]  Y. Uchino,et al.  Properties of central vestibular neurons fired by stimulation of the saccular nerve , 1978, Brain Research.

[33]  L. Muskens AN ANATOMICO-PHYSIOLOGICAL STUDY OF THE POSTERIOR LONGITUDINAL BUNDLE IN ITS RELATION TO FORCED MOVEMENTS , 1914 .

[34]  W. F. Poon,et al.  An electrophysiological study of the sacculo-ocular pathways in cats. , 1975, The Japanese journal of physiology.

[35]  O. Pompeiano,et al.  Commissural, perihypoglossal and reticular afferent projections to the vestibular nuclei in the cat. An experimental anatomical study with the method of the retrograde transport of horseradish peroxidase. , 1978, Archives Italiennes de Biologie.

[36]  G. B. Stanton Afferents to oculomotor nuclei from area “y” in Macaca mulatta: An anterograde degeneration study , 1980, The Journal of comparative neurology.

[37]  E Fluur,et al.  Utricular stimulation and oculomotor reactions , 1970, The Laryngoscope.

[38]  R. Gacek,et al.  Location of brain stem neurons projecting to the oculomotor nucleus in the cat , 1977, Experimental Neurology.

[39]  N. Barmack,et al.  A subparafascicular projection to the medial vestibular nucleus of the rabbit , 1979, Brain Research.

[40]  A. Brodal,et al.  The projection of the "vestibulocerebellum" onto the vestibular nuclei in the cat. , 1967, Archives italiennes de biologie.

[41]  J. Büttner-Ennever,et al.  Oculomotor nucleus afferents in the monkey demonstrated with horseradish peroxidase , 1979, Brain Research.

[42]  A. R. Buchanan The course of the secondary vestibular fibers in the cat , 1937 .

[43]  B. Cohen The Vestibulo-Ocular Reflex Arc , 1974 .

[44]  C. Noback The Cerebellum of the Cat. , 1964 .

[45]  A. Brodal,et al.  Experimental studies of commissural and reticular formation projections from the vestibular nuclei in the cat. , 1968, Brain research.

[46]  Y. Akagi The localization of the motor neurons innervating the extraocular muscles in the oculomotor nuclei of the cat and rabbit, using horseradish peroxidase , 1978, The Journal of comparative neurology.

[47]  A. T. Rasmussen Secondary vestibular tracts in the cat , 1932 .

[48]  Ichiro Shimoyama,et al.  Differential localization of rabbit's flocculus Purkinje cells projecting to the medial and superior vestibular nuclei, investigated by means of the horseradish peroxidase retrograde axonal transport , 1977, Neuroscience Letters.

[49]  M. Carpenter,et al.  Cerebello‐oculomotor fibers in the rhesus monkey , 1964, The Journal of comparative neurology.

[50]  L. Heimer,et al.  Double and triple labeling of neurons with fluorescent substances; The study of collateral pathways in the ascending raphe system , 1980, Neuroscience Letters.

[51]  R. Baker,et al.  Vestibular projections to medial rectus subdivision of oculomotor nucleus. , 1978, Journal of neurophysiology.

[52]  M. Sanders Handbook of Sensory Physiology , 1975 .

[53]  M. Carpenter,et al.  Accessory oculomotor nuclei in the monkey: Projections and effects of discrete lesions , 1970, The Journal of comparative neurology.

[54]  R. Gacek Location of commissural neurons in the vestibular nuclei of the cat , 1978, Experimental Neurology.

[55]  Masao Ito,et al.  Demonstration of zonal projections from the cerebellar flocculus to vestibular nuclei in monkeys (Macaca fuscata) , 1981, Neuroscience Letters.

[56]  H. Kuypers,et al.  Retrograde transport of bisbenzimide and propidium iodide through axons to their parent cell bodies , 1979, Neuroscience Letters.

[57]  S. Highstein,et al.  The ascending tract of Deiters' conveys a head velocity signal to medial rectus motoneurons , 1979, Brain Research.

[58]  W. Abend,et al.  Functional organization of the superior vestibular nucleus of the squirrel monkey , 1977, Brain Research.

[59]  R. Roth,et al.  Evidence for the absence of impulse-regulating somatodendritic and synthesis-modulating nerve terminal autoreceptors on subpopulations of mesocortical dopamine neurons , 1984, Neuroscience.

[60]  R. Warwick Representation of the extra‐ocular muscles in the oculomotor nuclei of the monkey , 1953, The Journal of comparative neurology.

[61]  D. Haines Cerebellar corticonuclear and corticovestibular fibers of the flocculonodular lobe in a prosimian primate (Galago senegalensis) , 1977, The Journal of comparative neurology.

[62]  Shiroh Watanabe,et al.  Properties of secondary vestibular neurons fired by stimulation of ampullary nerve of the vertical, anterior or posterior, semicircular canals in the cat , 1981, Brain Research.

[63]  O. Pompeiano,et al.  The vestibular nuclei in cat. , 1957, Journal of anatomy.

[64]  A. Brodal,et al.  SITE AND MODE OF TERMINATION OF PRIMARY VESTIBULOCEREBELLAR FIBRES IN THE CAT. AN EXPERIMENTAL STUDY WITH SILVER IMPREGNATION METHODS. , 1964, Archives italiennes de biologie.

[65]  O. Pompeiano,et al.  Descending connections to the vestibular nuclei. An experimental study in the cat , 1957, The Journal of comparative neurology.

[66]  Yu Sato,et al.  Zonal organization of the floccular Purkinje cells projecting to the group y of the vestibular nuclear complex and the lateral cerebellar nucleus in cats , 1982, Brain Research.

[67]  V. J. Wilson,et al.  Mammalian Vestibular Physiology , 1979, Springer US.

[68]  Direct projections from vestibular nuclei to facial nucleus in cats. , 1983, Journal of neurophysiology.

[69]  Lloyd P. Gray,et al.  Some experimental evidence on the connections of the vestibular mechanism in the cat , 1926 .

[70]  M. Carpenter,et al.  Afferent and efferent connections of the medial, inferior and lateral vestibular nuclei in the cat and monkey , 1983, Brain Research.

[71]  J. Büttner-Ennever,et al.  A cell group associated with vertical eye movements in the rostral mesencephalic reticular formation of the monkey , 1978, Brain Research.

[72]  M. B. Bender,et al.  Downward gaze in monkeys: stimulation and lesion studies. , 1979, Brain : a journal of neurology.

[73]  S. Nakao,et al.  Direct projection of cat mesodiencephalic neurons to the inferior rectus subdivision of the oculomotor nucleus , 1983, Neuroscience Letters.

[74]  S. Highstein,et al.  Vestibular nucleus neurons relaying excitation from the anterior canal to the oculomotor nucleus , 1978, Brain Research.

[75]  M. Mabuchi,et al.  Mesodiencephalic projections to the inferior olive and the vestibular and perihypoglossal nuclei. , 1970, Brain research.

[76]  E. Hauglie-hanssen Intrinsic Neuronal Organization of the Vestibular Nuclear Complex in the Cat , 1968, Ergebnisse der Anatomie und Entwicklungsgeschichte / Advances in Anatomy, Embryology and Cell Biology / Revues d’anatomie et de morphologie expérimentale.

[77]  C. Saper,et al.  Edinger-Westphal nucleus: Projections to the brain stem and spinal cord in the cat , 1978, Brain Research.

[78]  W. Precht Neuronal Operations in the Vestibular System , 1978, Studies of Brain Function.

[79]  V. Chan‐Palay Cerebellar Dentate Nucleus: Organization, Cytology and Transmitters , 1977 .

[80]  D. Haines,et al.  Secondary vestibulocerebellar projections to flocculonodular lobe in a prosimian primate, Galago senegalensis , 1981, The Journal of comparative neurology.

[81]  Y. Uchino,et al.  Axon collaterals to the extraocular motoneuron pools of inhibitory vestibuloocular neurons activated from the anterior, posterior and horizontal semicircular canals in the cat , 1983, Neuroscience Letters.