Inferior olive and oculomotor system.

Three subnuclei within the inferior olive are implicated in the control of eye movement; the dorsal cap (DC), the beta-nucleus and the dorsomedial cell column (DMCC). Each of these subnuclei can be further divided into clusters of cells that encode specific parameters of optokinetic and vestibular stimulation. DC neurons respond to optokinetic stimulation in one of three planes, corresponding to the anatomical planes of the semicircular canals. Neurons in the beta-nucleus and DMCC respond to vestibular stimulation in the planes of the vertical semicircular canals and otoliths. Each these olivary nuclei receives excitatory and inhibitory signals from pre-olivary structures. The DC receives excitatory signals from the ipsilateral nucleus of the optic tract (NOT) and inhibitory signals from the contralateral nucleus prepositus hypoglossi (NPH). The beta-nucleus and DMCC receive inhibitory signals from the ipsilateral nucleus parasolitarius (Psol) and excitatory signals from the contralateral dorsal Y group. Consequently, the olivary projection to the cerebellum, although totally crossed, still represents bilateral sensory stimulation. Inputs to the inferior olive from the NOT, NPH, Psol or Y-group discharge at frequencies of 10-100 imp/s. CFRs discharge at 1-5 imp/s; a frequency reduction of an order of magnitude. Inferior olivary projections to the contralateral cerebellum are sagittally arrayed onto multiple cerebellar folia. These arrays establish coordinate systems in the flocculus and nodulus, representing head-body movement. These climbing fiber-defined spatial coordinate systems align Purkinje cell discharge onto subjacent cerebellar and vestibular nuclei. In the oculomotor system, olivo-cerebellar circuitry enhances and modifies eye movements based on movement of the head-body in space.

[1]  H. Noda,et al.  Afferent and efferent connections of the oculomotor cerebellar vermis in the macaque monkey , 1987, The Journal of comparative neurology.

[2]  M. Kusunoki,et al.  Nature of optokinetic response and zonal organization of climbing fiber afferents in the vestibulocerebellum of the pigmented rabbit , 1990, Experimental Brain Research.

[3]  N H Barmack,et al.  Effects of microlesions of dorsal cap of inferior olive of rabbits on optokinetic and vestibuloocular reflexes. , 1980, Journal of neurophysiology.

[4]  Yu Sato,et al.  Zonal organization of olivocerebellar projections to the uvula in rabbits , 1985, Brain Research.

[5]  C. Bell,et al.  Discharge properties of Purkinje cells recorded on single and double microelectrodes. , 1969, Journal of Neurophysiology.

[6]  J. Voogd,et al.  The parasagittal zonation within the olivocerebellar projection. I. Climbing fiber distribution in the vermis of cat cerebellum , 1977, The Journal of comparative neurology.

[7]  N. Barmack,et al.  Cerebellar Climbing Fibers Modulate Simple Spikes in Purkinje Cells , 2003, The Journal of Neuroscience.

[8]  Yu Sato,et al.  Differential mossy fiber projections to the dorsal and ventral uvula in the cat , 1989, The Journal of comparative neurology.

[9]  T. Kawasaki,et al.  Short-term modulation of cerebellar Purkinje cell activity after spontaneous climbing fiber input. , 1992, Journal of neurophysiology.

[10]  E. Mugnaini,et al.  Fine structure of the dorsal cap of the inferior olive and its GAB aergic and non‐Gabaergic input from the nucleus prepositus hypoglossi in rat and rabbit , 1993, The Journal of comparative neurology.

[11]  C. I. Zeeuw,et al.  Coexistence of choline acetyltransferase and GABA in axon terminals in the dorsal cap of the rat inferior olive , 1996, Brain Research.

[12]  J. Voogd,et al.  Organization of projections from the inferior olive to the cerebellar nuclei in the rat , 2000, The Journal of comparative neurology.

[13]  T. Ebner,et al.  The changes in Purkinje cell simple spike activity following spontaneous climbing fiber inputs , 1982, Brain Research.

[14]  R Llinás,et al.  Long-term modifiability of anomalous and delayed rectification in guinea pig inferior olivary neurons , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  R. Llinás,et al.  The olivo-cerebellar system: Functional properties as revealed by harmaline-induced tremor , 1973, Experimental Brain Research.

[16]  J. Simpson The accessory optic system. , 1984, Annual review of neuroscience.

[17]  C. Bell,et al.  Relations among climbing fiber responses of nearby Purkinje Cells. , 1972, Journal of neurophysiology.

[18]  N. Gerrits,et al.  Input of anterior and posterior semicircular canal interneurons encoding head-velocity to the dorsal Y group of the vestibular nuclei. , 2000, Journal of neurophysiology.

[19]  J. Simpson,et al.  The accessory optic system of rabbit. I. Basic visual response properties. , 1988, Journal of neurophysiology.

[20]  E. Mugnaini,et al.  Parasolitary nucleus: A source of GABAergic vestibular information to the inferior olive of rat and rabbit , 1998, The Journal of comparative neurology.

[21]  Yu Sato,et al.  Zonal organization of climbing fiber projections to the uvula in the cat , 1989, The Journal of comparative neurology.

[22]  W. Precht,et al.  Responses of cat prepositus hypoglossi neurons to horizontal angular acceleration , 1977, Neuroscience.

[23]  K. Hoffmann,et al.  A quantitative analysis of the direction-specific response of neurons in the cat's nucleus of the optic tract , 2004, Experimental Brain Research.

[24]  H. Shojaku,et al.  Activity of neurons in the beta nucleus of the inferior olive of the rabbit evoked by natural vestibular stimulation , 2004, Experimental Brain Research.

[25]  J I Simpson,et al.  The Accessory Optic System Analyzer of Self‐Motion a , 1988, Annals of the New York Academy of Sciences.

[26]  A. Perachio,et al.  Distribution of vestibular afferents that innervate the sacculus and posterior canal in the gerbil , 1986, The Journal of comparative neurology.

[27]  K. Maekawa,et al.  Responses of the nucleus of the optic tract neurons projecting to the nucleus reticularis tegmenti pontis upon optokinetic stimulation in the rabbit , 1984, Neuroscience Research.

[28]  N H Barmack,et al.  Eye movements evoked by microstimulation of dorsal cap of inferior olive in the rabbit. , 1980, Journal of neurophysiology.

[29]  I. Winship,et al.  Zonal organization of the vestibulocerebellum in pigeons (Columba livia): I. Climbing fiber input to the flocculus , 2003, The Journal of comparative neurology.

[30]  C. I. Zeeuw,et al.  Olivary projecting neurons in the nucleus prepositus hypoglossi, group y and ventral dentate nucleus do not project to the oculomotor complex in the rabbit and the rat , 1995, Neuroscience Letters.

[31]  H Collewijn,et al.  Oculomotor areas in the rabbits midbrain and pretectum. , 1975, Journal of neurobiology.

[32]  A. Brodal,et al.  The olivocerebellar projection studied with the method of retrograde axonal transport of horseradish peroxidase. V. The projections to the flocculonodular lobe and the paraflocculus in the rabbit , 1977, The Journal of comparative neurology.

[33]  C. Buisseret-Delmas,et al.  Sagittal organization of the olivocerebellonuclear pathway in the rat. I. Connections with the nucleus fastigii and the nucleus vestibularis lateralis , 1988, Neuroscience Research.

[34]  J. Voogd,et al.  Chemoarchitectonic zonation of the monkey cerebellum , 1986, Brain Research.

[35]  H. Fushiki,et al.  Topography and reciprocal activity of cerebellar Purkinje cells in the uvula-nodulus modulated by vestibular stimulation. , 1997, Journal of neurophysiology.

[36]  C. W. Oyster,et al.  Retinal ganglion cells projecting to the rabbit accessory optic system , 1980, The Journal of comparative neurology.

[37]  H. Collewijn,et al.  A search for habituation of vestibulo-ocular reactions to rotatory and linear sinusoidal accelerations in the rabbit , 1975, Experimental Neurology.

[38]  D E Hillman,et al.  The primate cerebellar cortex: a Golgi and electron microscopic study. , 1967, Progress in brain research.

[39]  G. Blatt,et al.  The olivocerebellar projection to the uvula in the mouse , 1983, The Journal of comparative neurology.

[40]  R. Blanks,et al.  Projections of the dorsal and lateral terminal accessory optic nuclei and of the interstitial nucleus of the superior fasciculus (posterior fibers) in the rabbit and rat , 1988, The Journal of comparative neurology.

[41]  K. Maekawa,et al.  Receptive field organization of climbing fiber afferents responding to optokinetic stimulation in the cerebellar nodulus and flocculus of the pigmented rabbit , 2004, Experimental Brain Research.

[42]  PROGRESS IN BRAIN RESEARCH Vol. 25. The Cerebellum , 1968 .

[43]  C. Sotelo,et al.  Postnatal development of the inferior olivary complex in the rat. II. Topographic organization of the immature olivocerebellar projection , 1984, The Journal of comparative neurology.

[44]  Enrico Mugnaini,et al.  The rat inferior olive as seen with immunostaining for glutamate decarboxylase , 2004, Anatomy and Embryology.

[45]  B. P. Choudhury Ganglion cell distribution in the albino rabbit's retina , 1981, Experimental Neurology.

[46]  Tadashi Kawasaki,et al.  Topographical distribution of Purkinje cells in the uvula and the nodulus projecting to the vestibular nuclei in cats , 1987, Brain Research.

[47]  K. Maekawa,et al.  Bilateral visual inputs to the dorsal cap of inferior olive: Differential localization and inhibitory interactions , 2004, Experimental Brain Research.

[48]  M. Bentivoglio,et al.  Independent efferent populations in the nucleus of the optic tract: An anatomical and physiological study in rat and cat , 1995, The Journal of comparative neurology.

[49]  H. Shojaku,et al.  Vestibularly induced slow oscillations in climbing fiber responses of Purkinje cells in the cerebellar nodulus of the rabbit , 1992, Neuroscience.

[50]  A. Berthoz,et al.  Neuronal activity in prepositus nucleus correlated with eye movement in the alert cat. , 1982, Journal of neurophysiology.

[51]  A. Fuchs,et al.  Anatomical connections of the primate pretectal nucleus of the optic tract , 1994, The Journal of comparative neurology.

[52]  J. Simpson,et al.  Visual climbing fiber input to rabbit vestibulo-cerebellum: a source of direction-specific information. , 1974, Brain research.

[53]  R. Llinás,et al.  Electrotonic coupling between neurons in cat inferior olive. , 1974, Journal of neurophysiology.

[54]  N. Barmack,et al.  Vestibular signals in the parasolitary nucleus. , 2000, Journal of neurophysiology.

[55]  J. Büttner-Ennever,et al.  Pretectal projections to the oculomotor complex of the monkey and their role in eye movements , 1996, The Journal of comparative neurology.

[56]  J. Simpson,et al.  Spatial organization of visual messages of the rabbit's cerebellar flocculus. I. Typology of inferior olive neurons of the dorsal cap of Kooy. , 1988, Journal of neurophysiology.

[57]  T. Yamadori,et al.  Corticonuclear and corticovestibular projections from the uvula in the albino rat: differential projections from sublobuli of the uvula , 1989, Brain Research.

[58]  R. Llinás,et al.  Properties and distribution of ionic conductances generating electroresponsiveness of mammalian inferior olivary neurones in vitro. , 1981, The Journal of physiology.

[59]  C. Balaban,et al.  Zonal organization of olivo-nodulus projections in albino rabbits , 1988, Neuroscience Research.

[60]  J. Szentágothai,et al.  Participation of Golgi neuron processes in the cerebellar glomeruli: An electron microscope study , 1966, Experimental Brain Research.

[61]  N H Barmack,et al.  Vestibular and visual climbing fiber signals evoked in the uvula-nodulus of the rabbit cerebellum by natural stimulation. , 1995, Journal of neurophysiology.

[62]  J. Fallon,et al.  GABAergic neurons comprise a major cell type in rodent visual relay nuclei: an immunocytochemical study of pretectal and accessory optic nuclei , 2004, Experimental Brain Research.

[63]  M. Molliver,et al.  The Olivocerebellar Projection Mediates Ibogaine-Induced Degeneration of Purkinje Cells: A Model of Indirect, Trans-Synaptic Excitotoxicity , 1997, The Journal of Neuroscience.

[64]  N. Slater,et al.  Unipolar brush cell: a potential feedforward excitatory interneuron of the cerebellum , 2000, Neuroscience.

[65]  J. Eccles,et al.  The excitatory synaptic action of climbing fibres on the Purkinje cells of the cerebellum , 1966, The Journal of physiology.

[66]  John P Welsh,et al.  Fundamental role of inferior olive connexin 36 in muscle coherence during tremor. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[67]  R Llinás,et al.  Bilaterally synchronous complex spike Purkinje cell activity in the mammalian cerebellum , 2001, The European journal of neuroscience.

[68]  J. Simpson,et al.  Climbing fiber responses evoked in vestibulocerebellum of rabbit from visual system. , 1973, Journal of neurophysiology.

[69]  Enrico Mugnaini,et al.  Comparative study of glutamate decarboxylase immunoreactive boutons in the mammalian inferior olive , 1989, The Journal of comparative neurology.

[70]  Johannes van der Steen,et al.  Floccular Complex Spike Response to Transparent Retinal Slip , 2001, Neuron.

[71]  P. Strata,et al.  The inhibitory effect of the olivocerebellar input on the cerebellar Purkinje cells in the rat † , 1982, The Journal of physiology.

[72]  A. Brodal The olivocerebellar projection in the cat as studied with the method of retrograde axonal transport of horseradish peroxidase. II. The projection to the uvula , 1976, The Journal of comparative neurology.

[73]  J. Simpson,et al.  Spatial organization of visual messages of the rabbit's cerebellar flocculus. II. Complex and simple spike responses of Purkinje cells. , 1988, Journal of neurophysiology.

[74]  A. Fuchs,et al.  Floccular efferents in the rhesus macaque as revealed by autoradiography and horseradish peroxidase , 1985, The Journal of comparative neurology.

[75]  J. Bernard Topographical organization of olivocerebellar and corticonuclear connections in the rat—An WGA‐HRP study: I. Lobules IX, X, and the flocculus , 1987, The Journal of comparative neurology.

[76]  M. Mustari,et al.  Transneuronal pathways to the vestibulocerebellum , 1996, The Journal of comparative neurology.

[77]  Yoshikazu Shinoda,et al.  Functional compartmentalization in the flocculus and the ventral dentate and dorsal group y nuclei: An analysis of single olivocerebellar axonal morphology , 2004, The Journal of comparative neurology.

[78]  N. Gerrits,et al.  Zonal organization of the climbing fiber projection to the flocculus and nodulus of the rabbit: A combined axonal tracing and acetylcholinesterase histochemical study , 1995, The Journal of comparative neurology.

[79]  Are the climbing fibres essential for the Purkinje cell inhibitory action? , 2004, Experimental Brain Research.

[80]  N. Crowder,et al.  Zonal organization of the vestibulocerebellum in pigeons (Columba livia): II. Projections of the rotation zones of the flocculus , 2003, The Journal of comparative neurology.

[81]  K. Maekawa,et al.  Collateralized projection of visual climbing fibers to the flocculus and nodulus of the rabbit , 1984, Neuroscience Research.

[82]  S. Katayama,et al.  Parasagittal zonal pattern of olivo-nodular projections in rabbit cerebellum , 1988, Neuroscience Research.

[83]  B. N. Cardozo,et al.  Ultrastructural organization of the retino‐pretecto‐olivary pathway in the rabbit: A combined WGA‐HRP tracing and gaba immunocytochemical study , 1990, The Journal of comparative neurology.

[84]  R. Llinás,et al.  Structural study of inferior olivary nucleus of the cat: morphological correlates of electrotonic coupling. , 1974, Journal of neurophysiology.

[85]  J. Büttner-Ennever Neuroanatomy of the oculomotor system , 1988 .

[86]  N. Barmack,et al.  Multiple-unit activity evoked in dorsal cap of inferior olive of the rabbit by visual stimulation. , 1980, Journal of neurophysiology.

[87]  H. Noda,et al.  Topographical organization of the olivocerebellar projection upon the posterior vermis in the rat , 1989, Neuroscience Research.

[88]  R. Baker,et al.  Anatomical connections of the nucleus prepositus of the cat , 1985, The Journal of comparative neurology.

[89]  N. Barmack,et al.  Optokinetically evoked expression of corticotropin-releasing factor in inferior olivary neurons of rabbits , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[90]  N. Barmack,et al.  Cholinergic projection to the dorsal cap of the inferior olive of the rat, rabbit, and monkey , 1993, The Journal of comparative neurology.

[91]  Toshiaki Takeda,et al.  Origin of descending afferents to the rostral part of dorsal cap of inferior olive which transfers contralateral optic activities to the flocculus. a horseradish peroxidase study , 1979, Brain Research.

[92]  T. Kawasaki,et al.  Target neurons of floccular caudal zone inhibition in Y-group nucleus of vestibular nuclear complex. , 1987, Journal of neurophysiology.

[93]  W. Young,et al.  Optokinetic stimulation increases corticotropin-releasing factor mRNA in inferior olivary neurons of rabbits , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[94]  D. Rossi,et al.  Properties of transmission at a giant glutamatergic synapse in cerebellum: the mossy fiber-unipolar brush cell synapse. , 1995, Journal of neurophysiology.

[95]  C. Tanaka,et al.  Immunohistochemical localization of γ-aminobutyric acid- and aspartate-containing neurons in the guinea pig vestibular nuclei , 1987, Brain Research.

[96]  E. Mugnaini,et al.  The unipolar brush cell: A neglected neuron of the mammalian cerebellar cortex , 1994, The Journal of comparative neurology.

[97]  A. Hughes Topographical relationships between the anatomy and physiology of the rabbit visual system , 1971, Documenta Ophthalmologica.

[98]  C. G. Phillips,et al.  Excitatory and inhibitory processes acting upon individual Purkinje cells of the cerebellum in cats , 1956, The Journal of physiology.

[99]  J. Bloedel,et al.  Action of climbing fibers in cerebellar cortex of the cat. , 1971, Journal of neurophysiology.

[100]  N. Gerrits,et al.  The rostral dorsal cap and ventrolateral outgrowth of the rabbit inferior olive receive a GABAergic input from dorsal group Y and the ventral dentate nucleus , 1994, The Journal of comparative neurology.

[101]  N. Barmack,et al.  Regional and cellular distribution of protein kinase C in rat cerebellar purkinje cells , 2000, The Journal of comparative neurology.

[102]  J. Simpson,et al.  Afferents to the vestibulo-cerebellum and the origin of the visual climbing fibers in the rabbit , 1975, Brain Research.

[103]  H. Collewijn Direction-selective units in the rabbit's nucleus of the optic tract , 1975, Brain Research.

[104]  Y. Lamarre,et al.  Rhythmic activity induced by harmaline in the olivo-cerebello-bulbar system of the cat. , 1973, Brain research.

[105]  T. Ruigrok Collateralization of climbing and mossy fibers projecting to the nodulus and flocculus of the rat cerebellum , 2003, The Journal of comparative neurology.

[106]  J. Simpson,et al.  Projections of individual purkinje cells of identified zones in the flocculus to the vestibular and cerebellar nuclei in the rabbit , 1994, The Journal of comparative neurology.

[107]  R. Llinás,et al.  The mossy fibre-granule cell relay of the cerebellum and its inhibitory control by Golgi cells , 2004, Experimental Brain Research.

[108]  Blank Rh,et al.  The pretectal nuclear complex and the accessory optic system. , 1988 .

[109]  Toshiaki Takeda,et al.  Electrophysiological identification of the climbing and mossy fiber pathways from the rabbit's retina to the contralateral cerebellar flocculus , 1976, Brain Research.

[110]  J. Voogd,et al.  Organization of inferior olivary projections to the flocculus and ventral paraflocculus of the rat cerebellum , 1992, The Journal of comparative neurology.

[111]  Masao Ito The molecular organization of cerebellar long-term depression , 2002, Nature Reviews Neuroscience.

[112]  M. Cynader,et al.  Electrophysiology of lateral and dorsal terminal nuclei of the cat accessory optic system. , 1984, Journal of neurophysiology.

[113]  C I De Zeeuw,et al.  Effects of nucleus prepositus hypoglossi lesions on visual climbing fiber activity in the rabbit flocculus. , 2000, Journal of neurophysiology.

[114]  Yosef Yarom,et al.  Low threshold calcium spikes, intrinsic neuronal oscillation and rhythm generation in the CNS , 1989, Journal of Neuroscience Methods.

[115]  Robert E. Foster,et al.  Oscillatory behavior in inferior olive neurons: Mechanism, modulation, cell aggregates , 1986, Brain Research Bulletin.

[116]  J. Yamada,et al.  Descending pathways of the nucleus of the optic tract in the rat , 1979, Brain Research.

[117]  J. Sladek,et al.  Morphology of the inferior olivary complex of the rhesus monkey (Macaca mulatta) , 1973, The Journal of comparative neurology.

[118]  E. Dietrichs,et al.  The interconnection between the vestibular nuclei and the nodulus: a study of reciprocity , 1988, Brain Research.

[119]  R. Blanks,et al.  Projections of medial terminal accessory optic nucleus, ventral tegmental nuclei, and substantia nigra of rabbit and rat as studied by retrograde axonal transport of horseradish peroxidase , 1985, The Journal of comparative neurology.

[120]  A. Fuchs,et al.  Discharge patterns in nucleus prepositus hypoglossi and adjacent medial vestibular nucleus during horizontal eye movement in behaving macaques. , 1992, Journal of neurophysiology.

[121]  Yu Sato,et al.  Zonal organization of climbing fiber projections to the nodulus in the cat , 1994, Brain Research.

[122]  Y. Zhang,et al.  Dorsal Y group in the squirrel monkey. I. Neuronal responses during rapid and long-term modifications of the vertical VOR. , 1995, Journal of neurophysiology.

[123]  J. Voogd,et al.  Anatomical compartments in the white matter of the rabbit flocculus , 1995, The Journal of comparative neurology.

[124]  A. Fuchs,et al.  Afferents to the flocculus of the cerebellum in the rhesus macaque as revealed by retrograde transport of horseradish peroxidase , 1985, The Journal of comparative neurology.

[125]  M. Kano,et al.  Nature of optokinetic response and zonal organization of climbing fiber afferents in the vestibulocerebellum of the pigmental rabbit. I, The flocculus. II, The nodulus , 1990 .

[126]  P Strata,et al.  Inferior olive inactivation decreases the excitability of the intracerebellar and lateral vestibular nuclei in the rat. , 1983, The Journal of physiology.

[127]  R. A. Hensbroek,et al.  Analysis of Cx36 Knockout Does Not Support Tenet That Olivary Gap Junctions Are Required for Complex Spike Synchronization and Normal Motor Performance , 2002, Annals of the New York Academy of Sciences.