Organization of visual mossy fiber projections and zebrin expression in the pigeon vestibulocerebellum

Extensive research has revealed a fundamental organization of the cerebellum consisting of functional parasagittal zones. This compartmentalization has been well documented with respect to physiology, biochemical markers, and climbing fiber afferents. Less is known about the organization of mossy fiber afferents in general, and more specifically in relation to molecular markers such as zebrin. Zebrin is expressed by Purkinje cells that are distributed as a parasagittal array of immunopositive and immunonegative stripes. We examined the concordance of zebrin expression with visual mossy fiber afferents in the vestibulocerebellum (folium IXcd) of pigeons. Visual afferents project directly to folium IXcd as mossy fibers and indirectly as climbing fibers via the inferior olive. These projections arise from two retinal recipient nuclei: the lentiformis mesencephali (LM) and the nucleus of the basal optic root (nBOR). Although it has been shown that these two nuclei project to folium IXcd, the detailed organization of these projections has not been reported. We injected anterograde tracers into LM and nBOR to investigate the organization of mossy fiber terminals and subsequently related this organization to the zebrin antigenic map. We found a parasagittal organization of mossy fiber terminals in folium IXcd and observed a consistent relationship between mossy fiber organization and zebrin stripes: parasagittal clusters of mossy fiber terminals were concentrated in zebrin‐immunopositive regions. We also describe the topography of projections from LM and nBOR to the inferior olive and relate these results to previous studies on the organization of climbing fibers and zebrin expression. J. Comp. Neurol. 518:175–198, 2010. © 2009 Wiley‐Liss, Inc.

[1]  Richard Hawkes,et al.  Aldolase C/zebrin II and the regionalization of the cerebellum , 2007, Journal of Molecular Neuroscience.

[2]  C. Jahr,et al.  Patterned expression of Purkinje cell glutamate transporters controls synaptic plasticity , 2005, Nature Neuroscience.

[3]  N. Gerrits,et al.  Organization of the Vestibulocerebellum , 1996, Annals of the New York Academy of Sciences.

[4]  G. Grant,et al.  Topographic relationship between sagittal Purkinje cell bands revealed by a monoclonal antibody to zebrin I and spinocerebellar projections arising from the central cervical nucleus in the rat , 2004, Experimental Brain Research.

[5]  S. Miller,et al.  Termination and functional organization of the dorsolateral spino‐olivocerebellar path , 1969, The Journal of physiology.

[6]  R. Parenti,et al.  Multiple zonal projections of the basilar pontine nuclei to the cerebellar cortex of the rat , 2001, The Journal of comparative neurology.

[7]  Toshiaki Takeda,et al.  The origin of the pretecto-olivary tract. A study using the horseradish peroxidase method , 1976, Brain Research.

[8]  B. J. Frost,et al.  The visual response properties of neurons in the nucleus of the basal optic root of the pigeon: a quantitative analysis , 2004, Experimental Brain Research.

[9]  J M Bower,et al.  Congruence of mossy fiber and climbing fiber tactile projections in the lateral hemispheres of the rat cerebellum , 2001, The Journal of comparative neurology.

[10]  R. Necker Sensorimotor aspects of flight control in birds: specializations in the spinal cord. , 1994, European journal of morphology.

[11]  Henrik Jörntell,et al.  Synaptic Integration in Cerebellar Granule Cells , 2008, The Cerebellum.

[12]  Monica Valsangkar-Smyth,et al.  Projections of Purkinje cells in the translation and rotation zones of the vestibulocerebellum in pigeon (Columba livia) , 1999, The Journal of comparative neurology.

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

[14]  L. Puelles,et al.  Plurisegmental vestibulocerebellar projections and other hindbrain cerebellar afferents in midterm chick embryos: biotinylated dextranamine experiments in vitro , 2003, Neuroscience.

[15]  J. Simpson,et al.  Projections of individual purkinje cells of identified zones in the ventral nodulus to the vestibular and cerebellar nuclei in the rabbit , 2022 .

[16]  B. Frost,et al.  The pigeon optokinetic system: Visual input in extraocular muscle coordinates , 1996, Visual Neuroscience.

[17]  Richard Hawkes,et al.  Purkinje cell compartmentation as revealed by Zebrin II expression in the cerebellar cortex of pigeons (Columba livia) , 2007, The Journal of comparative neurology.

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

[19]  I. Sugihara Organization and remodeling of the olivocerebellar climbing fiber projection , 2008, The Cerebellum.

[20]  K. Itoh Efferent projections of the pretectum in the cat , 1977, Experimental Brain Research.

[21]  N. Mizuno,et al.  Pretectal projections to the inferior olive in the rabbit. , 1973, Experimental neurology.

[22]  J. Voogd,et al.  Time dependence of terminal degeneration in spino‐cerebellar mossy fiber rosettes in the chicken and the application of terminal degeneration in successive degeneration experiments , 1977, The Journal of comparative neurology.

[23]  K. Hoffmann,et al.  Retinal input to direction selective cells in the nucleus tractus opticus of the cat , 1975, Brain Research.

[24]  J. Pakan,et al.  Inferior olivary neurons innervate multiple zones of the flocculus in pigeons (Columba livia) , 2005, The Journal of comparative neurology.

[25]  Yu Sato,et al.  Afferent projection from the dorsal nucleus of the raphe to the flocculus in cats , 1980, Brain Research.

[26]  H. Jörntell,et al.  Parallel fibre receptive fields of Purkinje cells and interneurons are climbing fibre‐specific , 2001, The European journal of neuroscience.

[27]  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.

[28]  J. Pakan,et al.  Congruence of zebrin II expression and functional zones defined by climbing fiber topography in the flocculus , 2008, Neuroscience.

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

[30]  M. Ariel,et al.  Connectivity of the turtle accessory optic system , 2003, Brain Research.

[31]  B. Frost,et al.  Common reference frame for neural coding of translational and rotational optic flow , 1998, Nature.

[32]  R. Hawkes Antigenic markers of cerebellar modules in the adult mouse. , 1992, Biochemical Society transactions.

[33]  H. Yaginuma,et al.  Differential distribution of spinocerebellar fiber terminals within the lobules of the cerebellar anterior lobe in the cat: An anterograde WGA-HRP study , 1984, Brain Research.

[34]  C. Ekerot,et al.  Correlation between sagittal projection zones of climbing and mossy fibre paths in cat cerebellar anterior lobe. , 1973, Brain research.

[35]  R. Parenti,et al.  Multiple zonal projections of the nucleus reticularis tegmenti pontis to the cerebellar cortex of the rat , 2002, The European journal of neuroscience.

[36]  R. Hawkes,et al.  Transverse zones in the vermis of the mouse cerebellum , 1999, The Journal of comparative neurology.

[37]  Masahiko Watanabe,et al.  Compartmentation of the cerebellar cortex of hummingbirds (Aves: Trochilidae) revealed by the expression of zebrin II and phospholipase Cβ4 , 2009, Journal of Chemical Neuroanatomy.

[38]  M. Garwicz,et al.  Anatomical and physiological foundations of cerebellar information processing , 2005, Nature Reviews Neuroscience.

[39]  N. Gerrits,et al.  The mossy fiber projection of the nucleus reticularis tegmenti pontis to the flocculus and adjacent ventral paraflocculus in the cat , 1984, Neuroscience.

[40]  Richard Apps,et al.  The Distribution of Climbing and Mossy Fiber Collateral Branches from the Copula Pyramidis and the Paramedian Lobule: Congruence of Climbing Fiber Cortical Zones and the Pattern of Zebrin Banding within the Rat Cerebellum , 2003, The Journal of Neuroscience.

[41]  Volker Henn,et al.  Gaze stabilization in the primate , 1987 .

[42]  M. Dawson,et al.  Temporal frequency and velocity-like tuning in the pigeon accessory optic system. , 2003, Journal of neurophysiology.

[43]  Henrik Jörntell,et al.  Properties of Somatosensory Synaptic Integration in Cerebellar Granule Cells In Vivo , 2006, The Journal of Neuroscience.

[44]  D. Cohen,et al.  Projections of the retinorecipient pretectal nuclei in the pigeon (columba livia) , 1988, The Journal of comparative neurology.

[45]  B. Frost,et al.  Responses of pigeon vestibulocerebellar neurons to optokinetic stimulation. II. The 3-dimensional reference frame of rotation neurons in the flocculus. , 1993, Journal of neurophysiology.

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

[47]  W. Precht,et al.  Afferent projections to the cerebellar flocculus in the pigmented rat demonstrated by retrograde transport of horseradish peroxidase , 2004, Experimental Brain Research.

[48]  S. Hunt,et al.  Projections of the nucleus of the basal optic root in the pigeon: An autoradiographic and horseradish peroxidase study , 1980, The Journal of comparative neurology.

[49]  N. Okado,et al.  The terminal distribution pattern of spinocerebellar fibers , 1987, Anatomy and Embryology.

[50]  伊藤 正男 The cerebellum and neural control , 1984 .

[51]  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.

[52]  R. Hawkes,et al.  Topography of purkinje cell compartments and mossy fiber terminal fields in lobules ii and iii of the rat cerebellar cortex: Spinocerebellar and cuneocerebellar projections , 1994, Neuroscience.

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

[54]  David J. Graham,et al.  Differential projections from the vestibular nuclei to the flocculus and uvula‐nodulus in pigeons (Columba livia) , 2008, The Journal of comparative neurology.

[55]  J. Voogd,et al.  Re-examination of the ponto-cerebellar projection in the adult white leghorn (Gallus domesticus). , 1975, Acta morphologica Neerlando-Scandinavica.

[56]  R. Hawkes,et al.  Compartmentation of the granular layer of the cerebellum. , 1997, Histology and histopathology.

[57]  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.

[58]  J. Yamada,et al.  Differences of the primate flocculus and ventral paraflocculus in the mossy and climbing fiber input organization , 1997, The Journal of comparative neurology.

[59]  Brie A. Linkenhoker,et al.  Topographical organization of inferior olive cells projecting to translation and rotation zones in the vestibulocerebellum of pigeons , 1998, Neuroscience.

[60]  B. Frost,et al.  Purkinje cells in the vestibulocerebellum of the pigeon respond best to either translational or rotational wholefield visual motion , 2004, Experimental Brain Research.

[61]  E. Marg THE ACCESSORY OPTIC SYSTEM * , 1964 .

[62]  I. Winship,et al.  Responses of neurons in the medial column of the inferior olive in pigeons to translational and rotational optic flowfields , 2001, Experimental Brain Research.

[63]  Y. Shinoda,et al.  Molecular, Topographic, and Functional Organization of the Cerebellar Cortex: A Study with Combined Aldolase C and Olivocerebellar Labeling , 2004, The Journal of Neuroscience.

[64]  R. Llinás,et al.  The Functional Organization of the Olivo‐Cerebellar System as Examined by Multiple Purkinje Cell Recordings , 1989, The European journal of neuroscience.

[65]  I. Winship,et al.  Spatiotemporal tuning of optic flow inputs to the vestibulocerebellum in pigeons: differences between mossy and climbing fiber pathways. , 2005, Journal of neurophysiology.

[66]  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.

[67]  R.H.S. Carpenter,et al.  Mammalian vestibular physiology , 1980, Nature.

[68]  M. Gottlieb,et al.  Light and electron microscopic study of an avian pretectal nucleus, the lentiform nucleus of the mesencephalon, magnocellular division , 1986, The Journal of comparative neurology.

[69]  R. Hawkes,et al.  Antigenic compartmentation in the mouse cerebellar cortex: Zebrin and HNK‐1 reveal a complex, overlapping molecular topography , 1993, The Journal of comparative neurology.

[70]  W. Precht,et al.  Anatomical studies on the nucleus reticularis tegmenti pontis in the pigmented rat. II. Subcortical afferents demonstrated by the retrograde transport of horseradish peroxidase , 1986, The Journal of comparative neurology.

[71]  H. Collewijn Latency and gain of the rabbit's optokinetic reactions to small movements. , 1972, Brain research.

[72]  Henrik Jörntell,et al.  Cutaneous receptive fields and topography of mossy fibres and climbing fibres projecting to cat cerebellar C3 zone , 1998, The Journal of physiology.

[73]  Richard Hawkes,et al.  Conservation of the architecture of the anterior lobe vermis of the cerebellum across mammalian species. , 2005, Progress in brain research.

[74]  David J. Graham,et al.  Projections of the nucleus of the basal optic root in pigeons (Columba livia): A comparison of the morphology and distribution of neurons with different efferent projections , 2007, Visual Neuroscience.

[75]  J. Voogd,et al.  Cerebellar and olivary projections of the external and rostral internal cuneate nuclei in the cat , 2004, Experimental Brain Research.

[76]  Jan Voogd,et al.  The organization of the corticonuclear and olivocerebellar climbing fiber projections to the rat cerebellar vermis: The congruence of projection zones and the zebrin pattern , 2004, Journal of neurocytology.

[77]  Florent Haiss,et al.  Why do Purkinje cells die so easily after global brain ischemia? Aldolase C, EAAT4, and the cerebellar contribution to posthypoxic myoclonus. , 2002, Advances in neurology.

[78]  S. E. Brauth,et al.  Direction-selective single units in the nucleus lentiformis mesencephali of the pigeon (Columba livia) , 2004, Experimental Brain Research.

[79]  N. Crowder,et al.  Zonal organization of the vestibulocerebellum in pigeons (Columba livia): III. Projections of the translation zones of the ventral uvula and nodulus , 2003, The Journal of comparative neurology.

[80]  J. Eccles,et al.  Analysis of electrical potentials evoked in the cerebellar anterior lobe by stimulation of hindlimb and forelimb nerves , 2004, Experimental Brain Research.

[81]  Yu Sato,et al.  Identification of the Purkinje cell/climbing fiber zone and its target neurons responsible for eye-movement control by the cerebellar flocculus , 1991, Brain Research Reviews.

[82]  H P Zeigler,et al.  Organization of the cerebellum in the pigeon (Columba livia): I. Corticonuclear and corticovestibular connections , 1991, The Journal of comparative neurology.

[83]  J. Voogd,et al.  The medio-lateral distribution of the spinocerebellar projection in the anterior lobe and the simple lobule in the cat and a comparison with some other afferent fibre systems. , 1969, Psychiatria, neurologia, neurochirurgia.

[84]  L. Eisenman,et al.  External cuneocerebellar projection and Purkinje cell zebrin II bands: A direct comparison of parasagittal banding in the mouse cerebellum , 1994, Journal of Chemical Neuroanatomy.

[85]  H. Zeigler,et al.  Cerebellar connections of the trigeminal system in the pigeon (Columbia livia) , 1989, Brain Research.

[86]  D. Marr A theory of cerebellar cortex , 1969, The Journal of physiology.

[87]  Jan Voogd,et al.  Functional and anatomical organization of floccular zones: A preserved feature in vertebrates , 2004, The Journal of comparative neurology.

[88]  D. R. Wylie,et al.  Spatiotemporal properties of fast and slow neurons in the pretectal nucleus lentiformis mesencephali in pigeons. , 2000, Journal of neurophysiology.

[89]  P. Clarke,et al.  Some visual and other connections to the cerebellum of the pigeon , 1977, The Journal of comparative neurology.

[90]  H. Karten,et al.  The accessory optic system in teleosts , 1978, Brain Research.

[91]  Izumi Sugihara,et al.  Identification of aldolase C compartments in the mouse cerebellar cortex by olivocerebellar labeling , 2007, The Journal of comparative neurology.

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

[93]  Richard Hawkes,et al.  From clusters to stripes: The developmental origins of adult cerebellar compartmentation , 2008, The Cerebellum.

[94]  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.

[95]  H. Karten,et al.  A bisynaptic retinocerebellar pathway in the turtle , 1978, Brain Research.

[96]  J. Wallman,et al.  Relation of single unit properties to the oculomotor function of the nucleus of the basal optic root (accessory optic system) in chickens , 2004, Experimental Brain Research.

[97]  Richard Apps,et al.  Precise Spatial Relationships between Mossy Fibers and Climbing Fibers in Rat Cerebellar Cortical Zones , 2006, The Journal of Neuroscience.

[98]  Martijn Schonewille,et al.  Zonal organization of the mouse flocculus: Physiology, input, and output , 2006, The Journal of comparative neurology.

[99]  R. Hawkes,et al.  The modular cerebellum , 1991, Progress in Neurobiology.

[100]  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.

[101]  D. R. Wylie,et al.  Quantitative reassessment of speed tuning in the accessory optic system and pretectum of pigeons. , 2006, Journal of neurophysiology.

[102]  J. Voogd,et al.  Topographical Aspects of the Olivocerebellar System in the Pigeon , 1989 .

[103]  R. Hawkes,et al.  The cloning of zebrin II reveals its identity with aldolase C. , 1994, Development.

[104]  J. Pakan,et al.  Projections of the nucleus lentiformis mesencephali in pigeons (Columba livia): A comparison of the morphology and distribution of neurons with different efferent projections , 2006, The Journal of comparative neurology.

[105]  H. Karten,et al.  A stereotaxic atlas of the brain of the pigeon (Columba livia) , 1967 .

[106]  V Henn,et al.  Gaze stabilization in the primate. The interaction of the vestibulo-ocular reflex, optokinetic nystagmus, and smooth pursuit. , 1987, Reviews of physiology, biochemistry and pharmacology.

[107]  Paul D. Gamlin The pretectum: connections and oculomotor-related roles. , 2006, Progress in brain research.

[108]  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.

[109]  R. Hawkes,et al.  Whole-mount Immunohistochemistry: A High-throughput Screen for Patterning Defects in the Mouse Cerebellum , 2002, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[110]  O. Oscarsson,et al.  Termination and functional organization of the dorsal spino-olivocerebellar path. , 1967, The Journal of physiology.

[111]  K. Fite,et al.  The accessory optic system of Rana pipiens: Neuroanatomical connections and intrinsic organization , 1981, The Journal of comparative neurology.

[112]  J. Voogd Comparative aspects of the structure and fibre connexions of the mammalian cerebellum. , 1967, Progress in brain research.

[113]  Nathan A. Crowder,et al.  Fast and slow neurons in the nucleus of the basal optic root in pigeons , 2001, Neuroscience Letters.

[114]  Brie A. Linkenhoker,et al.  Mossy fibres from the nucleus of the basal optic root project to the vestibular and cerebellar nuclei in pigeons , 1996, Neuroscience Letters.

[115]  B. J. Frost,et al.  Visual response characteristics of neurons in nucleus of basal optic root of pigeons , 2004, Experimental Brain Research.

[116]  H. Collewijn,et al.  The efferent connections of the nucleus of the optic tract and the superior colliculus in the rabbit , 1982, The Journal of comparative neurology.

[117]  W. Precht,et al.  Anatomical studies on the nucleus reticularis tegmenti pontis in the pigmented rat. I. Cytoarchitecture, topography, and cerebral cortical afferents , 1986, The Journal of comparative neurology.

[118]  D R Wylie,et al.  Projections from the nucleus of the basal optic root and nucleus lentiformis mesencephali to the inferior olive in pigeons (Columba livia) , 2001, The Journal of comparative neurology.

[119]  M. Glickstein,et al.  The anatomy of the cerebellum , 1998, Trends in Neurosciences.

[120]  James M Bower,et al.  Correlations between purkinje cell single-unit activity and simultaneously recorded field potentials in the immediately underlying granule cell layer. , 2005, Journal of neurophysiology.

[121]  J. Simpson,et al.  Temporal relations of the complex spike activity of Purkinje cell pairs in the vestibulocerebellum of rabbits , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[122]  O. Oscarsson,et al.  Projections to lateral vestibular nucleus from cerebellar climbing fiber zones , 1978, Experimental Brain Research.

[123]  C. Ekerot,et al.  Parallel fiber receptive fields: a key to understanding cerebellar operation and learning , 2008, The Cerebellum.

[124]  Jan Voogd,et al.  Oculomotor cerebellum. , 2006, Progress in brain research.

[125]  J. Albus A Theory of Cerebellar Function , 1971 .

[126]  B. Frost,et al.  Responses of pigeon vestibulocerebellar neurons to optokinetic stimulation. I. Functional organization of neurons discriminating between translational and rotational visual flow. , 1993, Journal of neurophysiology.

[127]  J. Simpson,et al.  The pretectal nuclear complex and the accessory optic system. , 1988, Reviews of oculomotor research.

[128]  I. Winship,et al.  Projections from the medial column of the inferior olive to different classes of rotation-sensitive Purkinje cells in the flocculus of pigeons , 1999, Neuroscience Letters.

[129]  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.

[130]  N. Crowder,et al.  Topographic organization of inferior olive cells projecting to translational zones in the vestibulocerebellum of pigeons , 2000, The Journal of comparative neurology.

[131]  O. Oscarsson,et al.  Climbing fiber microzones in cerebellar vermis and their projection to different groups of cells in the lateral vestibular nucleus , 1978, Experimental Brain Research.

[132]  Brie A. Linkenhoker,et al.  Projections of the nucleus of the basal optic root in pigeons (Columba livia) revealed with biotinylated dextran amine , 1997, The Journal of comparative neurology.

[133]  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.

[134]  R. Hawkes,et al.  Zebrin II: A polypeptide antigen expressed selectively by purkinje cells reveals compartments in rat and fish cerebellum , 1990, The Journal of comparative neurology.

[135]  M. Magnin,et al.  Non-cerebellar visual afferents to the vestibular nuclei involving the prepositus hypoglossal complex: An autoradiographic study in the rat , 2004, Experimental Brain Research.

[136]  Yoshikazu Shinoda,et al.  Molecular, Topographic, and Functional Organization of the Cerebellar Nuclei: Analysis by Three-Dimensional Mapping of the Olivonuclear Projection and Aldolase C Labeling , 2007, The Journal of Neuroscience.

[137]  J. Kimm,et al.  Anatomical evidence that the medial terminal nucleus of the accessory optic tract in mammals provides a visual mossy fiber input to the flocculus , 1978, Brain Research.

[138]  J. Wallman,et al.  Accessory optic system and pretectum of birds: comparisons with those of other vertebrates. , 1985, Brain, behavior and evolution.

[139]  R. Blanks,et al.  Pretectal and brain stem projections of the medial terminal nucleus of the accessory optic system of the rabbit and rat as studied by anterograde and retrograde neuronal tracing methods , 1984, The Journal of comparative neurology.

[140]  D. Schwarz,et al.  The primary vestibular projection to the cerebellar cortex in the pigeon (Columba livia) , 1983, The Journal of comparative neurology.

[141]  J. Pakan,et al.  Two optic flow pathways from the pretectal nucleus lentiformis mesencephali to the cerebellum in pigeons (Columba livia) , 2006, The Journal of comparative neurology.

[142]  D. Haines,et al.  Evidence of a direct projection from the medial terminal nucleus of the accessory optic system to lobule IX of the cerebellar cortex in the tree shrew (Tupaia glis) , 1985, Neuroscience Letters.

[143]  J. Voogd,et al.  Topography of olivo‐cortico‐nuclear modules in the intermediate cerebellum of the rat , 2005, The Journal of comparative neurology.

[144]  F. Lui,et al.  The accessory optic system: basic organization with an update on connectivity, neurochemistry, and function. , 2006, Progress in brain research.

[145]  H. Richard,et al.  Structural and Molecular Compartmentation in the Cerebellum , 1993, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[146]  B. Frost,et al.  Complex spike activity of Purkinje cells in the ventral uvula and nodulus of pigeons in response to translational optic flow. , 1999, Journal of neurophysiology.

[147]  H. Gioanni,et al.  Single unit activity in the nucleus of the basal optic root (nBOR) during optokinetic, vestibular and visuo-vestibular stimulations in the alert pigeon (Columbia livia) , 2004, Experimental Brain Research.

[148]  R. Hawkes,et al.  Parasagittal organization of the rat cerebellar cortex: Direct comparison of purkinje cell compartments and the organization of the spinocerebellar projection , 1990, The Journal of comparative neurology.

[149]  K. Herrup,et al.  The compartmentalization of the cerebellum. , 1997, Annual review of neuroscience.