Zonal organization of the vestibulocerebellum in pigeons (Columba livia): III. Projections of the translation zones of the ventral uvula and nodulus

Previous electrophysiological studies in pigeons have shown that the complex spike activity of Purkinje cells in the medial vestibulocerebellum (nodulus and ventral uvula) is modulated by patterns of optic flow that result from self‐translation along a particular axis in three‐dimensional space. There are four response types based on the axis of preferred translational optic flow. By using a three axis system, where +X, +Y, and +Z represent rightward, upward, and forward self‐motion, respectively, the four cell types are t(+Y), t(–Y), t(–X–Z), and t(–X+Z), with the assumption of recording from the left side of the head. These response types are organized into parasagittal zones. In this study, we injected the anterograde tracer biotinylated dextran amine into physiologically identified zones. The t(–X–Z) zone projected dorsally within the vestibulocerebellar process (pcv) on the border with the medial cerebellar nucleus (CbM), and labeling was found in the CbM itself. The t(–X+Z) zone also projected to the pcv and CbM, but to areas ventral to the projection sites of the t(–X–Z) zone. The t(–Y) zone also projected to the pcv, but more ventrally on the border with the superior vestibular nucleus (VeS). Some labeling was also found in the dorsal VeS and the dorsolateral margin of the caudal descending vestibular nucleus, and a small amount of labeling was found laterally in the caudal margin of the medial vestibular nucleus. The data set was insufficient to draw conclusions about the projection of the t(+Y) zone. These results are contrasted with the projections of the flocculus, compared with the primary vestibular projection, and implications for collimotor function are discussed. J. Comp. Neurol. 465:179–194, 2003. © 2003 Wiley‐Liss, Inc.

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

[2]  J. Labandeira-Garcia,et al.  Identification of abducens motoneurons, accessory abducens motoneurons, and abducens internuclear neurons in the chick by retrograde transport of horseradish peroxidase , 1987, The Journal of comparative neurology.

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

[4]  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.

[5]  R. W. Allan,et al.  Organization of the cerebellum in the pigeon (Columba livia): III. Corticovestibular connections with eye and neck premotor areas , 1991, The Journal of comparative neurology.

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

[7]  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.

[8]  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.

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

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

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

[12]  M. Friedman Visual control of head movements during avian locomotion , 1975, Nature.

[13]  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.

[14]  J. Wold The vestibular nuclei in the domestic hen (Gallus domesticus). I. Normal anatomy. , 1976, Anatomy and embryology.

[15]  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.

[16]  J. Simpson,et al.  Representations of ocular rotations in the cerebellar flocculus of the rabbit. , 1989, Progress in brain research.

[17]  J. I. Simpson,et al.  Three-Dimensional Representation of Retinal Image Movement by Climbing Fiber Activity , 1989 .

[18]  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.

[19]  A. Reiner,et al.  Biotinylated dextran amine as an anterograde tracer for single- and double-labeling studies , 1992, Journal of Neuroscience Methods.

[20]  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.

[21]  D. Schwarz,et al.  Projection of afferents from individual vestibular sense organs to the vestibular nuclei in the pigeon. , 1986, Acta oto-laryngologica.

[22]  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.

[23]  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.

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

[25]  F. Jorge-Barreiro,et al.  Afferent connections of the oculomotor nucleus in the chick , 1989, The Journal of comparative neurology.

[26]  J. Simpson,et al.  Functional and anatomic organization of three-dimensional eye movements in rabbit cerebellar flocculus. , 1994, Journal of neurophysiology.

[27]  O. Larsell The development and subdivisions of the cerebellum of birds , 1948, The Journal of comparative neurology.

[28]  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.

[29]  J. Wold The vestibular nuclei in the domestic hen (Gallus domesticus). IV. The projection to the spinal cord. , 1978, Brain, behavior and evolution.

[30]  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.

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

[32]  O. Larsell,et al.  Further observations on the cerebellum of birds , 1952, The Journal of comparative neurology.

[33]  J. Voogd,et al.  Reciprocal connections between the caudal vermis and the vestibular nuclei in the rabbit , 1985, Neuroscience Letters.

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

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

[36]  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.

[37]  F. Lui,et al.  Projections of the lateral terminal accessory optic nucleus of the common marmoset (Callithrix jacchus) , 1995, The Journal of comparative neurology.

[38]  I. Gibson,et al.  Isolation of DNA from B Chromosomes in Grasshoppers , 1970, Nature.

[39]  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.

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

[41]  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.

[42]  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.

[43]  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.

[44]  J. Simpson,et al.  The accessory optic system and its relation to the vestibulocerebellum. , 1979, Progress in brain research.

[45]  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.

[46]  D. Whitlock A neurohistological and neurophysiological study of afferent fiber tracts and receptive areas of the avian cerebellum , 1952, The Journal of comparative neurology.

[47]  J. Dickman,et al.  Differential central projections of vestibular afferents in pigeons , 1996, The Journal of comparative neurology.

[48]  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.

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

[50]  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.

[51]  C. Balaban,et al.  Olivo-vestibular and cerebello-vestibular connections in albino rabbits , 1984, Neuroscience.

[52]  W. Graf,et al.  A quantitative analysis of the spatial organization of the vestibulo-ocular reflexes in lateral- and frontal-eyed animals—I. Orientation of semicircular canals and extraocular muscles , 1984, Neuroscience.

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

[54]  B. Frost The Optokinetic Basis of Head-bobbing in the Pigeon , 1978 .

[55]  B. Frost,et al.  Responses of neurons in the nucleus of the basal optic root to translational and rotational flowfields. , 1999, Journal of neurophysiology.

[56]  Peter L. Williams,et al.  The Cerebellum of the Cat , 1965 .

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

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

[59]  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.

[60]  J. Simpson,et al.  The accessory optic system of rabbit. II. Spatial organization of direction selectivity. , 1988, Journal of neurophysiology.

[61]  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.

[62]  J I Simpson,et al.  EYE‐MUSCLE GEOMETRY AND COMPENSATORY EYE MOVEMENTS IN LATERAL‐EYED AND FRONTAL‐EYED ANIMALS * , 1981, Annals of the New York Academy of Sciences.

[63]  J. Wold The vestibular nuclei in the domestic hen (Gallus domesticus). VII.--Afferents from the spinal cord. , 1979, Archives italiennes de biologie.

[64]  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.

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

[66]  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.

[67]  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.

[68]  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.

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

[70]  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.

[71]  J. Wild Descending projections of the songbird nucleus robustus archistriatalis , 1993, The Journal of comparative neurology.

[72]  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.

[73]  H. Zeigler,et al.  Organization of the cerebellum in the pigeon (Columba livia): II. Projections of the cerebellar nuclei , 1991, The Journal of comparative neurology.

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

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

[76]  G. Aston-Jones,et al.  Axonal collateral-collateral transport of tract tracers in brain neurons: false anterograde labelling and useful tool , 1997, Neuroscience.

[77]  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.

[78]  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.

[79]  J I Simpson,et al.  The selection of reference frames by nature and its investigators. , 1985, Reviews of oculomotor research.