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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

Published online by Cambridge University Press:  04 October 2007

DOUGLAS R.W. WYLIE ,
JANELLE M.P. PAKAN ,
CAMERON A. ELLIOTT ,
DAVID J. GRAHAM  and
ANDREW N. IWANIUK
DOUGLAS R.W. WYLIE
Affiliation:
Department of Psychology, University of Alberta, Edmonton, Alberta, Canada University Centre for Neuroscience, University of Alberta, Edmonton, Alberta, Canada
JANELLE M.P. PAKAN
Affiliation:
University Centre for Neuroscience, University of Alberta, Edmonton, Alberta, Canada
CAMERON A. ELLIOTT
Affiliation:
University Centre for Neuroscience, University of Alberta, Edmonton, Alberta, Canada
DAVID J. GRAHAM
Affiliation:
University Centre for Neuroscience, University of Alberta, Edmonton, Alberta, Canada
ANDREW N. IWANIUK
Affiliation:
Department of Psychology, University of Alberta, Edmonton, Alberta, Canada
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Abstract

The avian nucleus of the basal optic root (nBOR) is a visual structure involved in the optokinetic response. nBOR consists of several morphologically distinct cell types, and in the present study, we sought to determine if these different cell types had differential projections. Using retrograde tracers, we examined the morphology and distribution of nBOR neurons projecting to the vestibulocerebellum (VbC), inferior olive (IO), dorsal thalamus, the pretectal nucleus lentiformis mesencephali (LM), the contralateral nBOR, the oculomotor complex (OMC) and a group of structures along the midline of the mesencephalon. The retrogradely labeled neurons fell into two broad categories: large neurons, most of which were multipolar rather than fusiform and small neurons, which were either fusiform or multipolar. From injections into the IO, LM, contralateral nBOR, and structures along the midline-mesencephalon small nBOR neurons were labeled. Although there were no differences with respect to the size of the labeled neurons from these injections, there were some differences with the respect to the distribution of labeled neurons and the proportion of multipolar vs. fusiform neurons. From injections into the VbC, the large multipolar cells were labeled throughout nBOR. The only other cases in which these large neurons were labeled were contralateral OMC injections. To investigate if single neurons project to multiple targets we used paired injections of red and green fluorescent retrograde tracers into different targets. Double-labeled neurons were never observed indicating that nBOR neurons do not project to multiple targets. We conclude that individual nBOR neurons have unique projections, which may have differential roles in processing optic flow and controlling the optokinetic response.

Keywords

OptokineticOculomotorAccessory optic systemPretectumVestibulocerebellumInferior olive
Type
Research Article
Information
Visual Neuroscience , Volume 24 , Issue 5 , September 2007 , pp. 691 - 707
Copyright
© 2007 Cambridge University Press

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References

REFERENCES

Arends, J. & Voogd, J. (1989). Topographic aspects of the olivocerebellar system in the pigeon. Experimental Brain Research 17, 52–57.Google Scholar
Arends, J.J., Allan, R.W. & Zeigler, H.P. (1991). Organization of the cerebellum in the pigeon (Columba livia): III. Corticovestibular connections with eye and neck premotor areas. Journal of Comparative Neurology 306, 273–289.Google Scholar
Azevedo, T.A., Cukiert, A. & Britto, L.R. (1983). A pretectal projection upon the accessory optic nucleus in the pigeon: An anatomical and electrophysiological study. Neuroscience Letter 43, 13–18.Google Scholar
Baldo, M.V. & Britto, L.R. (1990). Accessory optic-pretectal interactions in the pigeon. Brazilian Journal of Medical and Biological Research 23, 1037–1040.Google Scholar
Brecha, N., Karten, H.J. & Hunt, S.P. (1980). Projections of the nucleus of the basal optic root in the pigeon: An autoradiographic and horseradish peroxidase study. Journal of Comparative Neurology 189, 615–670.Google Scholar
Burns, S. & Wallman, J. (1981). Relation of single unit properties to the oculomotor function of the nucleus of the basal optic root (accessory optic system) in chickens. Experimental Brain Research 42, 171–180.Google Scholar
Cao, P., Yang, Y. & Wang, S.R. (2006). Differential modulation of thalamic neurons by optokinetic nuclei in the pigeon. Brain Research 1069, 159–165.Google Scholar
Casini, G., Bingman, V.P. & Bagnoli, P. (1986). Connections of the pigeon dorsomedial forebrain studied with WGA-HRP and 3H-proline. Journal of Comparative Neurology 245, 454–470.Google Scholar
Clarke, P.G. (1977). Some visual and other connections to the cerebellum of the pigeon. Journal of Comparative Neurology 174, 535–552.Google Scholar
Clarke, R.J., Giolli, R.A., Blanks, R.H., Torigoe, Y. & Fallon, J.H. (1989). Neurons of the medial terminal accessory optic nucleus of the rat are poorly collateralized. Visual Neuroscience 2, 269–273.Google Scholar
Crowder, N.A., Dawson, M.R. & Wylie, D.R. (2003a). Temporal frequency and velocity-like tuning in the pigeon accessory optic system. Journal of Neurophysiology 90, 1829–1841.Google Scholar
Crowder, N.A., Lehmann, H., Parent, M.B. & Wylie, D.R. (2003b). The accessory optic system contributes to the spatio-temporal tuning of motion-sensitive pretectal neurons. Journal of Neurophysiology 90, 1140–1151.Google Scholar
Eccles, J.C., Llinas, R., Sasaki, K. & Voorhoeve, P.E. (1966). Interaction experiments on the responses evoked in Purkinje cells by climbing fibres. Journal of Physiology 182, 297–315.Google Scholar
Fallon, J.H., Schmued, L.C., Wang, C., Miller, R. & Banales, G. (1984). Neurons in the ventral tegmentum have separate populations projecting to telencephalon and inferior olive, are histochemically different, and may receive direct visual input. Brain Research 321, 332–336.Google Scholar
Finger, T.E. & Karten, H.J. (1978). The accessory optic system in teleosts. Brain Research 153, 144–149.Google Scholar
Fite, K.V. (1985). Pretectal and accessory-optic visual nuclei of fish, amphibia and reptiles: Theme and variations. Brain, Behavior and Evolution 26, 71–90.Google Scholar
Fite, K.V., Brecha, N., Karten, H.J. & Hunt, S.P. (1981). Displaced ganglion cells and the accessory optic system of pigeon. Journal of Comparative Neurology 195, 279–288.Google Scholar
Fite, K.V., Carey, R.G. & Vicario, D. (1977). Visual neurons in frog anterior thalamus. Brain Research 127, 283–290.Google Scholar
Foster, T.C., Castro, C.A. & McNaughton, B.L. (1989). Spatial selectivity of rat hippocampal neurons: Dependence on preparedness for movement. Science 244, 1580–1582.Google Scholar
Frost, B.J., Wylie, D.R. & Wang, Y.C. (1990). The processing of object and self-motion in the tectofugal and accessory optic pathways of birds. Vision Research 30, 1677–1688.Google Scholar
Gamlin, P.D. (2005). The pretectum: connections and oculomotor-related roles. Progress in Brain Research 151, 379–405.Google Scholar
Gamlin, P.D. & Cohen, D H. (1988). Projections of the retinorecipient pretectal nuclei in the pigeon (Columba livia). Journal of Comparative Neurology 269, 18–46.Google Scholar
Gibson, J.J. (1954). The visual perception of objective motion and subjective movement. Psychological Review 61, 304–314.Google Scholar
Gioanni, H., Rey, J., Villalobos, J. & Dalbera, A. (1984). 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). Experimental Brain Research 57, 49–60.Google Scholar
Gioanni, H., Rey, J., Villalobos, J., Richard, D. & Dalbera, A. (1983). Optokinetic nystagmus in the pigeon (Columba livia). II. Role of the pretectal nucleus of the accessory optic system (AOS). Experimental Brain Research 50, 237–247.Google Scholar
Giolli, R.A., Blanks, R.H. & Lui, F. (2005). The accessory optic system: Basic organization with an update on connectivity, neurochemistry, and function. Progress in Brain Research 151, 407–440.Google Scholar
Giolli, R.A., Blanks, R.H. & Torigoe, Y. (1984). 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. Journal of Comparative Neurology 227, 228–251.Google Scholar
Giolli, R.A., Blanks, R.H., Torigoe, Y. & Williams, D.D. (1985). 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. Journal of Comparative Neurology 232, 99–116.Google Scholar
Giolli, R.A., Torigoe, Y. & Blanks, R.H. (1988). Nonretinal projections to the medial terminal accessory optic nucleus in rabbit and rat: A retrograde and anterograde transport study. Journal of Comparative Neurology 269, 73–86.Google Scholar
Giolli, RA., Torigoe, Y., Clarke, R.J., Blanks, R.H. & Fallon, J.H. (1992). GABAergic and non-GABAergic projections of accessory optic nuclei, including the visual tegmental relay zone, to the nucleus of the optic tract and dorsal terminal accessory optic nucleus in rat. Journal of Comparative Neurology 319, 349–358.Google Scholar
Gottlieb, M.D. & McKenna, O.C. (1986). Light and electron microscopic study of an avian pretectal nucleus, the lentiform nucleus of the mesencephalon, magnocellular division. Journal of Comparative Neurology 248, 133–145.Google Scholar
Graf, W., Simpson, J.I. & Leonard, C.S. (1988). Spatial organization of visual messages of the rabbit's cerebellar flocculus. II. Complex and simple spike responses of Purkinje cells. Journal of Neurophysiology 60, 2091–2121.Google Scholar
Grasse, K. & Cynader, M. (1990). The accessory optic system in frontal-eyed animals. In Vision and Visual Dysfunction, Vol. IV, The Neuronal Basis of Visual Function. New York: MacMillan.
Gu, Y., Wang, Y. & Wang, S.R. (2002). Visual responses of neurons in the nucleus of the basal optic root to stationary stimuli in pigeons. Journal of Neuroscience Research 67, 698–704.Google Scholar
Haines, D.E. & Sowa, T.E. (1985). 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). Neuroscience Letter 55, 125–130.Google Scholar
Ibbotson, M.R. & Clifford, C.W. (2001). Interactions between ON and OFF signals in directional motion detectors feeding the not of the wallaby. Journal of Neurophysiology 86, 997–1005.Google Scholar
Ibbotson, M.R., Mark, R.F. & Maddess, T.L. (1994). Spatiotemporal response properties of direction-selective neurons in the nucleus of the optic tract and dorsal terminal nucleus of the wallaby, Macropus eugenii. Journal of Neurophysiology 72, 2927–2943.Google Scholar
Ito, M., Orlov, I. & Yamamoto, M. (1982). Topographical representation of vestibulo-ocular reflexes in rabbit cerebellar flocculus. Neuroscience 7, 1657–1664.Google Scholar
Iwaniuk, A.N. & Wylie, D.R. (2007). Neural specialization for hovering in hummingbirds: Hypertrophy of the pretectal nucleus Lentiformis mesencephali. Journal of Comparative Neurology 500, 211–221.Google Scholar
Karten, H. & Hodos, W. (1967). A stereotaxic Atlas of the Brain of the Pigeon (Columba livia). Baltimore: Johns Hopkins Press.
Karten, H.J., Hodos, W., Nauta, W.J. & Revzin, A.M. (1973). Neural connections of the “visual wulst” of the avian telencephalon. Experimental studies in the piegon (Columba livia) and owl (Speotyto cunicularia). Journal of Comparative Neurology 150, 253–278.Google Scholar
Karten, J.H., Fite, K.V. & Brecha, N. (1977). Specific projection of displaced retinal ganglion cells upon the accessory optic system in the pigeon (Columbia livia). Proceedings of the National Academy of Sciences 74, 1753–1756.Google Scholar
Kawasaki, T. & Sato, Y. (1980). Afferent projection from the dorsal nucleus of the raphe to the flocculus in cats. Brain Research 197, 496–502.Google Scholar
Kenigfest, N., Rio, J.P., Belekhova, M., Reperant, J., Vesselkin, N. & Ward, R. (2004). Pretectal and tectal afferents to the dorsal lateral geniculate nucleus of the turtle: An electron microscopic axon tracing and gamma-aminobutyric acid immunocytochemical study. Journal of Comparative Neurology 475, 107–127.Google Scholar
Labandeira-Garcia, J.L., Guerra-Seijas, M.J., Labandeira-Garcia, J.A. & Jorge-Barreiro, F.J. (1989). Afferent connections of the oculomotor nucleus in the chick. Journal of Comparative Neurology 282, 523–534.Google Scholar
Lappe, M. & Rauschecker, J.P. (1994). Heading detection from optic flow. Nature 369, 712–713.Google Scholar
Lau, K.L., Glover, R.G., Linkenhoker, B. & Wylie, D.R. (1998). Topographical organization of inferior olive cells projecting to translation and rotation zones in the vestibulocerebellum of pigeons. Neuroscience 85, 605–614.Google Scholar
Lee, D.N. & Lishman, R. (1977). Visual control of locomotion. Scandinavian Journal of Psychology 18, 224–230.Google Scholar
Li, Z. & Fite, K.V. (2001). GABAergic visual pathways in the frog Rana pipiens. Visual Neuroscience 18, 457–464.Google Scholar
Lisberger, S.G., Miles, F.A. & Zee, D.S. (1984). Signals used to compute errors in monkey vestibuloocular reflex: Possible role of flocculus. Journal of Neurophysiology 52, 1140–1153.Google Scholar
McKenna, O.C. & Wallman, J. (1981). Identification of avian brain regions responsive to retinal slip using 2-deoxyglucose. Brain Research 210, 455–460.Google Scholar
McKenna, O.C. & Wallman, J. (1985). Accessory optic system and pretectum of birds: Comparisons with those of other vertebrates. Brain Behavior and Evolution 26, 91–116.Google Scholar
McNaughton, B.L., Barnes, C.A., Gerrard, J.L., Gothard, K., Jung, M.W., Knierim, J.J., Kudrimoti, H., Qin, Y., Skaggs, W.E., Suster, M. & Weaver, K.L. (1996). Deciphering the hippocampal polyglot: The hippocampus as a path integration system. Journal of Experimental Biology 199, 173–185.Google Scholar
McNaughton, N., Logan, B., Panickar, K.S., Kirk, I.J., Pan, W.X., Brown, N.T. & Heenan, A. (1995). Contribution of synapses in the medial supramammillary nucleus to the frequency of hippocampal theta rhythm in freely moving rats. Hippocampus 5, 534–545.Google Scholar
Montgomery, N., Fite, K.V. & Bengston, L. (1981). The accessory optic system of Rana pipiens: Neuroanatomical connections and intrinsic organization. Journal of Comparative Neurology 203, 595–612.Google Scholar
Morgan, B. & Frost, B.J. (1981). Visual response characteristics of neurons in nucleus of basal optic root of pigeons. Experimental Brain Research 42, 181–188.Google Scholar
Muller, R.U., Ranck, J.B., Jr. & Taube, J.S. (1996). Head direction cells: Properties and functional significance. Current Opinions in Neurobiology 6, 196–206.Google Scholar
Nagao, S. (1983). Effects of vestibulocerebellar lesions upon dynamic characteristics and adaptation of vestibulo-ocular and optokinetic responses in pigmented rabbits. Experimental Brain Research 53, 36–46.Google Scholar
Pakan, J.M., Krueger, K., Kelcher, E., Cooper, S., Todd, K.G. & Wylie, D.R. (2006). Projections of the nucleus lentiformis mesencephali in pigeons (Columba livia): A comparison of the morphology and distribution of neurons with different efferent projections. Journal of Comparative Neurology 495, 84–99.Google Scholar
Pakan, J.M., Todd, K.G., Nguyen, A.P., Winship, I.R., Hurd, P.L., Jantzie, L.L. & Wylie, D.R. (2005). Inferior olivary neurons innervate multiple zones of the flocculus in pigeons (Columba livia). Journal of Comparative Neurology 486, 159–168.Google Scholar
Pakan, J.M. & Wylie, D.R. (2006). Two optic flow pathways from the pretectal nucleus lentiformis mesencephali to the cerebellum in pigeons (Columba livia). Journal of Comparative Neurology 499, 732–744.Google Scholar
Prochnow, N., Lee, P., Hall, W.C. & Schmidt, M. (2007). In vitro properties of neurons in the rat pretectal nucleus of the optic tract. Journal of Neurophysiology 97, 3574–3584.Google Scholar
Reiner, A., Brecha, N. & Karten, H.J. (1979). A specific projection of retinal displaced ganglion cells to the nucleus of the basal optic root in the chicken. Neuroscience 4, 1679–1688.Google Scholar
Reiner, A. & Karten, H.J. (1978). A bisynaptic retinocerebellar pathway in the turtle. Brain Research 150, 163–169.Google Scholar
Robinson, D.A. (1976). Adaptive gain control of vestibuloocular reflex by the cerebellum. Journal of Neurophysiology 39, 954–969.Google Scholar
Schmidt, M., Van Der Togt, C., Wahle, P. & Hoffmann, K.P. (1998). Characterization of a directional selective inhibitory input from the medial terminal nucleus to the pretectal nuclear complex in the rat. European Journal of Neuroscience 10, 1533–1543.Google Scholar
Sharp, P.E., Blair, H.T., Etkin, D. & Tzanetos, D.B. (1995). Influences of vestibular and visual motion information on the spatial firing patterns of hippocampal place cells. Journal of Neuroscience 15, 173–189.Google Scholar
Shimizu, T. & Karten, H. (1991). Central Visual Pathways in Retiles and Birds: Evolution of the Visual System, Vol. 2, London: MacMillan.
Simpson, J.I. (1984). The accessory optic system. Annual Review of Neuroscience 7, 13–41.Google Scholar
Simpson, J.I., Giolli, R.A. & Blanks, R.H. (1988a). The pretectal nuclear complex and the accessory optic system. Reviews of Oculomotor Research 2, 335–364.Google Scholar
Simpson, J.I., Leonard, C.S. & Soodak, R.E. (1988b). The accessory optic system. Analyzer of self-motion. New York Academy of Sciences 545, 170–179.Google Scholar
Tang, Z.X. & Wang, S.R. (2002). Intracellular recording and staining of neurons in the pigeon nucleus lentiformis mesencephali. Brain, Behavior and Evolution 60, 52–58.Google Scholar
Van Der Togt, C., Nunes Cardozo, B. & Van Der Want, J. (1991). Medial terminal nucleus terminals in the nucleus of the optic tract contain GABA: An electron microscopical study with immunocytochemical double labeling of GABA and PHA-L. Journal of Comparative Neurology 312, 231–241.Google Scholar
Van Der Togt, C. & Schmidt, M. (1994). Inhibition of neuronal activity in the nucleus of the optic tract due to electrical stimulation of the medial terminal nucleus in the rat. European Journal of Neuroscience 6, 558–564.Google Scholar
Van Der Want, J.J., Nunes Cardozo, J.J. & Van Der Togt, C. (1992). GABAergic neurons and circuits in the pretectal nuclei and the accessory optic system of mammals. Progress in Brain Research 90, 283–305.Google Scholar
Veenman, C.L., Reiner, A. & Honig, M.G. (1992). Biotinylated dextran amine as an anterograde tracer for single- and double-labeling studies. Journal of Neuroscience Methods 41, 239–254.Google Scholar
Waespe, W., Cohen, B. & Raphan, T. (1983). Role of the flocculus and paraflocculus in optokinetic nystagmus and visual-vestibular interactions: Effects of lesions. Experimental in Brain Research 50, 9–33.Google Scholar
Weber, J.T. (1985). Pretectal complex and accessory optic system of primates. Brain Behavior and Evolution 26, 117–140.Google Scholar
Webster, D.M. & Steeves, J.D. (1988). Origins of brainstem-spinal projections in the duck and goose. Journal of Comparative Neurology 273, 573–583.Google Scholar
Whishaw, I.Q. & Maaswinkel, H. (1998). Rats with fimbria-fornix lesions are impaired in path integration: A role for the hippocampus in “sense of direction.” Journal of Neuroscience 18, 3050–3058.Google Scholar
Whishaw, I.Q., McKenna, J.E. & Maaswinkel, H. (1997). Hippocampal lesions and path integration. Current Opinions in Neurobiology 7, 228–234.Google Scholar
Wild, J.M. (1989). Pretectal and tectal projections to the homologue of the dorsal lateral geniculate nucleus in the pigeon: An anterograde and retrograde tracing study with cholera toxin conjugated to horseradish peroxidase. Brain Research 479, 130–137.Google Scholar
Wild, J.M., Karten, H.J. & Frost, B.J. (1993). Connections of the auditory forebrain in the pigeon (Columba livia). Journal of Comparative Neurology 337, 32–62.Google Scholar
Wilson, M.A. & McNaughton, B.L. (1993). Dynamics of the hippocampal ensemble code for space. Science 261, 1055–1058.Google Scholar
Winfield, J.A., Hendrickson, A. & Kimm, J. (1978). Anatomical evidence that the medial terminal nucleus of the accessory optic tract in mammals provides a visual mossy fiber input to the flocculus. Brain Research 151, 175–182.Google Scholar
Winship, I.R., Crowder, N.A. & Wylie, D.R. (2006). Quantitative reassessment of speed tuning in the accessory optic system and pretectum of pigeons. Journal of Neurophysiology 95, 546–551.Google Scholar
Winship, I.R., Hurd, P.L. & Wylie, D.R. (2005). Spatiotemporal tuning of optic flow inputs to the vestibulocerebellum in pigeons: Differences between mossy and climbing fiber pathways. Journal of Neurophysiology 93, 1266–1277.Google Scholar
Winship, I.R. & Wylie, D.R. (2001). Responses of neurons in the medial column of the inferior olive in pigeons to translational and rotational optic flowfields. Experimental Brain Research 141, 63–78.Google Scholar
Winship, I.R. & Wylie, D.R. (2003). Zonal organization of the vestibulocerebellum in pigeons (Columba livia): I. Climbing fiber input to the flocculus. Journal of Comparative Neurology 456, 127–139.Google Scholar
Winship, I.R. & Wylie, D.R. (2006). Receptive-field structure of optic flow responsive Purkinje cells in the vestibulocerebellum of pigeons. Visual Neuroscience 23, 115–126.Google Scholar
Winterson, B.J. & Brauth, S.E. (1985). Direction-selective single units in the nucleus lentiformis mesencephali of the pigeon (Columba livia). Experimental Brain Research 60, 215–226.Google Scholar
Wylie, D.R. (2001). Projections from the nucleus of the basal optic root and nucleus lentiformis mesencephali to the inferior olive in pigeons (Columba livia). Journal of Comparative Neurology 429, 502–513.Google Scholar
Wylie, D.R., Bischof, W.F. & Frost, B.J. (1998a). Common reference frame for neural coding of translational and rotational optic flow. Nature 392, 278–282.Google Scholar
Wylie, D.R., Brown, M.R., Barkley, R.R., Winship, I.R., Crowder, N.A. & Todd, K.G. (2003a). Zonal organization of the vestibulocerebellum in pigeons (Columba livia): II. Projections of the rotation zones of the flocculus. Journal of Comparative Neurology 456, 140–153.Google Scholar
Wylie, D.R., Brown, M.R., Winship, I.R., Crowder, N.A. & Todd, K.G. (2003b). Zonal organization of the vestibulocerebellum in pigeons (Columba livia): III. Projections of the translation zones of the ventral uvula and nodulus. Journal of Comparative Neurology 465, 179–194.Google Scholar
Wylie, D.R. & Crowder, N.A. (2000). Spatiotemporal properties of fast and slow neurons in the pretectal nucleus lentiformis mesencephali in pigeons. Journal of Neurophysiology 84, 2529–2540.Google Scholar
Wylie, D.R. & Frost, B.J. (1990). The visual response properties of neurons in the nucleus of the basal optic root of the pigeon: a quantitative analysis. Experimental Brain Research 82, 327–336.Google Scholar
Wylie, D.R. & Frost, B.J. (1991). Purkinje cells in the vestibulocerebellum of the pigeon respond best to either translational or rotational wholefield visual motion. Experimental Brain Research 86, 229–232.Google Scholar
Wylie, D.R. & Frost, B.J. (1993). Responses of pigeon vestibulocerebellar neurons to optokinetic stimulation. II. The 3-dimensional reference frame of rotation neurons in the flocculus. Journal of Neurophysiology 70, 2647–2659.Google Scholar
Wylie, D.R. & Frost, B.J. (1996). The pigeon optokinetic system: visual input in extraocular muscle coordinates. Visual Neuroscience 13, 945–953.Google Scholar
Wylie, D.R. & Frost, B.J. (1999a). Complex spike activity of Purkinje cells in the ventral uvula and nodulus of pigeons in response to translational optic flow. Journal of Neurophysiology 81, 256–266.Google Scholar
Wylie, D.R. & Frost, B.J. (1999b). Responses of neurons in the nucleus of the basal optic root to translational and rotational flowfields. Journal of Neurophysiology 81, 267–276.Google Scholar
Wylie, D.R., Glover, R.G. & Lau, K.L. (1998b). Projections from the accessory optic system and pretectum to the dorsolateral thalamus in the pigeon (Columbia livia): A study using both anteretrograde and retrograde tracers. Journal of Comparative Neurology 391, 456–469.Google Scholar
Wylie, D.R., Kripalani, T. & Frost, B.J. (1993). Responses of pigeon vestibulocerebellar neurons to optokinetic stimulation. I. Functional organization of neurons discriminating between translational and rotational visual flow. Journal of Neurophysiology 70, 2632–2646.Google Scholar
Wylie, D.R. & Linkenhoker, B. (1996). Mossy fibres from the nucleus of the basal optic root project to the vestibular and cerebellar nuclei in pigeons. Neuroscience Letter 219, 83–86.Google Scholar
Wylie, D.R., Linkenhoker, B. & Lau, K.L. (1997). Projections of the nucleus of the basal optic root in pigeons (Columba livia) revealed with biotinylated dextran amine. Journal of Comparative Neurology 384, 517–536.Google Scholar
Wylie, D.R., Winship, I.R. & Glover, R.G. (1999). Projections from the medial column of the inferior olive to different classes of rotation-sensitive Purkinje cells in the flocculus of pigeons. Neuroscience Letter 268, 97–100.Google Scholar
Zanker, J.M., Srinivasan, M.V. & Egelhaaf, M. (1999). Speed tuning in elementary motion detectors of the correlation type. Biological Cybernetics 80, 109–116.Google Scholar
Zayats, N., Davies, D.C., Nemeth, A. & Tombol, T. (2002). The intrinsic neuronal organisation of the nucleus of the basal optic root in the domestic chicken: A light and electron microscopic study using anterograde tracers and postembedding GABA-immunostaining. European Journal of Morphology 40, 101–113.Google Scholar
Zayats, N., Eyre, M.D., Nemeh, A. & Tombol, T. (2003). The intrinsic organization of the nucleus lentiformis mesencephali magnocellularis: A light- and electron-microscopic examination. Cells Tissues Organs 174, 194–207.Google Scholar
Zee, D.S., Yamazaki, A., Butler, P.H. & Gucer, G. (1981). Effects of ablation of flocculus and paraflocculus of eye movements in primate. Journal of Neurophysiology 46, 878–899.Google Scholar