Skip to main content

Expression of calcium-binding proteins in pathways from the nucleus of the basal optic root to the cerebellum in pigeons


Calcium-binding protein expression has proven useful in delineating neural pathways. For example, in birds, calbindin is strongly expressed in the tectofugal pathway, whereas parvalbumin (PV) is strongly expressed in the thalamofugal pathway. Whether neurons within other visual regions also differentially express calcium-binding proteins, however, has not been extensively studied. The nucleus of the basal optic root (nBOR) is a retinal-recipient nucleus that is critical for the generation of the optokinetic response. The nBOR projects to the cerebellum both directly and indirectly via the inferior olive (IO). The cerebellar and IO projections originate from different neurons within the nBOR, but whether they can also be differentiated based on calcium-binding protein expression is unknown. In this study, we combined retrograde neuronal tracing from the cerebellum and IO with fluorescent immunohistochemistry for PV and calretinin (CR) in the nBOR of pigeons. We found that about half (52.3%) of the cerebellar-projecting neurons were CR+ve, and about one-third (33.6%) were PV+ve. Most (90%) of these PV+ve cells were also labeled for CR. In contrast, very few of the IO-projecting neurons expressed CR or PV (≤2%). Thus, the direct nBOR–cerebellar and indirect nBOR–olivocerebellar pathways to the cerebellum can be distinguished based on the differential expression of CR and PV.

Corresponding author
*Address correspondence and reprint requests to: Douglas R. Wong-Wylie, Department of Psychology, University of Alberta, Edmonton, Alberta, Canada T6G 2E9. E-mail:
Hide All
Alley, K., Baker, R. & Simpson, J.I. (1975). Afferents to the vestibulo-cerebellum and the origin of the visual climbing fibers in the rabbit. Brain Research 98, 582589.
Arends, J. & Voogd, J. (1989). Topographic aspects of the olivocerebellar system in the pigeon. Experimental Brain Research Series 17, 5257.
Baimbridge, K.G., Celio, M.R. & Rogers, J.H. (1992). Calcium-binding proteins in the nervous system. Trends in Neurosciences 15, 303308.
Blümcke, I., Hof, P.R., Morrison, J.H. & Celio, M.R. (1990). Distribution of parvalbumin immunoreactivity in the visual cortex of Old World monkeys and humans. Journal of Comparative Neurology 301, 417432.
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, 615670.
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, 171180.
Celio, M.R. (1990). Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35, 375475.
Clarke, P.G. (1977). Some visual and other connections to the cerebellum of the pigeon. Journal of Comparative Neurology 174, 535552.
Crowder, N.A., Winship, I.R. & Wylie, D.R. (2000). Topographic organization of inferior olive cells projecting to translational zones in the vestibulocerebellum of pigeons. Journal of Comparative Neurology 419, 8795.
De Castro, F., Cobos, I., Puelles, L. & Martinez, S. (1998). Calretinin in pretecto- and olivocerebellar projections in the chick: Immunohistochemical and experimental study. Journal of Comparative Neurology 397, 149162.
DeFelipe, J. (1997). Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, parvalbumin and calretinin in the neocortex. Journal of Chemical Neuroanatomy 14, 119.
Eccles, J.C., Llinas, R. & Sasaki, K. (1966). The excitatory synaptic action of climbing fibres on the Purkinje cells of the cerebellum. Journal of Physiology 182, 268296.
Finger, T.E. & Karten, H.J. (1978). The accessory optic system in teleosts. Brain Research 153, 144149.
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, 279288.
Friedman, M.B. (1975). Visual control of head movements during avian locomotion. Nature 255, 6769.
Frost, B. (1978). The optokinetic basis of head-bobbing in the pigeon. Journal of Experimental Biology 74, 187195.
Gamlin, P.D. & Cohen, D.H. (1988). Projections of the retinorecipient pretectal nuclei in the pigeon (Columba livia). Journal of Comparative Neurology 269, 1846.
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, 4960.
Gioanni, H., Villalobos, J., Rey, J. & Dalbera, A. (1983). Optokinetic nystagmus in the pigeon (Columba livia). III. Role of the nucleus ectomamillaris (nEM): Interactions in the accessory optic system (AOS). Experimental Brain Research 50, 248258.
Giolli, R.A., Blanks, R.H. & Lui, F. (2006). The accessory optic system: Basic organization with an update on connectivity, neurochemistry, and function. Progress in Brain Research 151, 407440.
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, 228251.
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, 99116.
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, 7386.
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, 20912121.
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 Letters 55, 125130.
Heyers, D., Manns, M., Luksch, H., Gunturkun, O. & Mouritsen, H. (2008). Calcium-binding proteins label functional streams of the visual system in a songbird. Brain Research Bulletin 75, 348355.
Holstege, G. & Collewijn, H. (1982). The efferent connections of the nucleus of the optic tract and the superior colliculus in the rabbit. Journal of Comparative Neurology 209, 139175.
Ito, M., Orlov, I. & Yamamoto, M. (1982). Topographical representation of vestibulo-ocular reflexes in rabbit cerebellar flocculus. Neuroscience 7, 16571664.
Karten, H. & Hodos, W. (1967). A Stereotaxic Atlas of the Brain of the Pigeon (Columba livia). Baltimore, MD: Johns Hopkins Press.
Karten, H.J. & Shimizu, T. (1989). The origins of neocortex: Connections and lamination as distinct events in evolution. Journal of Cognitive Neuroscience 1, 290301.
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 of the United States of America 74, 17531756.
Kawasaki, T. & Sato, Y. (1980). Afferent projection from the dorsal nucleus of the raphe to the flocculus in cats. Brain Research 197, 496502.
Kohr, G., Lambert, C.E. & Mody, I. (1991). Calbindin-D28K (CaBP) levels and calcium currents in acutely dissociated epileptic neurons. Experimental Brain Research 85, 543551.
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, 605614.
Leonard, C.S., Simpson, J.I. & Graf, W. (1988). Spatial organization of visual messages of the rabbit’s cerebellar flocculus. I. Typology of inferior olive neurons of the dorsal cap of Kooy. Journal of Neurophysiology 60, 20732090.
Leuba, G. & Saini, K. (1997). Colocalization of parvalbumin, calretinin and calbindin D-28k in human cortical and subcortical visual structures. Journal of Chemical Neuroanatomy 13, 4152.
Lisberger, S.G., Miles, F.A. & Zee, D.S. (1984). Signals used to compute errors in monkey vestibuloocular reflex: possible role of flocculus. J Neurophysiology 52, 11401153.
Medina, L. & Reiner, A. (2000). Do birds possess homologues of mammalian primary visual, somatosensory and motor cortices? Trends in Neurosciences 23, 112.
Miceli, D., Gioanni, H., Reperant, J. & Peyrichoux, J. (1979). The avian visual Wulst: I. An anatomical study of afferent and efferent pathways. II. An electrophysiological study of the functional properties of single neurons. In Neural Mechanisms of Behaviour in the Pigeon, ed. Granda, A.M. & Maxwell, J.H., pp. 223254. New York: Plenum Press.
Miceli, D., Reperant, J., Villalobos, J. & Dionne, L. (1987). Extratelencephalic projections of the avian visual Wulst. A quantitative autoradiographic study in the pigeon Columbia livia. Journal für Hirnforschung 28, 4557.
Mizuno, N., Mochizuki, K., Akimoto, C. & Matsushima, R. (1973). Pretectal projections to the inferior olive in the rabbit. Experimental Neurology 39, 498506.
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, 595612.
Morgan, B. & Frost, B.J. (1981). Visual response characteristics of neurons in nucleus of basal optic root of pigeons. Experimental Brain Research 42, 181188.
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, 3646.
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, 732744.
Pfeiffer, C.P. & Britto, L.R. (1997). Distribution of calcium-binding proteins in the chick visual system. Brazilian Journal of Medical and Biological Research 30, 13151318.
Pritz, M.B. & Siadati, A. (1999). Calcium binding protein immunoreactivity in nucleus rotundus in a reptile, Caiman crocodilus. Brain, Behavior and Evolution 53, 277287.
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, 16791688.
Reiner, A. & Karten, H.J. (1978). A bisynaptic retinocerebellar pathway in the turtle. Brain Research 150, 163169.
Resibois, A. & Rogers, J.H. (1992). Calretinin in rat brain: An immunohistochemical study. Neuroscience 46, 101134.
Robinson, D.A. (1976). Adaptive gain control of vestibuloocular reflex by the cerebellum. Journal of Neurophysiology 39, 954969.
Rogers, J.H. & Resibois, A. (1992). Calretinin and calbindin-D28k in rat brain: Patterns of partial co-localization. Neuroscience 51, 843865.
Ruigrok, T.J., Osse, R.J. & Voogd, J. (1992). Organization of inferior olivary projections to the flocculus and ventral paraflocculus of the rat cerebellum. Journal of Comparative Neurology 316, 129150.
Schwaller, B., Meyer, M. & Schiffmann, S. (2002). ‘New’ functions for ‘old’ proteins: The role of the calcium-binding proteins calbindin D-28k, calretinin and parvalbumin, in cerebellar physiology. Studies with knockout mice. Cerebellum 1, 241258.
Simpson, J., Graf, W. & Leonard, C. (1981). The coordinate system of visual climbing fibres to the flocculus. In Progress in Oculomotor Research. pp. 475485. Amsterdam/New York/Oxford: Elsevier/North Holland.
Simpson, J.I. (1984). The accessory optic system. Annual Review of Neuroscience 7, 1341.
Van Brederode, J.F., Mulligan, K.A. & Hendrickson, A.E. (1990). Calcium-binding proteins as markers for subpopulations of GABAergic neurons in monkey striate cortex. Journal of Comparative Neurology 298, 122.
Van der Steen, J., Simpson, J.I. & Tan, J. (1994). Functional and anatomic organization of three-dimensional eye movements in rabbit cerebellar flocculus. Journal of Neurophysiology 72, 3146.
Waespe, W., Cohen, B. & Raphan, T. (1983). Role of the flocculus and paraflocculus in optokinetic nystagmus and visual-vestibular interactions: Effects of lesions. Experimental Brain Research 50, 933.
Wild, J.M., Williams, M.N., Howie, G.J. & Mooney, R. (2005). Calcium-binding proteins define interneurons in HVC of the zebra finch (Taeniopygia guttata). Journal of Comparative Neurology 483, 7690.
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, 175182.
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, 12661277.
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, 6378.
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, 127139.
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, 502513.
Wylie, D.R., Bischof, W.F. & Frost, B.J. (1998). Common reference frame for neural coding of translational and rotational optic flow. Nature 392, 278282.
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, 327336.
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, 229232.
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, 26472659.
Wylie, D.R. & Frost, B.J. (1999 a). Complex spike activity of Purkinje cells in the ventral uvula and nodulus of pigeons in response to translational optic flow. Journal of Neurophysiology 81, 256266.
Wylie, D.R. & Frost, B.J. (1999 b). Responses of neurons in the nucleus of the basal optic root to translational and rotational flowfields. Journal of Neurophysiology 81, 267276.
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, 26322646.
Wylie, D.R., Lau, K.L., Lu, X., Glover, R.G. & Valsangkar-Smyth, M. (1999 a). Projections of Purkinje cells in the translation and rotation zones of the vestibulocerebellum in pigeon (Columba livia). Journal of Comparative Neurology 413, 480493.
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 Letters 219, 8386.
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, 517536.
Wylie, D.R., Pakan, J.M., Elliott, C.A., Graham, D.J. & Iwaniuk, A.N. (2007). 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. Visual Neuroscience 24, 691707.
Wylie, D.R., Winship, I.R. & Glover, R.G. (1999 b). Projections from the medial column of the inferior olive to different classes of rotation-sensitive Purkinje cells in the flocculus of pigeons. Neuroscience Letters 268, 97100.
Yamaguchi, T., Winsky, L. & Jacobowitz, D.M. (1991). Calretinin, a neuronal calcium binding protein, inhibits phosphorylation of a 39 kDa synaptic membrane protein from rat brain cerebral cortex. Neuroscience Letters 131, 7982.
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, 878899.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Visual Neuroscience
  • ISSN: 0952-5238
  • EISSN: 1469-8714
  • URL: /core/journals/visual-neuroscience
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed