Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-10T21:46:42.980Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  01 September 2008

DOUGLAS R.W. WYLIE ,
JANELLE M.P. PAKAN ,
CRISTIÁN GUTIÉRREZ-IBÁÑEZ  and
ANDREW N. IWANIUK
DOUGLAS R.W. WYLIE*
Affiliation:
Centre for Neuroscience, University of Alberta, Edmonton, Alberta, Canada
JANELLE M.P. PAKAN
Affiliation:
Centre for Neuroscience, University of Alberta, Edmonton, Alberta, Canada
CRISTIÁN GUTIÉRREZ-IBÁÑEZ
Affiliation:
Centre for Neuroscience, University of Alberta, Edmonton, Alberta, Canada
ANDREW N. IWANIUK
Affiliation:
Canadian Centre for Behavioural Neuroscience, Lethbridge University, Lethbridge, Alberta, Canada
*
*Address correspondence and reprint requests to: Douglas R. Wong-Wylie, Department of Psychology, University of Alberta, Edmonton, Alberta, Canada T6G 2E9. E-mail: dwylie@ualberta.ca
Get access Rights & Permissions [Opens in a new window]

Abstract

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.

Keywords

CalretininParvalbuminPretectumCerebellumInferior oliveOptokinetic
Type
Brief Communications
Information
Visual Neuroscience , Volume 25 , Issue 5-6 , September 2008 , pp. 701 - 707
Copyright
Copyright © Cambridge University Press 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

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, 582–589.CrossRefGoogle Scholar
Arends, J. & Voogd, J. (1989). Topographic aspects of the olivocerebellar system in the pigeon. Experimental Brain Research Series 17, 52–57.Google Scholar
Baimbridge, K.G., Celio, M.R. & Rogers, J.H. (1992). Calcium-binding proteins in the nervous system. Trends in Neurosciences 15, 303–308.CrossRefGoogle ScholarPubMed
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, 417–432.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Celio, M.R. (1990). Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35, 375–475.CrossRefGoogle ScholarPubMed
Clarke, P.G. (1977). Some visual and other connections to the cerebellum of the pigeon. Journal of Comparative Neurology 174, 535–552.CrossRefGoogle Scholar
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, 87–95.3.0.CO;2-W>CrossRefGoogle ScholarPubMed
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, 149–162.3.0.CO;2-0>CrossRefGoogle ScholarPubMed
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, 1–19.CrossRefGoogle ScholarPubMed
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, 268–296.CrossRefGoogle ScholarPubMed
Finger, T.E. & Karten, H.J. (1978). The accessory optic system in teleosts. Brain Research 153, 144–149.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Friedman, M.B. (1975). Visual control of head movements during avian locomotion. Nature 255, 67–69.CrossRefGoogle ScholarPubMed
Frost, B. (1978). The optokinetic basis of head-bobbing in the pigeon. Journal of Experimental Biology 74, 187–195.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 248–258.Google ScholarPubMed
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, 407–440.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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, 125–130.CrossRefGoogle ScholarPubMed
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, 348–355.CrossRefGoogle Scholar
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, 139–175.CrossRefGoogle ScholarPubMed
Ito, M., Orlov, I. & Yamamoto, M. (1982). Topographical representation of vestibulo-ocular reflexes in rabbit cerebellar flocculus. Neuroscience 7, 1657–1664.CrossRefGoogle ScholarPubMed
Karten, H. & Hodos, W. (1967). A Stereotaxic Atlas of the Brain of the Pigeon (Columba livia). Baltimore, MD: Johns Hopkins Press.Google Scholar
Karten, H.J. & Shimizu, T. (1989). The origins of neocortex: Connections and lamination as distinct events in evolution. Journal of Cognitive Neuroscience 1, 290–301.CrossRefGoogle ScholarPubMed
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, 1753–1756.CrossRefGoogle ScholarPubMed
Kawasaki, T. & Sato, Y. (1980). Afferent projection from the dorsal nucleus of the raphe to the flocculus in cats. Brain Research 197, 496–502.CrossRefGoogle Scholar
Kohr, G., Lambert, C.E. & Mody, I. (1991). Calbindin-D28K (CaBP) levels and calcium currents in acutely dissociated epileptic neurons. Experimental Brain Research 85, 543–551.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 2073–2090.CrossRefGoogle ScholarPubMed
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, 41–52.CrossRefGoogle ScholarPubMed
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, 1140–1153.CrossRefGoogle ScholarPubMed
Medina, L. & Reiner, A. (2000). Do birds possess homologues of mammalian primary visual, somatosensory and motor cortices? Trends in Neurosciences 23, 1–12.CrossRefGoogle ScholarPubMed
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. 223–254. New York: Plenum Press.Google Scholar
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, 45–57.Google ScholarPubMed
Mizuno, N., Mochizuki, K., Akimoto, C. & Matsushima, R. (1973). Pretectal projections to the inferior olive in the rabbit. Experimental Neurology 39, 498–506.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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, 1315–1318.CrossRefGoogle ScholarPubMed
Pritz, M.B. & Siadati, A. (1999). Calcium binding protein immunoreactivity in nucleus rotundus in a reptile, Caiman crocodilus. Brain, Behavior and Evolution 53, 277–287.CrossRefGoogle 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.CrossRefGoogle Scholar
Reiner, A. & Karten, H.J. (1978). A bisynaptic retinocerebellar pathway in the turtle. Brain Research 150, 163–169.CrossRefGoogle ScholarPubMed
Resibois, A. & Rogers, J.H. (1992). Calretinin in rat brain: An immunohistochemical study. Neuroscience 46, 101–134.CrossRefGoogle Scholar
Robinson, D.A. (1976). Adaptive gain control of vestibuloocular reflex by the cerebellum. Journal of Neurophysiology 39, 954–969.CrossRefGoogle ScholarPubMed
Rogers, J.H. & Resibois, A. (1992). Calretinin and calbindin-D28k in rat brain: Patterns of partial co-localization. Neuroscience 51, 843–865.CrossRefGoogle ScholarPubMed
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, 129–150.CrossRefGoogle Scholar
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, 241–258.CrossRefGoogle ScholarPubMed
Simpson, J., Graf, W. & Leonard, C. (1981). The coordinate system of visual climbing fibres to the flocculus. In Progress in Oculomotor Research. pp. 475–485. Amsterdam/New York/Oxford: Elsevier/North Holland.Google Scholar
Simpson, J.I. (1984). The accessory optic system. Annual Review of Neuroscience 7, 13–41.CrossRefGoogle ScholarPubMed
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, 1–22.CrossRefGoogle ScholarPubMed
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, 31–46.CrossRefGoogle ScholarPubMed
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, 9–33.CrossRefGoogle ScholarPubMed
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, 76–90.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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, 502–513.3.0.CO;2-E>CrossRefGoogle Scholar
Wylie, D.R., Bischof, W.F. & Frost, B.J. (1998). Common reference frame for neural coding of translational and rotational optic flow. Nature 392, 278–282.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 256–266.CrossRefGoogle ScholarPubMed
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, 267–276.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 480–493.3.0.CO;2-J>CrossRefGoogle ScholarPubMed
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, 83–86.CrossRefGoogle 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, 517–536.3.0.CO;2-5>CrossRefGoogle ScholarPubMed
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, 691–707.CrossRefGoogle ScholarPubMed
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, 97–100.CrossRefGoogle ScholarPubMed
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, 79–82.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed