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Expression of calcium-binding proteins in cerebellar- and inferior olivary-projecting neurons in the nucleus lentiformis mesencephali of pigeons

Published online by Cambridge University Press:  01 May 2009

ANDREW N. IWANIUK ,
JANELLE M.P. PAKAN ,
CRISTIÁN GUTIÉRREZ-IBÁÑEZ  and
DOUGLAS R. WYLIE
ANDREW N. IWANIUK
Affiliation:
Canadian Centre for Behavioural Neuroscience, University of Lethbridge, Lethbridge, Alberta, Canada
JANELLE M.P. PAKAN
Affiliation:
Department of Neuroscience, Centre for Neuroscience, University of Alberta, Edmonton, Alberta, Canada
CRISTIÁN GUTIÉRREZ-IBÁÑEZ
Affiliation:
Department of Neuroscience, Centre for Neuroscience, University of Alberta, Edmonton, Alberta, Canada
DOUGLAS R. WYLIE*
Affiliation:
Department of Neuroscience, Centre for Neuroscience, University of Alberta, Edmonton, Alberta, Canada
*
*Address correspondence and reprint requests to: Douglas R. Wylie, Department of Psychology, University of Alberta, Edmonton, Alberta, Canada T6G 2E9. E-mail: [email protected]
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Abstract

In the avian brain, the optokinetic response is controlled by two retinal-recipient nuclei: the nucleus of the basal optic root (nBOR) of the accessory optic system and the pretectal nucleus lentiformis mesencephali (LM). Although considered sister nuclei because of their similar response properties and function, there are both similarities and differences with respect to efferent projections and neurochemistry. Both nBOR and LM project to the cerebellum (Cb) directly as mossy fibers but also indirectly via the inferior olive (IO). In a previous report, we showed that the cerebellar- and inferior olivary-projecting neurons in nBOR of pigeons differentially express the calcium-binding proteins calretinin (CR) and parvalbumin (PV). Both CR and PV are expressed in the somata of LM neurons, although the latter is not as prevalent, and whether expression of CR and PV reflects cerebellar and IO projections is not known. In this report, by combining retrograde neuronal tracing from the Cb and IO with fluorescent immunohistochemistry, we examined the expression of these calcium-binding proteins in the pigeon LM. Half (52%) of the cerebellar-projecting neurons were CR+ve, but only 15% were PV+ve. Almost all (>95%) these PV+ve cells also expressed CR. In contrast, few of the IO-projecting neurons expressed CR or PV (≤5%). This is strikingly similar to what we observed in nBOR and reveals that calcium-binding protein expression is concordant with projection patterns in two nuclei that share similar functions.

Keywords

CalretininParvalbuminPretectumCerebellumInferior oliveOptokinetic
Type
Brief Communication
Information
Visual Neuroscience , Volume 26 , Issue 3 , May 2009 , pp. 341 - 347
Copyright
Copyright © Cambridge University Press 2009

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References

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. The 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. The 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
Cardozo, B.N., Buijs, R. & Van der Want, J. (1991). Glutamate-like immunoreactivity in retinal terminals in the nucleus of the optic tract in rabbits. The Journal of Comparative Neurology 309, 261–270.CrossRefGoogle ScholarPubMed
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. The 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. The 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. The Journal of Comparative Neurology 397, 149–162.3.0.CO;2-0>CrossRefGoogle ScholarPubMed
D’Orlando, C., Celio, M.R. & Schwaller, B. (2002). Calretinin and calbindin D-28k, but not parvalbumin protect against glutamate-induced delayed excitotoxicity in transfected N18-RE 105 neuroblastoma-retina hybrid cells. Brain Research 945, 181–190.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Fite, K.V., Reiner, A. & Hunt, S.P. (1979). Optokinetic nystagmus and the accessory optic system of pigeon and turtle. Brain, Behavior and Evolution 16, 192–202.CrossRefGoogle ScholarPubMed
Gall, D., Roussel, C., Susa, I., D’Angelo, E., Rossi, P., Bearzatto, B., Galas, M.C., Blum, D., Schurmans, S. & Schiffmann, S.N. (2003). Altered neuronal excitability in cerebellar granule cells of mice lacking calretinin. The Journal of Neuroscience 23, 9320–9327.CrossRefGoogle ScholarPubMed
Gamlin, P.D. (2006). The pretectum: Connections and oculomotor-related roles. Progress in Brain Research 151, 379–405.CrossRefGoogle ScholarPubMed
Gamlin, P.D. & Cohen, D.H. (1988 a). Retinal projections to the pretectum in the pigeon (Columba livia). The Journal of Comparative Neurology 269, 1–17.CrossRefGoogle Scholar
Gamlin, P.D. & Cohen, D.H. (1988 b). Projections of the retinorecipient pretectal nuclei in the pigeon (Columba livia). The Journal of Comparative Neurology 269, 18–46.CrossRefGoogle ScholarPubMed
Gioanni, H., Rey, J., Villalobos, J., Richard, D. & Dalbera, A. (1983 a). 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 ScholarPubMed
Gioanni, H., Villalobos, J., Rey, J. & Dalbera, A. (1983 b). 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
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. The Journal of Comparative Neurology 248, 133–145.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
Karten, H. & Hodos, W. (1967). A Stereotaxic Atlas of the Brain of the Pigeon (Columba livia). Baltimore, MD: Johns Hopkins Press.Google 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
McKenna, O.C. & Wallman, J. (1985 a). Accessory optic system and pretectum of birds: Comparisons with those of other vertebrates. Brain, Behavior and Evolution 26, 91–116.CrossRefGoogle ScholarPubMed
McKenna, O.C. & Wallman, J. (1985 b). Functional postnatal changes in avian brain regions responsive to retinal slip: A 2-deoxy-D-glucose study. The Journal of Neuroscience 5, 330–342.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
Nakayama, K. (1985). Biological image motion processing: A review. Vision Research 25, 625–660.CrossRefGoogle ScholarPubMed
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. The Journal of Comparative Neurology 495, 84–99.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). The 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
Resibois, A. & Rogers, J.H. (1992). Calretinin in rat brain: An immunohistochemical study. Neuroscience 46, 101–134.CrossRefGoogle Scholar
Schwaller, B. (2007). Emerging functions of the “Ca2+ buffers” parvalbumin, calbindin D-28k and calretinin in the brain. In Handbook of Neurochemistry and Molecular Neurobiology. Neural Protein Metabolism and Function, Vol. 7, eds. Lajtha, A. & Banik, N., pp. 197–222. New York: Springer.CrossRefGoogle Scholar
Schwaller, B. (2009). The continuing disappearance of “pure” Ca2+ buffers. Cellular and Molecular Life Sciences 66, 275–300.CrossRefGoogle ScholarPubMed
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.I. (1984). The accessory optic system. Annual Review of Neuroscience 7, 13–41.CrossRefGoogle ScholarPubMed
Simpson, J.I., Giolli, R.A. & Blanks, R.H. (1988). The pretectal nuclear complex and the accessory optic system. Reviews of Oculomotor Research 2, 335–364.Google 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. The Journal of Comparative Neurology 298, 1–22.CrossRefGoogle ScholarPubMed
Waespe, W. & Henn, V. (1987). Gaze stabilization in the primate. The interaction of the vestibulo-ocular reflex, optokinetic nystagmus, and smooth pursuit. Reviews of Physiology, Biochemistry and Pharmacology 106, 37–125.CrossRefGoogle ScholarPubMed
Weber, J.T. (1985). Prefectal complex and accessory optic system of primates. Brain Behaviour and Evolution 26, 117–140.CrossRefGoogle Scholar
Westheimer, G. & McKee, S.P. (1975). Visual acuity in the presence of retinal-image motion. Journal of Optical Society of America 65, 847–850.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). The Journal of Comparative Neurology 483, 76–90.CrossRefGoogle ScholarPubMed
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. The Journal of Comparative Neurology 456, 127–139.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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). The Journal of Comparative Neurology 429, 502–513.3.0.CO;2-E>CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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. The Journal of Comparative Neurology 384, 517–536.3.0.CO;2-5>CrossRefGoogle ScholarPubMed
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 Letters 268, 97–100.CrossRefGoogle ScholarPubMed
Wylie, D.R.W., Glover, R.G. & Lau, K.L. (1998). Projections from the accessory optic system and pretectum to the dorsolateral thalamus in the pigeon (Columba livia): A study using both anterograde and retrograde tracers. The Journal of Comparative Neurology 391, 456–469.3.0.CO;2-#>CrossRefGoogle Scholar
Wylie, D.R.W., Ogilvie, C.J., Crowder, N.A., Barkley, R.R. & Winship, I.R. (2005). Telencephalic projections to the nucleus of the basal optic root and pretectal nucleus lentiformis mesencephali in pigeons. Visual Neuroscience 22, 237–247.CrossRefGoogle Scholar
Wylie, D.R.W., Pakan, J.M.P., Gutierrez-Ibanez, C. & Iwaniuk, A.N. (2008). Expression of calcium-binding proteins in pathways from the nucleus of the basal optic root to the cerebellum in pigeons. Visual Neuroscience 25, 1–7.CrossRefGoogle Scholar
Wylie, D.R.W., Pakan, J.P., 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.W., Winship, I. & 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 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
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.CrossRefGoogle ScholarPubMed