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Visual deprivation fails to reduce calbindin 28kD or GABA immunoreactivity in the Rhesus monkey superior colliculus

Published online by Cambridge University Press:  02 June 2009

R. Ranney Mize  and
Qian Luo
R. Ranney Mize
Affiliation:
Department of Anatomy and Neurobiology, College of Medicine, University of Tennessee, The Health Science Center, Memphis
Qian Luo
Affiliation:
Department of Anatomy and Neurobiology, College of Medicine, University of Tennessee, The Health Science Center, Memphis
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Abstract

Antibody labeling of the calcium-binding protein calbindin 28kD (CaBP) and gamma-aminobutyric acid (GABA) is altered by short-term monocular deprivation in the lateral geniculate nucleus and visual cortex of adult primates. It is not known whether these alterations occur in other subcortical visual structures. We therefore have examined antibody labeling to CaBP and GABA in the superior colliculus (SC) of visually deprived Rhesus monkeys. One group was monocularly enucleated as adults. The other monkeys experienced different types of monocular and binocular deprivation from birth, including occlusion of one eye, and/or surgically induced aphakia, optically corrected with extended-wear contact lenses, or an intraocular lens implant. Some of these monkeys also had one eye enucleated prior to perfusion.

In the SC of normal monkeys, CaBP-immunoreactive neurons formed three laminar tiers within SC, one within the zonal layer (ZL) and upper superficial gray layer (SGL), another bridging the optic and intermediate gray layers, and a third within the deep gray layer. CaBP neurons within the upper tier had small pyriform or stellate morphologies while those in the deeper tiers were slightly larger neurons, most with a stellate morphology. GABA-immunoreactive neurons were densely distributed within the SGL and more sparsely distributed within the deeper layers. These cells were mostly small neurons with horizontal, pyriform, or stellate morphologies.

Neither monocular enucleation nor occlusion nor aphakia combined with continuous occlusion of the fellow eye produced any visible reduction in antibody labeling in cells or neuropil within the SC. Full-field measures of labeling intensity (optical density) within the ZL and upper SGL revealed no consistent differences between the SC contralateral or ipsilateral to the affected eye in either CaBP- or GABA-labeled sections. Measures of the optical density, number, and size of labeled neurons also showed no consistent effects of enucleation and/or occlusion. We therefore conclude that the retino-geniculostriate and retino-collicular systems differ in their response to deprivation which is likely due to the significant overlap of retinal axons from the two eyes that occurs in the SC of the Rhesus monkey.

Keywords

CalciumlmmunocytochemistryVisual pathwaysInterneuronsEnucleationOcclusionInhibition
Type
Research Articles
Information
Visual Neuroscience , Volume 9 , Issue 2 , August 1992 , pp. 157 - 168
Copyright
Copyright © Cambridge University Press 1992

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References

Baimbridge, K.G. & Miller, J.J. (1982). Immunohistochemical localization of calcium-binding protein in the cerebellum, hippocampal formation, and olfactory bulb o f the rat. Brain Research 245, 223–229.CrossRefGoogle Scholar
Baimbridge, K.G., Miller, J.J. & Parkes, C.O. (1982). Calcium-binding protein distribution in the rat brain. Brain Research 239, 519–525.CrossRefGoogle ScholarPubMed
Banfro, F. & Mize, R.R. (1991). Calbindin antibodies label specific cell classes in the cat lateral geniculate nucleus. Society for Neuroscience Abstracts 17, 628.Google Scholar
Bear, M.F., Schmechel, D.E. & Ebner, F.F. (1985). Glutamic acid decarboxylase in the striate cortex of normal and monocularly deprived kittens. Journal of Neuroscience 5, 1262–1275.CrossRefGoogle ScholarPubMed
Benson, D.L., Isackson, P.J., Hendry, S.H.C. & Jones, E.G. (1989). Expression of glutamic acid decarboxylase mRNA in normal and monocularly deprived cat visual cortex. Molecular Brain Research 5, 279–287.CrossRefGoogle ScholarPubMed
Berman, N. & Sterling, P. (1976). Cortical suppression of the retinocollicular pathway in the monocularly deprived cat. Journal of Physiology (London) 255, 263–273.CrossRefGoogle ScholarPubMed
Bronner, F., Pansu, D. & Stein, W.D. (1986). Analysis of calcium transport in rat intestine. Advances in Experimental Medicine and Biology 208, 227–234.CrossRefGoogle ScholarPubMed
Celio, M.R. (1990). Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35, 375–475.Google Scholar
Cowan, R., Wilson, C. & Emson, P. (1990). Parvalbumin containing Gabaergic interneurons in the rat neostriatum. Journal of Comparative Neurology 302, 197–205.CrossRefGoogle ScholarPubMed
Cynader, M. & Berman, N. (1972). Receptive-field organization of monkey superior colliculus. Journal of Neurophysiology 35, 187–201.CrossRefGoogle ScholarPubMed
Defelipe, J., Hendry, S.H.C. & Jones, E.G. (1989). Synapses of double bouquet cells in monkey cerebral cortex visualized by calbindin immunoreactivity. Brain Research 503, 49–54.Google Scholar
Demeulemeester, H., Vandesande, F., Orban, G.A., Heizmann, C.W. & Pochet, R. (1989). Calbindin D-28K and parvalbumin immunoreactivity is confined to two separate neuronal subpopulations in the cat visual cortex, whereas partial coexistence is shown in the dorsal lateral geniculate nucleus. Neuroscience Letters 99, 6–11.CrossRefGoogle ScholarPubMed
Demeulemeester, H., Arckens, L., Vandesande, F., Orban, G.A., Heizmann, C.W. & Pochet, R. (1991). Calcium binding proteins as molecular markers for cat geniculate neurons. Experimental Brain Research 83, 513–520.CrossRefGoogle ScholarPubMed
Difiglia, M., Christakos, S. & Aronin, N. (1989). Ultrastructural localization of immunoreactive calbindin-D28K in the rat and monkey basal ganglia, including subcellular distribution with colloidal gold labeling. Journal of Comparative Neurology 279, 653–665.Google Scholar
Ficalora, A.N. & Mize, R.R. (1989). The neurons of the substantia nigra and zona incerta which project to the cat superior colliculus are GABA immunoreactive: A double-label study using GABA immunocytochemistry and lectin retrograde transport. Neuroscience 29, 567–581.Google Scholar
Fonnum, F., Lund Karlsen, R., Malthe-Sorenssen, D., Skrede, K. & Walaas, I. (1979). Localization of neurotransmitters, particularly glutamate, in hippocampus, septum, nucleus accumbens, and superior colliculus. Progress in Brain Research 51, 167–191.CrossRefGoogle ScholarPubMed
Goldberg, M.E. & Wurtz, R.H. (1972). Activity of superior colliculus in behaving monkey. I. Visual receptive fields of single neurons. Journal of Neurophysiology 35, 542–559.Google Scholar
Graybiel, A.M. (1975). Anatomical organization of retinotectal afferents in the cat: An autoradiographic study. Brain Research 96, 1–23.Google Scholar
Graybiel, A.M. (1976). Evidence for banding of the cat's ipsilateral retinotectal connections. Brain Research 114, 318–327.Google Scholar
Heizmann, C.W. & Berchtold, M.W. (1987). Expression of parvalbumin and other Ca2+ binding proteins in normal and tumor cells: A topic review. Cell Calcium 8, 1–41.CrossRefGoogle Scholar
Heizmann, C.W. & Hunziker, W. (1990). Intracellular calcium-binding molecules. In Intracellular Calcium Regulation, ed. Bronner, F., pp. 211–248. New York: Alan R. Liss.Google Scholar
Hendry, S.H.C. (1991). Delayed reduction in GABA and GAD immunoreactivity of neurons in the adult monkey dorsal lateral geniculate nucleus following monocular deprivation or enucleation. Experimental Brain Research 86, 47–59.Google Scholar
Hendry, S.H.C. & Carder, R. (1992). Organization and plasticity of GABA neurons and receptors in monkey visual cortex. In GABA in the Retina and Central Visual System, ed. Mize, R.R., Marc, R. & Sillito, A., Amsterdam: Elsevier Science Publishers (in press).Google Scholar
Hendry, S.H.C. & Jones, E.G. (1986). Reduction in number of GABA immunostained neurons in deprived-eye dominance columns of monkey area 17. Nature 320, 750–753.Google Scholar
Hendry, S.H., Jones, E.G., Emson, P.C., Lawson, D.E., Heizmann, C.W. & Streit, P. (1989). Two classes of cortical GABA neurons defined by differential calcium binding protein immunoreactivities. Experimental Brain Research 76, 467–472.Google Scholar
Hikosaka, O. & Wurtz, R. H. (1985). Modification of saccadic eye movements by GABA-related substances. I. Effect of muscimol and bicuculline in monkey superior colliculus. Journal of Neurophysiology 53, 266–291.Google Scholar
Hoffmann, K.-P. & Sherman, S.M. (1974). Effects of early monocular deprivation on visual input to cat superior colliculus. Journal of Neurophysiology 37, 1267–1286.CrossRefGoogle ScholarPubMed
Houser, C.R., Lee, M. & Vaughn, J.E. (1983). Immunocytochemical localization of glutamic acid decarboxylase in normal and deafferented superior colliculus: Evidence for reorganization of gamma-aminobutyric acid synapses. Journal of Neuroscience 3, 2030–2042.Google Scholar
Hubel, D.H., Levay, S. & Wiesel, T.N. (1975). Mode of termination of retinotectal fibers in macaque monkey: An autoradiographic study. Brain Research 96, 25–40.Google Scholar
Huerta, M.F. & Harting, J.K. (1984). The mammalian superior colliculus: Studies of its morphology and connections. In Comparative Neurology of the Optic Tectum, ed. Vanegas, H., pp. 687–773. New York: Plenum Press.Google Scholar
Iuvone, P.M., Tigges, M., Stone, R.A., Lambert, S. & Lattes, A.M. (1991). Effects of apomorphine, a dopamine receptor agonist, on ocular refraction and axial elongation in a primate model of myopia. Investigative Ophthalmology and Visual Science 32, 1674–1677.Google Scholar
Luo, Q., Mize, R.R. & Tigges, M. (1991a). Anti-calbindin labeling in the lateral geniculate nucleus o f the Rhesus monkey and its reduction by enucleation. Neuroscience Abstracts 116, 108.Google Scholar
Luo, X.G., Kong, X.Y. & Wong-Riley, M.T.T. (1991b). Effect of monocular enucleation or impulse blockage on gamma-aminobutyric acid and cytochrome oxidase levels in neurons of the adult cat lateral geniculate nucleus. Visual Neuroscience 6, 55–68.CrossRefGoogle ScholarPubMed
Ma, T.P., Cheng, H.-W., Czech, J.A. & Rafols, J.A. (1990). Intermediate and deep layers of the macaque superior colliculus: A Golgi study. Journal of Comparative Neurology 295, 92–110.Google Scholar
Mize, R.R. (1985). Morphometric measurement using a computerized digitizing system. In The Microcomputer in Cell and Neurobiology Research, ed. Mize, R.R., pp. 177–215. New York: Elsevier.Google Scholar
Mize, R.R. (1988). Immunocytochemical localization o f gamma-aminobutyric acid (GABA) in the cat superior colliculus. Journal of Comparative Neurology 276, 169–187.Google Scholar
Mize, R.R. (1989a). Enkephalin-like immunoreactivity in the cat superior colliculus: distribution, ultrastructure, and co-localization with GABA. Journal of Comparative Neurology 285, 133–155.CrossRefGoogle Scholar
Mize, R.R. (1989b). The analysis of immunohistochemical data. In Computer Techniques in Neuroanatomy, ed. Capowski, J.J., pp. 333–372. New York: Plenum Press.Google Scholar
Mize, R.R. (1992). The organization of GABAergic neurons in the mammalian superior colliculus. In GABA in the Retina and Central Visual System, ed. Mize, R.R., Marc, R. & Sillito, A., Amsterdam: Elsevier Science Publishers (in press).Google Scholar
Mize, R.R. & Murphy, E.H. (1976). Alterations in receptive field properties of superior colliculus cells produced by visual cortex ablation in infant and adult cats. Journal of Comparative Neurology 168, 393–424.Google Scholar
Mize, R.R., Spencer, R.F. & Sterling, P. (1982). Two types of GABA-accumulating neurons in the superficial gray layer of the cat superior colliculus. Journal of Comparative Neurology 206, 180–192.Google Scholar
Mize, R.R., Jeon, C.-J., Hamada, O.L. & Spencer, R.F. (1991a). Organization of neurons labeled by antibodies to gamma-aminobutyric acid (GABA) in the superior colliculus of the Rhesus monkey. Visual Neuroscience 6, 75–92.CrossRefGoogle ScholarPubMed
Mize, R.R., Jeon, C.-J., Butler, G.D., Luo, Q. & Emson, P.C. (1991b). The calcium binding protein calbindin-D 28K reveals sub-populations of projection and interneurons in the cat superior colliculus. Journal of Comparative Neurology 307, 417–436.Google Scholar
Nabors, L.B. & Mize, R.R. (1991). A unique neuronal organization in the cat pretectum revealed by antibodies to the calcium-binding protein calbindin-D 28K. Journal of Neuroscience 11, 2460–2476.CrossRefGoogle Scholar
Okada, Y. (1974). Distribution of γ-aminobutyric acid (GABA) in the layers of superior colliculus of the rabbit. Brain Research 75, 362–365.Google Scholar
Pollack, J.C. & Hickey, T.L. (1979). The distribution of retino-collicular axon terminals in rhesus monkey. Journal of Comparative Neurology 185, 587–602.CrossRefGoogle ScholarPubMed
Rosenquist, A.C. & Palmer, L.A. (1971). Visual receptive field properties o f cells of the superior colliculus after cortical lesions in the cat. Experimental Neurology 33, 629–652.Google Scholar
Sandberg, M., Jacobson, I. & Hamberger, A. (1982). Release of endogenous amino acids in vitro from the superior colliculus and the hippocampus. Progress in Brain Research 55, 157–166.Google Scholar
Schiller, P.H. & Koerner, F. (1971). Discharge characteristics of single units in superior colliculus of the alert rhesus monkey. Journal of Neurophysiology 35, 920–936.CrossRefGoogle Scholar
Schiller, P.H., Stryker, M., Cynader, M. & Berman, N. (1974). Response characteristics o f single cells in the monkey superior colliculus following ablation or cooling o f visual cortex. Journal of Neurophysiology 37, 181–194.Google Scholar
Shatz, C. & Stryker, M.P. (1978). Ocular dominance in layer IV of the cat's visual cortex and the effects of monocular deprivation. Journal of Physiology (London) 281, 267–283.CrossRefGoogle ScholarPubMed
Sherman, S.M. & Spear, P.D. (1982). Organization of visual pathways in normal and visually deprived cats. Physiological Review 62, 738–855.Google Scholar
Tigges, M. & Tigges, J. (1991). Parvalbumin immunoreactivity of the lateral geniculate nucleus in adult Rhesus monkey after monocular eye enucleation. Visual Neuroscience 6, 375–382.Google Scholar
Van Brederode, J.F.M., 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
Wasserman, R.H. & Fullmer, C.S. (1982). Vitamin D-induced calcium binding protein. In Molecular Biology. An International Series of Monograph and Textbooks, ed. Cheung, W.Y.H., pp. 175–216. New York: Academic Press.Google Scholar
Wenthold, R.J., Zempel, J.M., Parakkal, M.H., Reeks, K.A. & Altshuler, R.A. (1986). Immunocytochemical localization of GABA in the cochlear nucleus of the guinea pig. Brain Research 380, 7–18.CrossRefGoogle ScholarPubMed
Wickelgren, B.G. & Sterling, P. (1969a). Influence of visual cortex on receptive fields in the superior colliculus of the cat. Journal of Neurophysiology 32, 16–23.CrossRefGoogle ScholarPubMed
Wickelgren, B.G. & Sterling, P. (1969b). Effects on the superior colliculus of cortical removal in visually deprived cats. Nature (London) 224, 1032–1033.Google Scholar