Hostname: page-component-7dd5485656-npwhs Total loading time: 0 Render date: 2025-10-29T22:32:33.750Z Has data issue: false hasContentIssue false
  • English
  • Français

Monocular enucleation reduces immunoreactivity to the calcium-binding protein calbindin 28 kD in the Rhesus monkey lateral geniculate nucleus

Published online by Cambridge University Press:  02 June 2009

R. Ranney Mize ,
Qian Luo  and
Margarete Tigges
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
Margarete Tigges
Affiliation:
Yerkes Regional Primate Research Center and Departments of Anatomy and Cell Biology and Ophthalmology, Emory University, Atlanta
Get access Rights & Permissions [Opens in a new window]

Abstract

The calcium-binding proteins calbindin (CaBP) and parvalbumin (PV) are important in regulating intracellular calcium in brain cells. PV immunoreactivity is reduced by enucleation in the lateral geniculate nucleus (LGN) and by enucleation and visual deprivation in the striate cortex of adult monkeys. The effects of enucleation and visual deprivation on CaBP immunoreactivity in the LGN are not known. We therefore have studied cells and neuropil in the LGN that are labeled by antibodies to CaBP in normal and visually deprived Rhesus monkeys to determine if there is an effect on this calcium-binding protein. One group of monkeys had one eye removed 2 weeks to 4.3 years before sacrifice. A second group had one eye occluded with opaque lenses from infancy without enucleation. A final group had one eye occluded long-term followed by short-term enucleation 2 weeks before sacrifice.

In normal monkeys, CaBP-immunoreactive neurons were found throughout the LGN. They were sparsely distributed within the six main laminae, and more densely distributed within layer S and the interlaminar zones (ILZ). The labeled ILZ neurons had a distinct morphology, with fusiform somata and elaborate dendritic trees that were confined primarily to the ILZ. Most CaBP-labeled neurons in the main layers had dendrites that radiated in all directions from the soma. ILZ and main layer cells labeled by CaBP thus probably represent two different cell types.

Monocular enucleation with or without occlusion produced a significant reduction in antibody labeling in the deafferented laminae. Field measures revealed an average 11.5% reduction in optical density in each deafferented lamina compared to its adjacent, nondeprived layer. The differences in field optical density between deprived and nondeprived layers were statistically significant. CaBP neurons were still visible, but the optical density of antibody labeling in these cells also was reduced. Occlusion without enucleation had no effect. Thus, deafferentation, but not light deprivation, reduces concentrations of CaBP in monkey LGN. This effect is different than that seen in striate cortex of adult monkeys, where visual deprivation as well as enucleation alters CaBP immunoreactivity.

Keywords

CalciumImmunocytochemistryVisual pathwaysEnucleationOcclusion

Information

Type
Research Articles
Information
Visual Neuroscience , Volume 9 , Issue 5 , November 1992 , pp. 471 - 482
Copyright
Copyright © Cambridge University Press 1992

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.)

Article purchase

Temporarily unavailable

References

Baimbridoe, K.G. & Miller, J.J. (1982). Immunohistochemical localization of calcium-binding protein in the cerebellum, hippocampal formation, and olfactory bulb of 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. (1992). The calcium-binding protein calbindin-D 28K labels relay and GABAergic neurons in the cat lateral geniculate nucleus. Journal of Neurocytology (submitted).Google Scholar
Benevento, L.A. & Yoshida, K. (1981). The afferent and efferent organization of the lateral geniculo-prestriate pathways in the Macaque monkey. Journal of Comparative Neurology 203, 456–474.Google 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., Baier, W., Scharer, L., Gregersen, H.J., De Viragh, P.A. & Norman, A.W. (1990). Monoclonal antibodies directed against the calcium binding protein Calbindin-D 28 K. Cell Calcium 11, 599–602.CrossRefGoogle Scholar
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.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 S3, 513–520.Google ScholarPubMed
Demeulemeester, H., Vandesande, F., Orban, G.A., Heizmann, C.W. & Pochet, R. (1989). Calbindin D-28k & 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
Dineen, J.T., Hendrickson, A. & Keating, E.G. (1982). Alterations of retinal inputs following striate cortex removal in adult monkey. Experimental Brain Research 47, 446–456.CrossRefGoogle ScholarPubMed
Feldman, S.C. & Christakos, S. (1983). Vitamin D dependent calciumbinding protein in rat brain: Biochemical and immunocytochemical characterization. Endocrinology 112, 290–302.CrossRefGoogle ScholarPubMed
Fernandes, A., Tigges, M., Tigges, J., Gammon, J.A. & Chandler, C. (1988). Management of extended-wear contact lenses in infant Rhesus monkeys. Behavior Research Methods, Instruments, and Computers 20, 11–17.CrossRefGoogle Scholar
Heizmann, C.W. & Berchtold, M.W. (1987). Expression of parvalbumin and other Ca2+ binding proteins in normal & 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
Hendrickson, A.E., Ogren, M.P., Vaughn, J.E., Barber, R.P. & Wu, J.Y. (1983). Light and electron microscopic immunocytochemical localization of gamma-aminobutyric acid decarboxylase in the monkey geniculate nucleus: Evidence for GABAergic neurons and synapses. Journal of Neuroscience 3, 1245–1262.CrossRefGoogle ScholarPubMed
Hendry, S.H.C. (1991). Delayed reduction in GABA and GAD immunoreactivity of neurons in the adult monkey lateral geniculate nucleus following monocular deprivation or enucleation. Experimental Brain Research 86, 47–59.CrossRefGoogle ScholarPubMed
Hendry, S.H.C. & Carder, R. (1992). Organization of 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., pp. 477–502. Amsterdam: Elsevier Science Publishers.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Hendry, S.H.C., 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.CrossRefGoogle ScholarPubMed
Irvin, G.E., Norton, T.T., Sesma, M.A. & Casagrande, V.A. (1986). W-like response properties of interlaminar zone cells in the lateral geniculate nucleus of a primate (Galago crassicaudatus). Brain Research 362, 254–270.CrossRefGoogle ScholarPubMed
Iuvone, P.M., Tigges, M., Stone, R.A., Lambert, S. & Laties, 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
Jande, S.S., Maler, L. & Lawson, D.E.M. (1981). Immunohistochemical mapping of vitamin D-dependent calcium-binding protein in brain. Nature 294, 765–767.CrossRefGoogle ScholarPubMed
Jones, E.G. & Hendry, S.H.C. (1989). Differential calcium-binding protein immunoreactivity distinguishes classes of relay neurons in monkey thalamic nuclei. European Journal of Neuroscience 1, 222–246.CrossRefGoogle ScholarPubMed
Luo, X.G., Kong, X.Y. & Wong-Riley, M.T.T. (1991). 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
Mize, R.R. (1989). The analysis of immunohistochemical data. In Computer Techniques in Neuroanatomy, ed. Capowski, J.J., pp. 333–372. New York: Plenum Press.CrossRefGoogle Scholar
Norton, T.T. & Casagrande, V.A. (1982). Laminar organization of receptive-field properties in the lateral geniculate nucleus of the bush baby (Galago crassicaudatus). Journal of Neurophysiology 47, 715–741.CrossRefGoogle ScholarPubMed
Saini, K.D. & Garey, L.J. (1981). Morphology of neurons in the lateral geniculate nucleus of the monkey. A Golgi study. Experimental Brain Research 42, 235–248.Google ScholarPubMed
Sherman, S.M. & Spear, P.D. (1982). Organization of visual pathways in normal and visually deprived cats. Physiological Review 62, 738–855.CrossRefGoogle ScholarPubMed
Tigges, M., Boothe, R.G., Tigges, J. & Wilson, J.R. (1992). Competition between an aphakic and an occluded eye for territory in striate cortex of developing Rhesus monkeys: Cytochrome oxidase histochemistry in layer 4C. Journal of Comparative Neurology 316, 173–186.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Wasserman, R.H. & Fullmer, C.S. (1982). Vitamin D-induced calciumbinding 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
Wilson, J.R. & Hendrickson, A.E. (1981). Neuronal and synaptic structure of the dorsal lateral geniculate nucleus in normal and monocularly deprived Macaca monkeys. Journal of Comparative Neurology 197, 513–539.Google ScholarPubMed
Yoshida, K. & Benevento, L.A. (1981). The projection from the dorsal lateral geniculate nucleus of the thalamus to the extrastriate visual association cortex in the macaque monkey. Neuroscience Letters 22, 103–108.CrossRefGoogle Scholar