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Discrete reduction patterns of parvalbumin and calbindin D-28k immunoreactivity in the dorsal lateral geniculate nucleus and the striate cortex of adult macaque monkeys after monocular enucleation

Published online by Cambridge University Press:  02 June 2009

Ingmar Blümcke ,
Eduardo Weruaga ,
Sandor Kasas ,
Anita E. Hendrickson  and
Marco R. Celio
Ingmar Blümcke
Affiliation:
Institute of Histology and General Embryology, University of Fribourg, Rte. A. Gockel, CH-1705 Fribourg, Switzerland
Eduardo Weruaga
Affiliation:
Institute of Histology and General Embryology, University of Fribourg, Rte. A. Gockel, CH-1705 Fribourg, Switzerland
Sandor Kasas
Affiliation:
Institute of Histology and General Embryology, University of Fribourg, Rte. A. Gockel, CH-1705 Fribourg, Switzerland
Anita E. Hendrickson
Affiliation:
Department of Biological Structure and Ophthalmology, SM-20, University of Washington, Seattle
Marco R. Celio
Affiliation:
Institute of Histology and General Embryology, University of Fribourg, Rte. A. Gockel, CH-1705 Fribourg, Switzerland
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Abstract

We analyzed the immunohistochemical distribution of the two calcium-binding proteins, parvalbumin (PV) and calbindin D-28k (CB), in the primary visual cortex and lateral dorsal geniculate nucleus (dLGN) of monocularly enucleated macaque monkeys (Macaca fascicularis and Macaca nemestrind) in order to determine how the expression of PV and CB is affected by functional inactivity. The monkeys survived 1–17 weeks after monocular enucleation. The distribution pattern of each of the proteins was examined immunocytochemically using monoclonal antibodies and compared with that of the metabolic marker cytochrome oxidase (CO). We recorded manually the number of immunostained neurons and estimated the concentration of immunoreactive staining product using a computerized image-acquisition system. Our results indicate a decrease of approximately 30% in the labeling of PV-immunoreactive (ir) neuropil particularly in those layers of denervated ocular-dominance columns receiving the geniculocortical input. There was no change in the number of PV-ir neurons in any compartment irrespective of the enucleation interval. For CB-ir, we found a 20% decrease in the neuropil labeling in layer 2/3 of the denervated ocular-dominance columns. In addition, a subset of pyramidal CB-ir neurons in layers 2 and 4B, which are weakly stained in control animals, showed decreased labeling. In the dLGN of enucleated animals, PV-ir and CB-ir were decreased only in the neuropil of the denervated layers.

From these results, we conclude that cortical interneurons and geniculate projection neurons still express PV and CB in their cell bodies after disruption of the direct functional input from one eye. The only distinct decrease of PV and CB expression is seen in axon terminals from retinal ganglion cells in the dLGN, and in the axons and terminals of both geniculocortical projection cells and cortical interneurons in the cerebral cortex.

Keywords

Calcium-binding proteinsCytochrome oxidaseVisual deprivationNeuroanatomyPrimates
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 1 , January 1994 , pp. 1 - 11
Copyright
Copyright © Cambridge University Press 1994

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References

Andressen, C., I., Blümcke & Celio, M.R. (1993). Calcium-binding proteins: Selective markers of nerve cells. Cell and Tissue Research 271, 181–208.Google Scholar
Batmbridge, K.G., Celio, M.R. & Rogers, J.H. (1992). Calcium-binding proteins in the nervous system. Trends in Neuroscience 15, 303–308.Google Scholar
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
Blümcke, I., Hof, P.R., Morrison, J.H. & Celio, M.R. (1991). Parvalbumin in the monkey striate cortex: A quantitative immunoelec-tron-microscopy study. Brain Research 554, 237–243.CrossRefGoogle ScholarPubMed
Braun, K. (1990). Calcium-binding proteins in avian and mammalian central nervous system: Localization, development, and possible functions. Progress in Histochemistry and Cytochemistry 21, 1–64.CrossRefGoogle ScholarPubMed
Celio, M.R. (1986). Parvalbumin in most γ-aminobutyric acid-containing neurons of the rat cerebral cortex. Science 231, 995–997.Google Scholar
Celio, M.R. (1990). Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35, 375–475.CrossRefGoogle ScholarPubMed
Celio, M.R., Baier, W., Schärer, L., de Viragh, P.A. & Gerday, C (1988). Monoclonal antibodies directed against the calcium-binding protein parvalbumin. Cell Calcium 9, 81–86.CrossRefGoogle ScholarPubMed
Celio, M.R., Baier, W., Schärer, L., Gregersen, H.J., de Viragh, P.A. & Norman, A.W. (1990). Monoclonal antibodies directed against the calcium-binding protein calbindin D-28k. Cell Calcium 11, 599–602.Google Scholar
Celio, M.R., Schärer, L., Morrison, J.H., Norman, A.W. & Bloom, F.E. (1986). Calbindin immunoreactivity alternates with cytochrome C oxidase-rich zones in some layers of the primate visual cortex. Nature 323, 715–717.CrossRefGoogle ScholarPubMed
Cellerino, A., Sicillano, R., Domenici, L. & Maffei, L. (1992). Parvalbumin immunoreactivity: A reliable marker for the effects of monocular deprivation in the rat visual cortex. Letters to Neuroscience 51, 749–753.Google Scholar
Chard, P.S., Bleakman, D. & Miller, R.J. (1991). Parvalbumin is an intracellular Ca2+-buffering protein. Society of Neuroscience Abstracts 17, 343.Google Scholar
DeFelipe, J., Hendry, S.H.C. & Jones, E.G. (1989). Visualization of chandelier cell axons by parvalbumin immunoreactivity in monkey cerebral cortex. Proceedings National Academy of Sciences of the U.S.A. 86, 2093–2097.Google Scholar
DeFelipe, J., Hendry, S.H.C, Hashikawa, T., Molinari, M. & Jones, E.G. (1990). A microcolumnar structure of monkey cerebral cortex revealed by immunocytochemical studies of double bouquet cell axons. Neuroscience 37, 655–673.Google Scholar
DeFelipe, J. & Jones, E.G. (1991). Parvalbumin immunoreactivity reveals layer-IV of monkey cerebral cortex as a mosaic of micro-zones of thalamic afferent terminations. Brain Research 562, 39–47.Google Scholar
DeFelipe, J. & Jones, E.G. (1992). High-resolution light- and electron-microscopic immunocytochemistry of colocalized GABA and calbindin D-28k in somata and double bouquet cell axons of monkey somatosensory cortex. European Journal of Neuroscience 4, 46–60.Google Scholar
Ferrer, I., Tuñón, T., Soriano, E., del Río, A., Iraizoz, I., Fonseca, M. & Guionnet, N. (1992). Calbindin immunoreactivity in normal human temporal neocortex. Brain Research 572, 33–41.Google Scholar
Friedländer, M.J., Martin, K.A.C. & Wassenhove-McCarthy, D. (1991). Effects of monocular visual deprivation on geniculocortical innervation of area 18 in cat. Journal of Neuroscience 11, 3268–3288.Google Scholar
Haseltine, E.C., de Bruyn, E.J. & Casagrande, V.A. (1979). Demonstration of ocular-dominance columns in Nissl-stained sections of monkey visual cortex following enucleation. Brain Research 176, 153–158.CrossRefGoogle ScholarPubMed
Hendrickson, A.E., Wilson, J.R. & Ogren, M.P. (1978). The neuro-anatomical organization of pathways between the dorsal lateral geniculate nucleus and the visual cortex in Old World and New World primates. Journal of Comparative Neurology 182, 123–136.CrossRefGoogle Scholar
Hendrickson, A.E., VanBrederode, J.F., Mulligan, K.A. & Celio, M.R. (1991). Development of the calcium-binding protein parvalbumin and calbindin in monkey striate cortex. Journal of Comparative Neurology 307, 626–646.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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., pp. 477–502. Amsterdam: Elsevier Science Publishers.Google Scholar
Hendry, S.H.C. & Jones, E.G. (1986). Reduction in number of immu-nostained GABAergic neurons in deprived-eye dominance columns of monkey area 17. Nature 320, 750–753.CrossRefGoogle Scholar
Hendry, S.H.C. & Jones, E.G. (1988). Activity-dependent regulation of GABA expression in the visual cortex of adult monkeys. Neuron 1, 701–712.CrossRefGoogle ScholarPubMed
Hendry, S.H.C., Jones, E.G., Emson, P.C., Lawson, D.E.M., Heiz-mann, C.W. & Streit, P. (1989). Two classes of cortical GABA neurons defined by differential calcium-binding protein immunoreactivity. Experimental Brain Research 76, 467–472.Google Scholar
Hof, P.R., Cox, K., Young, W.G., Celio, M.R., Rogers, J. & Morrison, J.H. (1991). Parvalbumin-immunoreactive neurons in the neocortex are resistant to degeneration in Alzheimer’s disease. Journal of Neuropathology and Experimental Neurology 50, 451–462.CrossRefGoogle ScholarPubMed
Hogan, D. & Berman, N.E.J. (1991). Calbindin-D is transiently expressed in pyramidal cells of neonatal kittens in an area-dependent pattern. Society of Neuroscience Abstracts 17, 367.Google Scholar
Horton, J.C. (1984). Cytochrome-oxidase patches, a new cytoarchi-tectonic feature of monkey visual cortex. Philosophical Transactions of the Royal Society B (London) 304, 199–253.Google Scholar
Hsu, S.M., Raine, L. & Fanger, H. (1981). Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: A comparison between ABC and unlabeled antibody (PAP) procedures. Journal of Histochemistry and Cytochemistry 29, 577–580.Google Scholar
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.Google Scholar
Kawaguchi, Y., Katsumaru, H., Kosaka, T., Heizmann, C.W. & Hama, K. (1987). Fast spiking cells in rat hippocampus (CA1 region) contain the calcium-binding protein parvalbumin. Brain Research 416, 369–374.Google Scholar
Köhr, 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
Lewis, D.A. & Lund, J.S. (1990). Heterogeneity of chandelier neurons in monkey neocortex: Corticotropin-releasing factor- and parvalbumin-immunoreactive populations. Journal of Comparative Neurology 293, 599–615.Google Scholar
Livingstone, M.S., Hubel, D.H. (1982). Thalamic inputs to cytochrome oxidase-rich regions in monkey visual cortex. Proceedings National Academy Sciences of the U.S.A. 79, 6098–6101.Google Scholar
Lund, J.S. (1988). Anatomical organization of macaque monkey striate visual cortex. Annual Review of Neuroscience 11, 1062–1075.Google Scholar
Mize, R.R. & Luo, Q. (1992). Visual deprivation fails to reduce calbindin 28 kD or GABA immunoreactivity in the Rhesus monkey superior colliculus. Visual Neuroscience 9, 157–168.Google Scholar
Mize, R.R., Luo, Q. & Tigges, M. (1992 a). Monocular enucleation reduces immunoreactivity to the calcium-binding protein calbindin 28 kD in the Rhesus monkey lateral geniculate nucleus. Visual Neuroscience 9, 471–482.Google Scholar
Mize, R.R., Luo, Q., Butler, G.D., Jeon, C.J. & Nabors, B. (1992 b). The calcium-binding proteins parvalbumin and calbindin-D-28K form complementary patterns in the cat superior colliculus. Journal of Comparative Neurology 320, 243–256.CrossRefGoogle ScholarPubMed
Nitsch, R. & Frotscher, M. (1991). Maintenance of peripheral dendrites of GABAergic neurons requires specific input. Brain Research 554, 304–307.Google Scholar
Sachs, H. (1892). Das Hemisphärenmark des menschlichen Grosshirns, 1. Der Hinterhauptslappen. Leipzig: Georg Thieme.Google Scholar
Schmidt-Kastner, R., Meller, D. & Eysel, U.T. (1992). Immunohis-tochemical changes of neuronal calcium-binding proteins parvalbumin and calbindin-D-28k following unilateral deafferentiation in the rat visual system. Experimental Neurology 117, 230–246.Google Scholar
Séquier, J.M., Hunziker, W., Andressen, C. & Celio, M.R. (1990). Calbindin D-28k protein and mRNA localization in the rat brain. European Journal of Neuroscience 2, 1118–1126.CrossRefGoogle ScholarPubMed
Spatz, W.B., Illing, R.B. & Vogt, D.M. (1992). Cytochrome-oxidase blobs, parvalbumin- and calbindin-like immunoreactivity in area 17 of New and Old World monkeys. European Journal of Neuroscience (Suppl). 5, 260.Google Scholar
Tigges, M. & Tigges, J. (1991). Parvalbumin immunoreactivity of the lateral geniculate nucleus in adult rhesus monkeys after monocular eye enucleation. Visual Neuroscience 6, 375–382.CrossRefGoogle ScholarPubMed
VanBrederode, J.F., Mulligan, K.A. & Hendrickson, A.E. (1990). Calcium-binding proteins as markers for subpopulations of GABA-ergic neurons in monkey striate cortex. Journal of Comparative Neurology 298, 1–22.Google Scholar
Wiesel, T.N. & Hubel, D.H. (1965). Comparison of the effects of unilateral and bilateral closure on cortical unit responses in kittens. Journal of Neurophysiology 28, 1029–1040.CrossRefGoogle ScholarPubMed
Williams, R.J.P. (1992). Calcium fluxes in cells: New views on their significance. Cell Calcium 13, 273–275.Google Scholar
Williams, S.M., Goldman-Rakic, P.S. & Leranth, C. (1992). The syn-aptology of parvalbumin-immunoreactive neurons in the primate prefrontal cortex. Journal of Comparative Neurology 320, 353–369.Google Scholar
Wong-Riley, M.T.T. (1979). Changes in the visual system of monocu-larly sutured or enucleated cats demonstrable with cytochrome-oxidase histochemistry. Brain Research 171, 11–28.CrossRefGoogle ScholarPubMed
Wong-Rtley, M.T.T. & Carroll, E. W. (1984). Effect of impulse blockage on cytochrome-oxidase activity in monkey visual cortex. Nature 307, 262–264.CrossRefGoogle Scholar