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Effect of monocular enucleation or impulse blockage on gamma-aminobutyric acid and cytochrome oxidase levels in neurons of the adult cat lateral geniculate nucleus

Published online by Cambridge University Press:  02 June 2009

X. G. Luo ,
X. Y. Kong  and
M. T. T. Wong-Riley
X. G. Luo
Affiliation:
Department of Anatomy and Cellular Biology, Medical College of Wisconsin, Milwaukee
X. Y. Kong
Affiliation:
Department of Anatomy and Cellular Biology, Medical College of Wisconsin, Milwaukee
M. T. T. Wong-Riley
Affiliation:
Department of Anatomy and Cellular Biology, Medical College of Wisconsin, Milwaukee
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Abstract

Much attention has been paid to the effect of various types of neonatally induced retinal insults on neurons of the cat lateral geniculate nucleus (LGN). Little is known about cellular adjustment to functional altertions commencing in the adult. The present study was aimed at examining the effect of monocular enucleation or retinal impulse blockade on mature neurons of the cat LGN and perigeniculate nucleus. In addition to labeling the relay neurons with cytochrome oxidase (CO) histochemistry and immunohistochemistry, and presumed interneurons with GABA immunohistochemistry, the two markers were also combined in the same section. The results showed that GABA-immunoreactive neurons in the LGN can be subdivided into two major groups: highly immunoreactive neurons (Hir) and moderately immunoreactive neurons (Mir). These two groups differed slightly in their size and CO levels. With monocular enucleation or TTX treatment, there was a reduction in the numerical density of Hir and a concomitant increase in Mir in the affected laminae. However, there was no evidence of a reduction in GABA immunoreactivity in neurons of the perigeniculate nucleus. With regard to relay cells our data were in agreement with our previous findings (Kageyama & Wong-Riley, 1985) that there was a statistically significant positive correlation between cell size and CO levels, so that neurons with large cross-sectional areas were predominately darkly reactive for CO (Dco), while medium-to-small neurons were mainly moderate to lightly reactive (M/Lco). After monocular enucleation or TTX injections, the numerical density and size of Dco were significantly reduced, while those of M/Lco were proportionally increased in the affected laminae, indicating a conversion of some Dco to M/Lco. The results indicate that the maintenance of CO levels in predominately the large relay cells and GABA levels in a subclass of small neurons of the mature cat LGN are activity-dependent and are highly sensitive to retinal insults.

Keywords

Cat LGNPerigeniculate nucleusCytochrome oxidaseGABA double labelingTetrodotoxinMonocular enucleation
Type
Research Article
Information
Visual Neuroscience , Volume 6 , Issue 1 , January 1991 , pp. 55 - 68
Copyright
Copyright © Cambridge University Press 1991

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References

Bullier, J. & Norton, T.T. (1979). Comparison of receptive-field properties of X and Y ganglion cells with X and Y lateral geniculate cells in the cat. Journal of Neurophysiology 42, 274–291.CrossRefGoogle ScholarPubMed
Cleland, B.G., Dubin, M.W. & Levick, W.R. (1971). Sustained and transient neurons in the cat's retina and lateral geniculate nucleus. Journal of Physiology (London) 217, 473–496.CrossRefGoogle ScholarPubMed
Dubin, M.W. & Cleland, B.G. (1977). Organization of visual inputs to interneurons of lateral geniculate nucleus of the cat. Journal of Neurophysiology 40, 410–427.CrossRefGoogle ScholarPubMed
Enroth-Cugell, C. & Robson, J.G. (1966). The contrast sensitivity of retinal ganglion cells of the cat. Journal of Physiology (London) 187, 517–552.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. Jr & Peters, A. (1972). The synaptic glomerulus and the intrinsic neurons in the dorsal lateral geniculate nucleus of the cat. Journal of Comparative Neurology 144, 285–334.CrossRefGoogle ScholarPubMed
Fitzpatrick, D.,Penny, G.R. & Schmechel, D.E. (1984). Glutamic acid decarboxylase-immunoreactive neurons and terminals in the lateral geniculate nucleus of the cat. Journal of Neuroscience 4, 1809–1829.CrossRefGoogle ScholarPubMed
Friedlander, M.J., Stanford, L.R. & Sherman, S.M. (1982). Effects of monocular deprivation on the structure/function relationship of individual neurons in the cat's lateral geniculate nucleus. Journal of Neuroscience 2, 321–330.CrossRefGoogle ScholarPubMed
Fukuda, Y. & Stone, J. (1976). Evidence of differential inhibitory influences on X- and Y-type relay cells in the cat's lateral geniculate nucleus. Brain Research 113, 188–196.CrossRefGoogle ScholarPubMed
Garey, L.J. & Blakemore, C. (1977). Monocular deprivation morphological effects on different classes of neurons in the lateral geniculate nucleus. Experimental Brain Research 28, 259–278.Google ScholarPubMed
Guillery, R.W. (1966). A study of Golgi preparations from the dorsal lateral geniculate nucleus of the adult cat. Journal of Comparative Neurology 128, 21–50.CrossRefGoogle ScholarPubMed
Hendry, S.H.C. & Jones, E.G. (1986). Reduction in number of immunostained GABAergic neurons in the 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
Hevner, R.F. & Wong-Riley, M. (1989). Brain cytochrome oxidase: Purification, antibody production, and histochemical/immunohistochemical correlations in the CNS. Journal of Neuroscience 9, 3884–3898.CrossRefGoogle Scholar
Hevner, R.F. & Wong-Riley, M.T.T. (1990). Regulation of cytochrome oxidase protein levels by functional activity in the macaque monkey visual system. Journal of Neuroscience 10, 1331–1340.CrossRefGoogle ScholarPubMed
Ito, M. (1984). The Cerebellum and Neural Control. New York: Raven Press.Google Scholar
Ito, M. & Oshima, T. (1962). Temporal summation of after-hyperpolarization following a motoneuron spike. Nature 195, 910–911.CrossRefGoogle Scholar
Kageyama, G.H. & Wong-Riley, M. (1985). An analysis of the cellular localization of cytochrome oxidase in the lateral geniculate nucleus of the adult cat. Journal of Comparative Neurology 242, 338–357.CrossRefGoogle ScholarPubMed
Kageyama, G.H. & Wong-Riley, M. (1986). Differential effect of visual deprivation on cytochrome-oxidase levels in major cell classes of the cat LGN. Journal of Comparative Neurology 246, 212–237.CrossRefGoogle ScholarPubMed
Lennie, P. (1980). Parallel visual pathways: A review. Vision Research 20, 564–594.CrossRefGoogle ScholarPubMed
LeVay, S. & Ferster, D. (1977). Relay cell classes in the lateral geniculate nucleus of the cat and the effects of visual deprivation. Journal of Comparative Neurology 172, 563–584.CrossRefGoogle Scholar
Lin, C.-S. & Sherman, S.M. (1978). Effects of early monocular eyelid suture upon development of relay cell classes in the cat's lateral geniculate nucleus. Journal of Comparative Neurology 181, 809–832.CrossRefGoogle ScholarPubMed
Luo, X.G., Hevner, R.F. & Wong-Riley, M.T.T. (1989). Double labeling of cytochrome oxidase and gamma-aminobutyric acid in the central nervous system neurons of adult cats. Journal of Neuroscience Methods 30, 189–195.CrossRefGoogle ScholarPubMed
Mjaatvedt, A.E. & Wong-Riley, M.T.T. (1988). The relationship between synaptogenesis and cytochrome oxidase activity in Purkinje cells of the developing rat cerebellum. Journal of Comparative Neurology 277, 155–182.CrossRefGoogle ScholarPubMed
Montero, V.M. (1986). Localization of gamma-aminobutyric acid (GABA) in type 3 cells and demonstration of their source to F2 terminals in the cat lateral geniculate nucleus: A Golgi-electron-micro scopic GABA-immunocytochemical study. Journal of Comparative Neurology 254, 228–245.CrossRefGoogle Scholar
Montero, V.M. & Singer, W. (1984). Ultrastructure and synaptic relations of neural elements containing glutamic acid decarboxylase (GAD) in the perigeniculate nucleus of the cat: A light- and electron-microscopic immunocytochemical study. Experimental Brain Research 56, 115–125.CrossRefGoogle Scholar
Montero, V.M. & Singer, W. (1985). Ultrastructural identification of somata and neural processes immunoreactive to antibodies against glutamic acid decarboxylase (GAD) in the dorsal lateral geniculate nucleus of the cat. Experimental Brain Research 59, 151–165.CrossRefGoogle ScholarPubMed
Montero, V.M. & Zempel, J. (1985). Evidence for two types of GABA-containing interneurons in the A laminae of the cat lateral geniculate nucleus: A double-label HRP and GABA-immunocytochemical study. Experimental Brain Research 60, 603–609.Google ScholarPubMed
Rapisardi, S.C. & Miles, T.P. (1984). Synaptology of retinal terminals in the dorsal lateral geniculate nucleus of the cat. Journal of Comparative Neurology 223, 515–534.CrossRefGoogle ScholarPubMed
Robson, J.A. & Martin-Elkins, C.L. (1985). The effects of monocular deprivation on the size of GAD+ neurons in the cat's dorsal lateral geniculate nucleus. Journal of Comparative Neurology 239, 62–67.CrossRefGoogle ScholarPubMed
Sherman, S.M., Hoffmann, K.-P. & Stone, J. (1972). Loss of a specific cell type from the dorsal lateral geniculate nucleus in visually deprived cats. Journal of Neurophysiology 35, 532–541.CrossRefGoogle 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
Vandesande, F., Demeulemeester, H., Orban, G.A. & Eysel, U. (1989). Influence of a binocular central retinal lesion on the GAD immunoreactivity in cat visual cortex and dLGN. Society for Neuroscience Abstracts 15, 1107.Google Scholar
Warren, R., Tremblay, N. & Dykes, R.W. (1989). Quantitative study of glutamic acid decarboxylase-immunoreactive neurons and cytochrome oxidase activity in normal and partially deafferented rat hindlimb somatosensory cortex. Journal of Comparative Neurology 288, 583–592.CrossRefGoogle ScholarPubMed
Wiesel, T.N. & Hubel, D.H. (1963). Effects of visual deprivation on morphology and physiology of cells in the cat's lateral geniculate body. Journal of Neurophysiology 26, 978–993.CrossRefGoogle Scholar
Wilson, J.R., Friedlander, M.J. & Sherman, S.M. (1984). Fine structural morphology of identified X- and Y-cells in the cat's lateral geniculate nucleus. Proceedings of the Royal Society B (London) 221, 411–436.Google ScholarPubMed
Wilson, P.D., Rowe, M.H. & Stone, J. (1976). Properties of relay cells in the cat's lateral geniculate nucleus. A comparison of W-cells with X- and Y-cells. Journal of Neurophysiology 39, 1193–1209.CrossRefGoogle ScholarPubMed
Wong-Riley, M. (1979). Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Research 171, 11–28.CrossRefGoogle ScholarPubMed
Wong-Riley, M. (1989). Cytochrome oxidase: An endogenous metabolic marker for neuronal activity. Trends in Neuroscience 12, 94–101.CrossRefGoogle ScholarPubMed
Wong-Riley, M.T.T. & Kageyama, G.H. (1986). Localization of cytochrome oxidase in the spinal cord and dorsal root ganglia, with quantitative analysis of ventral horn cells in the monkey. Journal of Comparative Neurology 245, 41–61.CrossRefGoogle Scholar
Wong-Riley, M.T.T. & Riley, D.A. (1983). The effect of impulse blockage on cytochrome-oxidase activity in the cat visual system. Brain Research 261, 185–193.CrossRefGoogle ScholarPubMed