Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-22T23:47:17.489Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of monocular enucleation, tetrodotoxin, and lid suture on cytochrome-oxidase reactivity in supragranular puffs of adult macaque striate cortex

Published online by Cambridge University Press:  02 June 2009

Thomas C. Trusk ,
Wayne S. Kaboord  and
Margaret T.T. Wong-Riley
Get access Rights & Permissions [Opens in a new window]

Abstract

The laminar structure and cellular distribution of cytochrome-oxidase (CO) reactivity in supragranular puffs of striate cortex was examined in adult macaque monkeys surviving various periods of monocular enucleation, lid suture, and retinal impulse blockage with tetrodotoxin (TTX). Enucleation and TTX produced a rapid and severe loss in the size of the CO reactive region in puffs dominated by the removed or treated eye compared to slower and less marked reductions obtained in deprived puffs of lid-sutured monkeys. In all deprived animals, the cross-sectional areas of deprived puffs decreased most rapidly in the upper layers (2 and 3A). In long-term enucleated (60 wks) and TTX-treated (4 wks) monkeys, puff area was severely reduced in layer 3B, while reactivity in layer 3B appeared partially spared in lid-sutured monkeys. The density of the CO reaction product was significantly and evenly reduced throughout deprived puffs for all of the monkeys examined; however, this decrease was less severe in adult monkeys lid-sutured for 11 wks. Although no evidence for cell loss was obtained, all three forms of visual deprivation led to lower counts of neuronal perikarya with high levels of CO reaction product in both deprived puff and interpuff areas. This effect was less marked in the deprived puffs of monkeys lid-sutured for 2.5 and 3 yrs, suggesting recovery of CO activity in some neurons. Neurons in deprived puffs and interpuffs were generally similar in size to those in nondeprived regions, although CO-reactive cells were significantly smaller in the deprived puffs of monkeys enucleated for 28.5 or 60 wks. These results indicate that the metabolic response of neuronal elements in supragranular striate cortex depends upon the nature of the visual deficit. The partial sparing of CO reactivity in deprived puffs of lid-sutured monkeys may reflect the continued transmission of certain types of visual stimuli through a closed eyelid.

Keywords

Macaque striate puffsEnucleationTetrodotoxinLid sutureCytochrome-oxidase histochemistryAdult metabolic plasticity
Type
Research Articles
Information
Visual Neuroscience , Volume 4 , Issue 3 , March 1990 , pp. 185 - 204
Copyright
Copyright © Cambridge University Press 1990

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.)

References

Carroll, E.W. & Wong-Riley, M. (1984). Quantitative light and electron microscopic analysis of cytochrome oxidase-rich zones in the striate cortex of the squirrel monkey. Journal of Comparative Neurology 222, 1–17.CrossRefGoogle ScholarPubMed
Carroll, E.W. & Wong-Riley, M. (1987). Recovery of cytochrome oxidase activity in the adult macaque visual system after termination of impulse blockage due to tetrodotoxin. Society for Neuroscience Abstracts 13, 1046.Google Scholar
Crawford, M.L.J. & Marc, R.E. (1976). Light transmission of cat and monkey eyelids. Vision Research 16, 323–324.CrossRefGoogle Scholar
Fitzpatrick, D., Itoh, K. & Diamond, I.T. (1983). The laminar organization of the lateral geniculate body and the striate cortex in the squirrel monkey (Saimiri sciureus). Journal of Neuroscience 3, 673–702.CrossRefGoogle ScholarPubMed
Fitzpatrick, D., Lund, J.S. & Blasdel, G.G. (1985). Intrinsic connections of macaque striate cortex. Afferent and efferent connections of lamina 4C. Journal of Neuroscience 5, 3329–3349.CrossRefGoogle ScholarPubMed
Freeman, R.D. & Bradley, A. (1980). Monocularly deprived humans: nondeprived eye has supernormal vernier acuity. Journal of Neurophysiology 43, 1645–1653.CrossRefGoogle ScholarPubMed
Graybiel, A.M. & Ragsdale, C.W. (1982). Pseudocholinesterase staining in the primary visual pathway of the macaque monkey. Nature 299, 439–442.CrossRefGoogle ScholarPubMed
Haseltine, E.C., De Bruyn, E.J. & Cassagrande, 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., Hunt, S.P. & Wu, J.-Y. (1981). Immunocytochemical localization of glutamic-acid decarboxylase in monkey striate cortex. Nature 292, 605–607.CrossRefGoogle ScholarPubMed
Hendrickson, A.E. & Tigges, M. (1985). Enucleation demonstrates ocular dominance columns in Old World macaque but not in New World squirrel monkey visual cortex. Brain Research 333, 340–344.CrossRefGoogle Scholar
Hendry, S.H.C. & Jones, E.G. (1986). Reduction in number of immunostained GABAergic neurones in deprived-eye dominance columns of monkey area 17. Nature 320, 750–753.CrossRefGoogle ScholarPubMed
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. & Burstein, N. (1987). Activity-dependent regulation of tachykinin-like immunoreactivity in visual cortical neurons: increased and decreased immunostaining in the cytochrome oxidase patches of monocularly aphakic monkeys. Society for Neuroscience Abstracts 13, 358.Google Scholar
Hiltgen, G. & Wong-Riley, M. (1986). Quantitative EM analysis of the effect of retinal impulse blockage on cytochrome oxidase activity in lamina IVC of macaque striate cortex. Society for Neuroscience Abstracts 12, 130.Google Scholar
Horton, J.C. (1984). Cytochrome oxidase patches: a new cytoarchitectonic feature of monkey visual cortex. Philosophical Transactions of the Royal Society B (London), 304, 199–253.Google ScholarPubMed
Horton, J.C. & Hedley-White, E.T. (1984). Mapping of cytochrome oxidase patches and ocular dominance columns in human visual cortex. Philosophical Transactions of the Royal Society B (London), 304, 255–272.Google ScholarPubMed
Horton, J.C. & Hubel, D.H. (1981). Regular patchy distribution of cytochrome oxidase staining in primary visual cortex of macaque monkey. Nature 292, 762–764.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1972). Laminar and columnar distribution of geniculocortical fibers in the macaque monkey. Journal of Comparative Neurology 146, 421–450.CrossRefGoogle ScholarPubMed
Katz, L., Gilbert, C. & Wiesel, T. (1989). Local circuits and ocular dominance columns in monkeys striate cortex. Journal of Neuroscience 9, 1389–1399.CrossRefGoogle ScholarPubMed
LeVay, S., Connolly, M., Houde, J. & Van, Essen D.C. (1985). The complete pattern of ocular dominance stripes in the striate cortex and visual field of the macaque monkey. Journal of Neuroscience 5, 486–501.CrossRefGoogle ScholarPubMed
LeVay, S., Wiesel, T.N. & Hubel, D.H. (1980). The development of ocular dominance columns in normal and visually deprived monkeys. Journal of Comparative Neurology 191, 1–51.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1982). Thalamic inputs to cytochrome oxidase-rich regions in monkey visual cortex. Proceedings of the National Academy of Sciences of the U.S.A. 79, 6098–6101.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1984). Anatomy and physiology of a color system in the primate visual cortex. Journal of Neuroscience 4, 309–356.CrossRefGoogle ScholarPubMed
Lund, J.S. (1988). Anatomical organization of macaque striate cortex. Annual Review of Neuroscience 11, 253–288.CrossRefGoogle Scholar
Matthews, M.R., Cowan, W.M. & Powell, T.P.S. (1960). Transneuronal cell degeneration in the lateral geniculate nucleus of the macaque monkey. Journal of Anatomy 94, 145–169.Google ScholarPubMed
Moran, J. & Gordon, B. (1982). Long-term visual deprivation in a human. Vision Research 22, 27–36.CrossRefGoogle ScholarPubMed
Scheffé, H. (1959). The Analysis of Variance. New York: Wiley.Google Scholar
Tootell, R.B.H., Silverman, M.S., Hamilton, S.L., De, Valois R.L. & Switkes, E. (1988 a). Functional anatomy of macaque striate cortex, III: Color. Journal of Neuroscience 8, 1569–1593.CrossRefGoogle ScholarPubMed
Tootell, R.B.H., Silverman, M.S., Hamilton, S.L., De, Valois R.L. & Switkes, E. (1988 b). Functional anatomy of macaque striate cortex, IV: Contrast and magno-parvo streams. Journal of Neuroscience 8, 1594–1609.CrossRefGoogle ScholarPubMed
Tootell, R.B.H., Silverman, M.S., Hamilton, S.L., Switkes, E. & De, Valois R.L. (1988 c). Functional anatomy of macaque striate cortex, V: Spatial frequency. Journal of Neurosciences 8, 1610–1624.CrossRefGoogle ScholarPubMed
Trusk, T. & Wong-Riley, M. (1987). Effect of monocular lid suture, enucleation, and retinal impulse blockage on the volume of cytochrome oxidase-rich puffs in the adult macaque striate cortex. Society for Neuroscience Abstracts 13, 1046.Google Scholar
Trusk, T., Wong-Riley, M. & Kaboord, W. (1988). Effect of monocular lid suture, enucleation, and retinal impulse blockage on cytochrome oxidase reactivity in laminae II-III of macaque striate cortex. Society for Neuroscience Abstracts 14, 1112.Google Scholar
Ts'o, D.Y. & Gilbert, C.D. (1988). The organization of chromatic and spatial interactions in the primate striate cortex. Journal of Neuroscience 8, 1712–1727.CrossRefGoogle ScholarPubMed
Weber, J.T., Huerta, M.F., Kaas, J.H. & Harting, J.K. (1983). The projections of the lateral geniculate nucleus of the squirrel monkey: studies of the interlaminar zones and the S layers. Journal of Comparative Neurology 213, 135–145.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 Neurosciences 12, 94–101.CrossRefGoogle ScholarPubMed
Wong-Riley, M. & Carroll, E. (1984). The effect of impulse blockage on cytochrome oxidase activity in the monkey visual system. Nature 307, 262–264.CrossRefGoogle ScholarPubMed
Wong-Riley, M. & Norton, T. (1988). Histochemical localization of cytochrome oxidase activity in the visual system of the tree shrew: normal patterns and effect of retinal impulse blockage. Journal of Comparative Neurology 272, 562–578.CrossRefGoogle ScholarPubMed
Wong-Riley, M. & Riley, D. (1983). The effect of impulse blockage on cytochrome oxidase activity in the cat visual system. Brain Research 261, 185–193.CrossRefGoogle ScholarPubMed
Wong-Riley, M., Tripathi, S., Trusk, T. & Hoppe, D.A. (1989 a). Effect of retinal impulse blockage on cytochrome oxidase-rich zones in the macaque striate cortex, I: Quantitative EM analysis of neurons. Visual Neuroscience 2, 483–497.CrossRefGoogle ScholarPubMed
Wong-Riley, M., Trusk, T. & Hoppe, D. (1988). Localization of cytochrome oxidase in macaque striate cortex during prenatal development. Society for Neuroscience Abstracts 14, 743.Google Scholar
Wong-Riley, M., Trusk, T., Tripathi, S. & Hoppe, D. (1989 b). Effect of retinal impulse blockage on cytochrome oxidase-rich zones in the macaque striate cortex, II: Quantitative EM analysis of neuropil. Visual Neuroscience 2, 499–514.CrossRefGoogle ScholarPubMed