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Effect of retinal impulse blockage on cytochrome oxidase-rich zones in the macaque striate cortex: I. Quantitative electron-microscopic (EM) analysis of neurons

Published online by Cambridge University Press:  02 June 2009

Margaret T. T. Wong-Riley ,
Satish C. Tripathi ,
Thomas C. Trusk  and
Daniel A. Hoppe
Margaret T. T. Wong-Riley
Affiliation:
Department of Anatomy and Cellular Biology, Medical College of Wisconsin, Milwaukee, Wisconsin
Satish C. Tripathi
Affiliation:
Department of Anatomy and Cellular Biology, Medical College of Wisconsin, Milwaukee, Wisconsin
Thomas C. Trusk
Affiliation:
Department of Anatomy and Cellular Biology, Medical College of Wisconsin, Milwaukee, Wisconsin
Daniel A. Hoppe
Affiliation:
Department of Anatomy and Cellular Biology, Medical College of Wisconsin, Milwaukee, Wisconsin
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Abstract

Our previous light-microscopic study indicates that unilateral retinal impulse blockage with tetrodotoxin (TTX) causes a reversible decrease of cytochrome oxidase (CO) in alternating rows of metabolically active zones (puffs) in the adult macaque striate cortex (Wong-Riley & Carroll, 1984b). The goal of the present study was to determine if TTX blockade adversely affects all neurons or only a subpopulation of neurons within the puffs. Three major neuronal types were identified based on mitochondrial CO activities and morphological characteristics. Type A neurons were the most prevalent, consisting of small pyramidal and nonpyramidal neurons that received only symmetrical axosomatic synapses. They had little cytoplasm and relatively low levels of CO activity, and showed the least change with TTX treatment. Type B cells were medium-to-large pyramidal neurons that received exclusively symmetrical axosomatic synapses and were moderately reactive for CO. Impulse blockage caused a decrease in mitochondrial size and packing density, but somal size remained within the control range. Type C cells were medium-sized nonpyramidal neurons contacted by both asymmetrical and symmetrical axosomatic synapses. They contained abundant darkly reactive mitochondria and presumably are metabolically the most active. This cell type suffered the greatest decrease in somal size and packing density of mitochondria, particularly the darkly reactive ones. A rare fourth cell type, type D, was a small, darkly reactive nonpyramidal variety that gave rise to somatodendritic synapses. Their low occurrence prevented statistical analysis under normal and TTX-treated conditions. These data indicate that retinal impulse blockade is most detrimental to the metabolically most active neurons in the adult primate cortical puffs. The alterations are not permanent, because the effects of TTX are fully reversible (Carroll & Wong-Riley, 1987).

Keywords

Macaque striate puffsTetrodotoxinCytochrome oxidase cytochemistryQuantitative EM analysisAdult metabolic plasticity
Type
Research Article
Information
Visual Neuroscience , Volume 2 , Issue 5 , May 1989 , pp. 483 - 497
Copyright
Copyright © Cambridge University Press 1989

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References

Carroll, E. & Wong-Riley, M. (1982). Light- and electron-microscopic analysis of cytochrome oxidase-rich zones in the striate cortex of squirrel monkeys. Society for Neuroscience Abstracts 8, 706.Google Scholar
Carroll, E. W. & Wong-Riley, M.T.T. (1984). Quantitative lightand electron-microscopic analysis of cytochrome oxidase-rich zones in the striate cortex of the squirrel monkey. Journal of Comparative Neurology 222, 1–17.CrossRefGoogle Scholar
Carroll, E.W. & Wono-Riley, M. (1985). Comparative effects of impulse blockage on cytochrome oxidase activity in the visual systems of Macaca mulatto, fascicularis and Saimiri sciureus. Society for Neuroscience Abstracts 11, 16.Google Scholar
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
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., Schmechel, D.E. & Towles, A.C. (1987). Distribution of GABAergic neurons and axon terminals in the macaque striate cortex. Journal of Comparative Neurology 264, 73–91.CrossRefGoogle ScholarPubMed
Garey, L.J. (1971). A light- and electron-microscopic study of the visual cortex of the cat and monkey. Proceedings of the Royal Society B (London) 179, 21–40.Google Scholar
Hendrickson, A.E. (1985). Dots, stripes, and columns in monkey visual cortex. Trends in Neurosciences 8, 406–410.CrossRefGoogle Scholar
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
Hendrickson, A.E. & Wilson, J.R. (1979). A difference in [14C] deoxyglucose autoradiographic patterns in striate cortex between Macaca and Saimiri monkeys following monocular stimulation. Brain Research 170, 353–358.CrossRefGoogle ScholarPubMed
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. & 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
Hendry, S.H.C. & Kennedy, M.B. (1986). Immunoreactivity for a calmodulin-dependent protein kinase is selectively increased in macaque striate cortex after monocular deprivation. Proceedings of the National Academy of Sciences of the U.S.A. 83, 1536–1540.CrossRefGoogle ScholarPubMed
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. & 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. (1974). Sequence regularity and geometry of orientation columns in the monkey striate cortex. Journal of Comparative Neurology 158, 267–294.CrossRefGoogle ScholarPubMed
Humphrey, A.L. & Hendrickson, A.E. (1983). Background and stimulus-induced patterns of high metabolic activity in the visual cortex (area 17) of the squirrel and macaque monkey. Journal of Neuroscience 3, 345–358.CrossRefGoogle ScholarPubMed
Jones, E.G. & Hendry, S.H.C. (1986). Co-localization of GABA and neuropeptides in neocortical neurons. Trends in Neurosciences 9, 71–76.CrossRefGoogle Scholar
Kageyama, G.H. & Wong-Riley, M.T.T. (1982). Histochemical localization of cytochrome oxidase in the hippocampus: correlation with specific neuronal types and afferent pathways. Neuroscience 7, 2337–2361.CrossRefGoogle ScholarPubMed
Kageyama, G.H. & Wong-Riley, M.T.T. (1984). The histochemical localization of cytochrome oxidase in the retina and lateral geniculate nucleus of the ferret, cat, and monkey, with particular reference to retinal mosaics and On/Off-center visual channels. Journal of Neuroscience 4, 2445–2459.CrossRefGoogle Scholar
Kageyama, G.H. & Wong-Riley, M.T.T. (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
Levay, S. (1973). Synaptic patterns in the visual cortex of the cat and monkey. Electron microscopy of Golgi preparations. Journal of Comparative Neurology 150, 53–86.CrossRefGoogle Scholar
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. (1983). Specificity of cortico-cortical connections in monkey visual system. Nature 304, 531–534.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1984a). Anatomy and physiology of a color system in the primate visual cortex. Journal of Neuroscience 4, 309–356.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1984b). Specificity of intrinsic connections in primate primary visual cortex. Journal of Neuroscience 4, 2830–2835.CrossRefGoogle ScholarPubMed
Lund, J.S. & Boothe, R.G. (1975). Interlaminar connections and pyramidal neuron organization in the visual cortex, area 17, of the macaque monkey. Journal of Comparative Neurology 159, 305–334.CrossRefGoogle Scholar
Ribak, C.E. (1978). Aspinous and sparsely spinous stellate neurons in the visual cortex of rats containing glutamic acid decarboxylase. Journal of Neurocytology 7, 461–478.CrossRefGoogle ScholarPubMed
Saint Marie, R.L. & Peters, A. (1985). The morphology and synaptic connections of spiny stellate neurons in monkey visual cortex (area 17): a Golgi-electron microscopic study. Journal of Comparative Neurology 233, 213–235.CrossRefGoogle ScholarPubMed
Skou, J.C. (1957). The influence of some cations on an adenosine triphosphatase from peripheral nerve. Biochemica et Biophysica Acta 23, 394–401.CrossRefGoogle Scholar
Somogyi, P., Freund, T.F., Wu, J.-Y. & Smith, A.D. (1983). The section-Golgi impregnation procedure. 2. Immunocytochemical demonstration of glutamate decarboxylase in Golgi-impregnated neurons in their afferent synaptic boutons in the visual cortex of the cat. Neuroscience 9, 475–490.CrossRefGoogle ScholarPubMed
Somogyi, P. & Hodgson, A.J. (1985). Antisera to gamma-aminobutyric acid. III. Demonstration of GABA in Golgi-impregnated neurons and in conventional electron-microscopic sections of cat striate cortex. Journal of Histochemistry and Cytochemistry 33, 249–257.CrossRefGoogle ScholarPubMed
Somogyi, P., Kisvarday, Z.F., Freund, T.F. & Cowey, A. (1984). Characterization by Golgi impregnation of neurons that accumulate 3H-GABA in the visual cortex of monkey. Experimental Brain Research 53, 295–303.CrossRefGoogle ScholarPubMed
Tootell, R.B.H., Silverman, M.S., DeValois, R.L. & Jacobs, G.H. (1983). Functional organization of the second cortical visual area in primates. Science 220, 737–739.CrossRefGoogle ScholarPubMed
Ts'o, D.Y. & Gilbert, Cd. (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. (1979a). Columnar cortico-cortical interconnections within the visual system of the squirrel and macaque monkeys. Brain Research 162, 201–217.CrossRefGoogle ScholarPubMed
Wong-Riley, M. (1979b). Changes in the visual system of monocularly sutured or enucleated cats demonstrable wtih cytochrome oxidase histochemistry. Brain Research 171, 11–28.CrossRefGoogle ScholarPubMed
Wong-Riley, M.T.T. (1988). Comparative study of the mammalian primary visual cortex with cytochrome oxidase histochemistry. In Vision: Structure and Function, ed. Yew, D.T., So, K.F. & Tsang, D.S., pp. 450–486. New Jersey: World Scientific Press.CrossRefGoogle Scholar
Wong-Riley, M.T.T. & Carroll, E.W. (1984a). Quantitative lightand electron-microscopic analysis of cytochrome oxidase-rich zones in VII prestriate cortex of the squirrel monkey. Journal of Comparative Neurology 222, 18–37.CrossRefGoogle Scholar
Wong-Riley, M. & Carroll, E.W. (1984b). The effect of impulse blockage on cytochrome oxidase activity in the monkey visual system. Nature 307, 262–264.CrossRefGoogle ScholarPubMed
Wong-Riley, M. & Kageyama, G. (1985). Cytochrome oxidase cytochemistry: electron-microscopic analysis of several postfixation variables. Anatomical Record 211, 217A.Google Scholar
Wong-Riley, M.T.T. & Kageyama, G. (1986). Localization of cytochrome oxidase in the spinal cord and dorsal root ganglia, with quantitative analysis of ventral horn cells in monkeys. Journal of Comparative Neurology 245, 41–61.CrossRefGoogle ScholarPubMed
Wong-Riley, M. & 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
Wong-Riley, M., Tripathi, S. & Hoppe, D. (1986). Quantitative EM analysis of the effect of retinal impulse blockage on cytochrome oxidase-rich zones in the macaque striate cortex. Society for Neuroscience Abstracts 12, 130.Google Scholar
Wong-Riley, M.T.T., Trusk, T.C., Tripathi, S.C. & Hoppe, D.A. (1989). Effect of retinal impulse blockage on cytochrome oxidaserich zones in the macaque striate cortex. II. Quantitative electronmicroscopic (EM) analysis of neuropil. Visual Neuroscience 2, 499.CrossRefGoogle ScholarPubMed