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Activity correlates of cytochrome oxidase-defined compartments in granular and supragranular layers of primary visual cortex of the macaque monkey

Published online by Cambridge University Press:  02 June 2009

Edgar A. Deyoe ,
Thomas C. Trusk  and
Margaret T.T. Wong-Riley
Edgar A. Deyoe
Affiliation:
Department of Cellular Biology and Anatomy, The Medical College of Wisconsin, Milwaukee
Thomas C. Trusk
Affiliation:
Department of Cellular Biology and Anatomy, The Medical College of Wisconsin, Milwaukee
Margaret T.T. Wong-Riley
Affiliation:
Department of Cellular Biology and Anatomy, The Medical College of Wisconsin, Milwaukee
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Abstract

To determine if changes in metabolic capacity revealed by cytochrome oxidase (CO) histochemistry are related to sustained changes in energy-utilizing neuronal activity, we assayed CO levels and recorded multiunit firing rates along nearly tangential penetrations of V1 in seven adult macaque monkeys before and after single, monocular injections of TTX. Within as little as 14 h, TTX blockade began to reduce CO staining in zones of layer 4C that received dominant input from the injected eye. Since simple monocular occlusion has only minor effects on cortical CO levels (Trusk et al., 1990), the changes in activity that were specifically associated with CO depletion were isolated by comparing spike rates during monocular TTX blockade and during monocular occlusion. Five second samples of multiunit spike rate were obtained after 2-min adaptation to each of four adapting fields: black, gray, white, and textured. Results were similar for these four conditions. In layer 4C, ocular dominance zones with input from the TTX eye had ongoing spike rates that were 48% of the rates in zones with input from a normal but occluded eye. In six animals, it was possible to record activity at a single site before, during, and after the onset of TTX blockade. Background activity at these interpuff sites decreased as much as 3-fold in less than 1 h but stabilized within 3–4 h to an average of 53% of pre-TTX rates. These data support the interpretation that energy utilization linked to sustained spike rates partially regulates CO levels under normal conditions, at least in layer 4. Furthermore, changes in neuronal activity induced by retinal TTX preceded the detectable reduction in CO activity in V1 suggesting that the adjustment of CO levels was in response to the altered activity.

Keywords

Cytochrome oxidaseVisual cortexMacaque monkeySustained activity
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 4 , July 1995 , pp. 629 - 639
Copyright
Copyright © Cambridge University Press 1995

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References

Carroll, E.W. & Wong-Riley, M.T.T. (1984). Quantitative light and electron microscopic analysis of cytochrome oxidase-rich zones in the striate cortex of the squirrel monkey. Journal of Comparative Neurology 221, 1–17.Google Scholar
Conti, F. (1991). Toward the anatomical identification of glutamatergic neurons and synapses in the cerebral cortex. In Excitatory Amino Acids, ed. Meldrum, B.S., Moroni, F., Simon, R.P. & Woods, J.H., pp. 45–53. New York: Raven Press.Google Scholar
DeYoe, E.A. (1983). An investigation in the awake macaque of the threshold for the detection of electrical currents applied to striate cortex: Psychophysical properties and laminar differences. Ph.D. Thesis, University of Rochester.Google Scholar
DeYoe, E.A. & Van Essen, D.C. (1985). Segregation of efferent connections and receptive field properties in visual area V2 of the macaque. Nature 317, 58–61.CrossRefGoogle ScholarPubMed
Douglas, R.J. & Martin, K.A.C. (1990). Neocortex. In The Synaptic Organization of the Brain, ed. Shepherd, G.M., pp. 389–438. New York: Oxford University Press.Google Scholar
Ferster, D. (1992). The synaptic inputs to simple cells of the cat visual cortex. Progress in Brain Research 90, 423–441.CrossRefGoogle ScholarPubMed
Hawken, M.J. & Parker, A.J. (1984). Contrast sensitivity and orientation selectivity in lamina IV of the striate cortex of old world monkeys. Experimental Brain Research 54, 367–372.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
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.T.T. (1990). Regulation of cytochrome oxidase protein levels by functional activity in the macaque visual system. Journal of Neuroscience 10, 1331–1340.CrossRefGoogle Scholar
Hille, B. (1968). Pharmacological modifications of the sodium channels of frog nerve. Journal of General Physiology 51, 199–219.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. & Livingstone, M.S. (1987). Segregation of form, color, and stereopsis in primate area 18. Journal of Neuroscience 7, 3378–3415.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Livingstone, M.S. (1990). Color and contrast sensitivity in the lateral geniculate body and primary visual cortex of the macaque monkey. Journal of Neuroscience 10, 2223–2237.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1968). Receptive fields and functional architecture of monkey striate cortex. Journal of Physiology 195, 215–243.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
Kayama, Y., Riso, R.R., Bartlett, J.R. & Doty, R.W. (1979). Luxotonic responses of units in macaque striate cortex. Journal of Neurophysiology 42, 1495–1517.CrossRefGoogle ScholarPubMed
Kennedy, H., Bullier, J. & Dehay, C. (1985). Cytochrome oxidase activity in the striate cortex and lateral geniculate nucleus of the newborn and adult macaque monkey. Experimental Brain Research 61, 204–209.CrossRefGoogle ScholarPubMed
Livingstone, M. & Hubel, D. (1988). Segregation of form, color, movement, and depth: Anatomy, physiology, and perception. Science 240, 740–749.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
Lowry, O.H. (1975). Energy metabolism in brain and its control. In Brain Work, Alfred Benzon Symposium VIII, ed. Ingvar, D.H. & Lassen, N.A., pp. 48–64. New York: Academic Press.Google Scholar
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
Poggio, G.F. (1984). Processing of stereoscopic information in primary visual cortex. In Dynamic Aspects of Neocortical Function, ed. Edelman, M.G., Gall, W.E. & Cowan, W.M., pp. 613–625. New York: Wiley.Google Scholar
Schein, S.J., de Monasterio, F.M., Kennedy, C. & Sokoloff, L. (1985). Deoxyglucose labeling of macaques with monocular enucleation shows stripes, not spots, outside of layer 4 of striate cortex. Society for Neuroscience Abstracts 11, 16.Google Scholar
Schiller, P.H., Finlay, B.L. & Volman, S.F. (1976). Quantitative studies of single cell properties in monkey striate cortex. II. Orientation specificity and ocular dominance. Journal of Neurophysiology 39, 1320–1333.CrossRefGoogle ScholarPubMed
Shipp, S. & Zeki, S. (1985). Segregation of pathways leading from area V2 to areas V4 and V5 of macaque monkey visual cortex. Nature 315, 322–324.CrossRefGoogle ScholarPubMed
Snodderly, D.M. & Gur, M. (1993). Spontaneous activity and response properties of neurons in striate cortex of trained monkeys. Society for Neuroscience Abstracts 19, 1574.Google Scholar
Sokoloff, L. (1974). Changes in enzyme activities in neural tissues with maturation and development of the nervous system. In The Neurosciences: Third Study Program, ed. Schmitt, F.O. & Worden, F.G., pp. 885–898. Cambridge, MA: MIT Press.Google Scholar
Tamura, H., Hicks, T.P., Hata, Y., Tsumoto, T. & Yamatodani, A. (1990). Release of glutamate and aspartate from the visual cortex of the cat following activation of afferent pathways. Experimental Brain Research 80, 447–455.CrossRefGoogle ScholarPubMed
Tootell, R.B.H. & Hamilton, S. (1989). Functional anatomy of the second visual area (V2) in the macaque. Journal of Neuroscience 9, 2620–2644.CrossRefGoogle ScholarPubMed
Trusk, T.C., Kaboord, W.S. & Wong-Riley, M.T.T. (1990). Effects of monocular enucleation, tetrodotoxin, and lid suture on cytochrome-oxidase reactivity in supragranular puffs of adult macaque striate cortex. Visual Neuroscience 4, 185–204.CrossRefGoogle ScholarPubMed
Trusk, T.C., Wong-Riley, M. & DeYoe, E.A. (1992). Changes in cytochrome oxidase and neuronal activity in V1 induced by monocular TTX blockade in macaque monkeys. Society for Neuroscience Abstracts 18, 298.Google Scholar
Ts'o, D.Y. & Gilbert, C.D. (1988). The organization of chromatic and spatial interactions in the primate. Journal of Neuroscience 8, 1712–1727.CrossRefGoogle ScholarPubMed
Vaughan, H.G. (1982). The neural origins of human event-related potentials. Annals of the New York Academy of Sciences 388, 125–138.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. & Carroll, E.W. (1984). Effect of impulse blockage on cytochrome oxidase activity in monkey visual system. Nature 307, 262–264.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.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.C., pp. 450–486. New Jersey: World Scientific Press.CrossRefGoogle Scholar
Wong-Riley, M.T.T. (1989). Cytochrome oxidase: An endogenous metabolic marker for neuronal activity. Trends in Neuroscience 12, 94–101.CrossRefGoogle ScholarPubMed
Wong-Riley, M.T.T. (1994). Primate visual cortex: Dynamic metabolic organization and plasticity revealed by cytochrome oxidase. In Cerebral Cortex: Primary Visual Cortex of Primates, ed. Peters, A. & Rockland, K., pp. 141–200. New York: Plenum Press.CrossRefGoogle Scholar
Wong-Riley, M.T.T., Tripathi, S.C., Trusk, T.C. & Hoppe, D.A. (1989 a). Effect of retinal impulse blockage on cytochrome oxidase-rich zones in the macaque striate cortex: I. Quantitative electron-microscopic (EM) analysis of neurons. Visual Neuroscience 2, 483–497.CrossRefGoogle ScholarPubMed
Wong-Riley, M.T.T., Trusk, T.C., Tripathi, S.C. & Hoppe, D.A. (1989 b). Effect of retinal impulse blockage on cytochrome oxidaserich zones in the macaque striate cortex: II. Quantitative electron-microscopic (EM) analysis of neuropil. Visual Neuroscience 2, 499–514.CrossRefGoogle ScholarPubMed
Wong-Riley, M.T.T., Trusk, T.C., Kaboord, W. & Huang, Z. (1994). Effect of retinal impulse blockage on cytochrome oxidase-poor interpuffs in the macaque striate cortex: Quantitative EM analysis of neurons. Journal of Neurocytology 23, 533–553.CrossRefGoogle ScholarPubMed