Skip to main content

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

  • Edgar A. Deyoe (a1), Thomas C. Trusk (a1) and Margaret T.T. Wong-Riley (a1)

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.

Hide All
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, 117.
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. 4553. New York: Raven Press.
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.
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, 5861.
Douglas R.J. & Martin K.A.C. (1990). Neocortex. In The Synaptic Organization of the Brain, ed. Shepherd G.M., pp. 389438. New York: Oxford University Press.
Ferster D. (1992). The synaptic inputs to simple cells of the cat visual cortex. Progress in Brain Research 90, 423441.
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, 367372.
Hendrickson A.E., Hunt S.P. & Wu J.Y. (1981). Immunocytochemical localization of glutamic acid decarboxylase in monkey striate cortex. Nature 292, 605607.
Hendry S.H.C. & Jones E.G. (1988). Activity-dependent regulation of GABA expression in the visual cortex of adult monkeys. Neuron 1, 701712.
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, 13311340.
Hille B. (1968). Pharmacological modifications of the sodium channels of frog nerve. Journal of General Physiology 51, 199219.
Horton J.C. (1984). Cytochrome oxidase patches: A new cytoarchitectonic feature of monkey visual cortex. Philosophical Transactions of the Royal Society B (London) 304, 199253.
Horton J.C. & Hubel D.H. (1981). Regular patchy distribution of cytochrome oxidase staining in primary visual cortex of macaque monkey. Nature 292, 762764.
Hubel D.H. & Livingstone M.S. (1987). Segregation of form, color, and stereopsis in primate area 18. Journal of Neuroscience 7, 33783415.
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, 22232237.
Hubel D.H. & Wiesel T.N. (1968). Receptive fields and functional architecture of monkey striate cortex. Journal of Physiology 195, 215243.
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, 345358.
Kayama Y., Riso R.R., Bartlett J.R. & Doty R.W. (1979). Luxotonic responses of units in macaque striate cortex. Journal of Neurophysiology 42, 14951517.
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, 204209.
Livingstone M. & Hubel D. (1988). Segregation of form, color, movement, and depth: Anatomy, physiology, and perception. Science 240, 740749.
Livingstone M.S. & Hubel D.H. (1984). Anatomy and physiology of a color system in the primate visual cortex. Journal of Neuroscience 4, 309356.
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. 4864. New York: Academic Press.
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, 305334.
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. 613625. New York: Wiley.
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.
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, 13201333.
Shipp S. & Zeki S. (1985). Segregation of pathways leading from area V2 to areas V4 and V5 of macaque monkey visual cortex. Nature 315, 322324.
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.
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. 885898. Cambridge, MA: MIT Press.
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, 447455.
Tootell R.B.H. & Hamilton S. (1989). Functional anatomy of the second visual area (V2) in the macaque. Journal of Neuroscience 9, 26202644.
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, 185204.
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.
Ts'o D.Y. & Gilbert C.D. (1988). The organization of chromatic and spatial interactions in the primate. Journal of Neuroscience 8, 17121727.
Vaughan H.G. (1982). The neural origins of human event-related potentials. Annals of the New York Academy of Sciences 388, 125138.
Wong-Riley M. (1979). Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Research 171, 1128.
Wong-Riley M. & Carroll E.W. (1984). Effect of impulse blockage on cytochrome oxidase activity in monkey visual system. Nature 307, 262264.
Wong-Riley M. & Riley D.A. (1983). The effect of impulse blockage on cytochrome oxidase activity in the cat visual system. Brain Research 261, 185193.
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. 450486. New Jersey: World Scientific Press.
Wong-Riley M.T.T. (1989). Cytochrome oxidase: An endogenous metabolic marker for neuronal activity. Trends in Neuroscience 12, 94101.
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. 141200. New York: Plenum Press.
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, 483497.
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, 499514.
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, 533553.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Visual Neuroscience
  • ISSN: 0952-5238
  • EISSN: 1469-8714
  • URL: /core/journals/visual-neuroscience
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Full text views

Total number of HTML views: 0
Total number of PDF views: 7 *
Loading metrics...

Abstract views

Total abstract views: 114 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 24th November 2017. This data will be updated every 24 hours.