Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-24T18:40:46.027Z Has data issue: false hasContentIssue false
  • English
  • Français

Cytochrome oxidase in the human visual cortex: Distribution in the developing and the adult brain

Published online by Cambridge University Press:  02 June 2009

Margaret T. T. Wong-Riley ,
Robert F. Hevner ,
Robert Cutlan ,
Melissa Earnest ,
Robert Egan ,
Julie Frost  and
Thuytien Nguyen
Margaret T. T. Wong-Riley
Affiliation:
Department of Cellular Biology and Anatomy, Medical College of Wisconsin, Milwaukee
Robert F. Hevner
Affiliation:
Department of Cellular Biology and Anatomy, Medical College of Wisconsin, Milwaukee
Robert Cutlan
Affiliation:
Department of Cellular Biology and Anatomy, Medical College of Wisconsin, Milwaukee
Melissa Earnest
Affiliation:
Department of Cellular Biology and Anatomy, Medical College of Wisconsin, Milwaukee
Robert Egan
Affiliation:
Department of Cellular Biology and Anatomy, Medical College of Wisconsin, Milwaukee
Julie Frost
Affiliation:
Department of Cellular Biology and Anatomy, Medical College of Wisconsin, Milwaukee
Thuytien Nguyen
Affiliation:
Department of Cellular Biology and Anatomy, Medical College of Wisconsin, Milwaukee
Get access Rights & Permissions [Opens in a new window]

Abstract

Cytochrome-oxidase (CO) histochemistry has revealed important functional subdivisions, modules, and processing streams in the macaque visual cortex. The present study is aimed at analyzing the development and characteristics of CO patterns in the human visual cortex by means of histochemistry and immunohistochemistry. At 26 weeks of gestation, both the ventricular and subventricular zones had low levels of CO, while the cortical plate had moderate levels of CO. At birth, supragranular CO-rich zones (puffs) were not clearly organized, indicating that the development of puffs in the neonatal striate cortex lags behind that of the macaque monkey, whose puffs appear weeks before birth. Puffs were more clearly discernible in human cortex at postnatal day 24, and became well organized by the fourth postnatal month. Layer IVcα in the neonate exhibited a higher level of activity and amount of CO than the central portion of IVcβ, which contained a dense aggregate of small neurons. The base of IVcβ, however, was often as CO reactive as IVcα. In contrast, the majority of specimens available to us from the fourth postnatal month and from adults with no known neurological diseases had significantly greater CO reactivity in layer IVcβ than in IVcaβ. Layer VI was moderately reactive for CO throughout development. In V2, stripes with globular zones of high CO activity were sporadically present at birth, suggesting that their development may parallel or precede that of puffs in VI. These stripes with CO-rich globular zones became more prominent in the adult and radiated orthogonally from the V1/V2 border. They were not, however, clearly organized into alternating thick and thin stripes as they are in the squirrel monkey. Visual cortical areas beyond V2 exhibited high CO activity mainly in layers III and IV and moderate levels in VI, suggesting that sites associated with cortico-cortical pathways may be metabolically most active.

Keywords

Human striate cortexExtrastriate cortexCytochrome-oxidase histochemistry and immunohistochemistryDevelopment of puffs
Type
Research Articles
Information
Visual Neuroscience , Volume 10 , Issue 1 , January 1993 , pp. 41 - 58
Copyright
Copyright © Cambridge University Press 1993

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

Belliveau, J.W., Kennedy, D.N., McKinstry, R.C., Buchbinder, B.R., Weisskoff, R.M., Cohen, M.S., Vevea, J.M., Brady, T.J. & Rosen, B.R. (1991). Functional mapping of the human visual cortex by magnetic resonance imaging. Science 254, 716–719.CrossRefGoogle ScholarPubMed
Boothe, R.G., Dobson, V. & Teller, D.Y. (1985). Postnatal development of vision in human and nonhuman primates. Annual Review of Neuroscience 8, 495–545.CrossRefGoogle ScholarPubMed
Braak, H. (1976). On the striate area of the human isocortex. A Golgi-and pigmentarchitectonic study. Journal of Comparative Neurology 166, 341–364.Google Scholar
Brodmann, K. (1905). Beitrage zur histologischen Lokalisation der Grosshirnrinde. Dritte Mitteilung: Die Rindenfelder der niederen Affen. Journal fur Psychologie und Neurologie 4, 177–226.Google Scholar
Brown, A.M. (1990). Development of visual sensitivity to light and color vision in human infants: A critical review. Vision Research 30, 1159–1188.Google Scholar
Burkhalter, A. & Bernardo, K.L. (1989). Organization of cortico-cortical connections in human visual cortex. Proceedings of the National Academy of Sciences of the U.S.A. 86, 1071–1075.CrossRefGoogle Scholar
Cajal, S., Ramon, Y. (1900–1906). Studien uber die Hirnrinde des Men-schen. Leipzig: J.A. Barth.Google Scholar
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 222, 1–17.Google Scholar
Clarke, S. & Miklossy, J. (1990). Occipital cortex in man: Organization of callosal connections, related myelo- and cytoarchitecture, and putative boundaries of functional visual areas. Journal of Comparative Neurology 298, 188–214.CrossRefGoogle ScholarPubMed
DeYoe, E.A., Hockfield, S., Garren, H. & Van Essen, D.C. (1990). Antibody labeling of functional subdivisions in visual cortex: Cat-301 immunoreactivity in striate and extrastriate cortex of the macaque monkey. Visual Neuroscience 5, 67–81.CrossRefGoogle ScholarPubMed
DeYoe, E.A. & Van Essen, D.C. (1985). Segregation of efferent connections and receptive field properties in visual area V2 of the macaque. Nature, 371 58–61.CrossRefGoogle Scholar
DeYoe, E.A. & Van Essen, D.C. (1988). Concurrent processing streams in monkey visual cortex. Trends in Neuroscience 11, 219–226.Google Scholar
Dobson, V. & Teller, D.Y. (1978). Visual acuity in human infants: A review and comparison of behavioral and electrophysiological studies. Vision Research 18, 1469–1483.Google Scholar
Duckett, S. & Pearse, A.G.E. (1968). The cells of Cajal-Retzius in developing human brain. Journal of Anatomy 102, 183–187.Google ScholarPubMed
Erecinska, M. & Silver, I.A. (1989). ATP and brain function. Journal of Cerebral Blood Flow and Metabolism 9, 2–19.CrossRefGoogle ScholarPubMed
Felleman, D.J. & Van Essen, D.C. (1991). Distributed hierarchical processing in the primate cerebral cortex. Cerebral Cortex 1, 1–47.Google Scholar
Fox, P.T., Meizin, F.M., Allman, J.M., Van Essen, D.C. & Raichle, M.E. (1987). Retinotopic organization of human visual cortex mapped with positron-emission tomography. Journal of Neuroscience 7, 913–922.CrossRefGoogle ScholarPubMed
Fries, W., Keizer, K. & Kuypers, H.G.J.M. (1985). Large layer VI cells in macaque striate cortex (Meynert cells) project to both superior colliculus and prestriate visual area V5. Experimental Brain Research 58, 613–616.Google Scholar
Garey, L.J. & De Courten, C. (1983). Structure development of the lateral geniculate nucleus and visual cortex in monkey and man. Behavioral Brain Research 10, 3–13.Google Scholar
Gwiazda, J., Brill, S., Mohindra, I. & Held, R. (1980). Preferential looking acuity in infants from two to fifty-eight weeks of age. American Journal of Optometry and Physiological Optics 57, 428–432.Google Scholar
Haxby, J.V., Grady, C.L., Horwitz, B., Ungerleider, L.G., Mishkin, M., Carson, R.E., Herscovitch, P., Schapiro, M.B. & Rapoport, S.I. (1991). Dissociation of object and spatial visual processing pathways in human extrastriate cortex. Proceedings of the National Academy of Sciences of the U.S.A. 88, 1621–1625.CrossRefGoogle ScholarPubMed
Hendrickson, A.E. (1985). Dots, stripes, and columns in monkey visual cortex. Trends in Neuroscience 8, 406–410.Google Scholar
Hevner, R.F. & Wong-Riley, M.T.T. (1989). Brain cytochrome oxidase: Purification, antibody production, and immunohistochemical/histochemical correlations in the CNS. Journal of Neuroscience 9, 3884–3898.Google 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.Google Scholar
Hiltgen, G. & Wong-Riley, M.T.T. (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
Hockfield, S., Tootell, R.B.H. & Zaremba, S. (1990). Molecular differences among neurons reveal an organization of human visual cortex. Proceedings of the National Academy of Sciences of the U.S.A. 87, 3027–3031.Google Scholar
Horton, J.C. (1984). Cytochrome oxidase patches: A new cytoarchitectonic feature of monkey visual cortex. Philosophical Transaction of the Royal Society B (London) 304, 199–253.Google Scholar
Horton, J.C. & Hedley-Whyte, E.T. (1984). Mapping of cytochrome oxidase patches and ocular dominance columns in human visual cortex. Philosophical Transaction of the Royal Society B (London) 304, 255–272.Google Scholar
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.Google Scholar
Huttenlocher, P.R. & De Courten, C. (1987). The development of synapses in striate cortex of man. Human Neurobiology 6, 1–9.Google Scholar
Huttenlocher, P.R., De Courten, C., Garey, L.J. & Van der Loos, H. (1982). Synaptogenesis in human visual cortex–Evidence for synapse elimination during normal development. Neuroscience Letters 33, 247–252.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 62, 204–209.Google Scholar
Lennie, P. (1984). Recent development in the physiology of color vision. Trends in Neuroscience 7, 243–248.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. (1984). 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. (1987). Psychophysical evidence for separate channels for the perception of form, color, movement and depth. Journal of Neuroscience 7, 3416–3468.Google Scholar
Livingstone, M. & Hubel, D. (1988). Segregation of form, color, movement and depth: Anatomy, physiology and perception. Science 240, 740–750.Google Scholar
Mann, I. (1964). The Development of the Human Eye. London: British Medical Association.Google Scholar
Mora, B.N., Carman, G.J. & Allman, J.M. (1989). In vivo functional localization of the human visual cortex using positron emission tomography and magnetic resonance imaging. Trends in Neuroscience 12, 282–284.Google Scholar
Purves, D. & Lamantia, A.-S. (1990). Number of “blobs” in the primary visual cortex of neonatal and adult monkeys. Proceedings of the National Academy of Sciences of the U.S.A. 87, 5764–5767.CrossRefGoogle ScholarPubMed
Rakic, P. (1972). Mode of cell migration to the superficial layers of fetal monkey neocortex. Journal of Comparative Neurology 145, 61–84.Google Scholar
Sauer, B., Kammradt, G., Krauthausen, I., Kretschmann, H.-J., Lange, H.W. & Wingert, F. (1983). Qualitative and quantitative development of the visual cortex in man. Journal of Comparative Neurology 214, 441–450.Google Scholar
Schein, S.J. & de Monasterio, F.M. (1987). Mapping of retinal and geniculate neurons onto striate cortex of macaque. Journal of Neuroscience 7, 996–1009.Google Scholar
Spatz, W.B. (1975). An efferent connection of the solitary cells of Meynert. A study with horseradish peroxidase in the marmoset Calli-thrix. Brain Research 92, 450–455.Google Scholar
Teller, D.Y. (1990). The development of visual function in infants. In Vision and the Brain, ed. Cohen, B. & Bodis-Wollner, I., pp. 109–118. New York: Raven Press, Ltd.Google Scholar
Tootell, R.B.H. & Hamilton, S. (1989). Functional anatomy of the second visual area (V2) in the macaque. Journal of Neuroscience 9, 2620–2644.Google Scholar
Tootell, R.B., Silverman, M.S., Devalois, R.L. & Jacobs, G.H. (1983). Functional organization of the second cortical visual area (V2) in the primate. Science 220, 737–739.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.Google Scholar
Van Sluyters, R.C., Atkinson, J., Banks, M.S., Held, R.M., Hoffmann, K.-P. & Shatz, C.S. (1990). The development of vision and visual perception. In Visual Perception. The Neurophysiological Foundations, ed. Spillmann, L. & Werner, J.S., pp. 349–379. New York: Academic Press, Inc.CrossRefGoogle Scholar
Von Economo, C. (1929). The Cytoarchitectonics of the Human Cerebral Cortex. London: Oxford University Press.Google Scholar
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.Google Scholar
Wong-Riley, M.T.T. (1989). Cytochrome oxidase: An endogenous metabolic marker for neuronal activity. Trends in Neuroscience 12, 94–101.Google Scholar
Wong-Riley, M.T.T. (1991). Cytochrome oxidase studies on the human visual cortex. Presented at the Wenner-Gren Center International Symposium on The Functional Organization of the Human Visual Cortex, Stockholm, Sweden.Google Scholar
Wong-Riley, M.T.T. & Carroll, E.W. (1984 a). Quantitative light- and electron-microscopic analysis of cytochrome oxidase-rich zones in V II prestriate cortex of the squirrel monkey. Journal of Comparative Neurology 222, 18–37.Google Scholar
Wong-Riley, M. & Carroll, E.W. (1984 b). The effect of impulse blockage on cytochrome oxidase activity in the monkey visual system. Nature 307, 262–264.Google Scholar
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., Tripathi, S.C., Trusk, T.C. & Hoppe, D.A. (1989). Effects 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., Trusk, T. & Hoppe, D. (1988). Localization of cytochrome oxidase in macaque striate cortex during prenatal development. Society for Neuroscience Abstracts 14, 743.Google Scholar
Yuodelis, C. & Hendrickson, A. (1986). A qualitative and quantitative analysis of the human fovea during development. Vision Research 26, 847–855.Google Scholar
Zeki, S., Watson, J.D.G., Lueck, C.J., Friston, K.J., Kennard, C. & Frackowiak, R.S.J. (1991). A direct demonstration of functional specialization in human visual cortex. Journal of Neuroscience 11, 641–649.Google Scholar