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Organization of ocular dominance and orientation columns in the striate cortex of neonatal macaque monkeys

Published online by Cambridge University Press:  02 June 2009

Gary Blasdel ,
Klaus Obermayer  and
Lynne Kiorpes
Gary Blasdel
Affiliation:
Department of Physiology, University of Calgary, Calgary Alberta, CanadaT2N-1N4 Department of Neurobiology, Harvard Medical School, Boston
Klaus Obermayer
Affiliation:
The Salk Institute, La Jolla The Rockefeller University, New York
Lynne Kiorpes
Affiliation:
Center for Neural Science, New York University, New York
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Abstract

Previous work has shown that small, stimulus-dependent changes in light absorption can be used to monitor cortical activity, and to provide detailed maps of ocular dominance and optimal stimulus orientation in the striate cortex of adult macaque monkeys (Blasdel & Salama, 1986; Ts'o et al., 1990). We now extend this approach to infant animals, in which we find many of the organizational features described previously in adults, including patch-like linear zones, singularities, and fractures (Blasdel, 1992b), in animals as young as 3/12 weeks of age. Indeed, the similarities between infant and adult patterns are more compelling than expected. Patterns of ocular dominance and orientation, for example, show many of the correlations described previously in adults, including a tendency for orientation specificity to decrease in the centers of ocular dominance columns, and for iso-orientation contours to cross the borders of ocular dominance columns at angles of 90 deg. In spite of these similarities, there are differences, one of which entails the strength of ocular dominance signals, which appear weaker in the younger animals and which increase steadily with age. Another, more striking, difference concerns the widths of ocular dominance columns, which increase by 20% during the first 3 months of life. Since the cortical surface area increases by a comparable amount, during the same time, this 20% expansion implies that growth occurs anisotropically, perpendicular to the ocular dominance columns, as the cortical surface expands. Since the observed patterns of orientation preference expand more slowly, at approximately half this rate, these results also imply that ocular dominance and orientation patterns change their relationship, and may even drift past one another, as young animals mature.

Keywords

DevelopmentPrimate striate cortexOcular dominanceOrientation selectivity
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 3 , May 1995 , pp. 589 - 603
Copyright
Copyright © Cambridge University Press 1995

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References

Bartfeld, E. & Grinvald, A. (1992). Relationships between orientation-preference pin-wheels, cytochrome oxidase blobs, and ocular-dominance columns in primate striate cortex. Proceedings of the National Academy of the Sciences of the U.S.A. 89, 11905–11909.CrossRefGoogle ScholarPubMed
Blakemore, C. & Cooper, G.F. (1972). Development of the brain depends on the visual environment. Nature (London) 228, 477–478.CrossRefGoogle Scholar
Blasdel, G.G., Mitchell, D.W., Muir, D.W. & Pettigrew, J.D. (1977). A physiological and behavioral study in cats of the effect of early visual experience with contours of a single orientation. Journal of Physiology (London) 265, 615–635.CrossRefGoogle ScholarPubMed
Blasdel, G.G. (1989). Visualization of neuronal activity in monkey striate cortex. Annual Review of Physiology 51, 561–581.CrossRefGoogle ScholarPubMed
Blasdel, G.G. (1992 a). Differential imaging of ocular dominance and orientation selectivity in monkey striate cortex. Journal of Neuroscience 12, 3117–3138.Google ScholarPubMed
Blasdel, G.G. (1992 b). Orientation selectivity, preference, and continuity in monkey striate cortex. Journal of Neuroscience 12, 3139–3161.CrossRefGoogle ScholarPubMed
Blasdel, G.G. &.Fitzpatrick, D. (1984). Physiological organization of layer 4 in macaque striate cortex. Journal of Neuroscience 4, 880–895.CrossRefGoogle ScholarPubMed
Blasdel, G.G. & Salama, G. (1986). Voltage sensitive dyes reveal a modular organization in monkey striate cortex. Nature 321, 579–585.CrossRefGoogle ScholarPubMed
Blasdel, G.G., Yoshioka, T., Levitt, J.B. & Lund, J.S. (1992). Correlation between patterns of lateral connectivity and patterns of orientation preference in monkey striate cortex. Society for Neuroscience Abstracts 18, 389.Google Scholar
Bonhoeffer, T. & Grinvald, A. (1991). Orientation columns in cat are organized in pin-wheel like patterns. Nature 353, 429–431.CrossRefGoogle Scholar
Callaway, E. & Katz, L. (1992). Development of axonal arbors of layer 4 spiny neurons in cat striate cortex. Journal of Neuroscience 12, 570–582.CrossRefGoogle ScholarPubMed
DesRosiers, M.H., Sakurada, O., Jehle, J., Shinohara, M., Kennedy, C. & Sokoloff, L. (1978). Functional plasticity in the immature striate cortex of the monkey shown by the [14C] deoxyglucose method. Science 200, 447–449.CrossRefGoogle Scholar
Gilbert, C.D. & Wiesel, T.N. (1992). Receptive field dynamics in adult primary visual cortex. Nature 356, 150–152.CrossRefGoogle ScholarPubMed
Hirsch, H.V.B. & Spinelli, D.N. (1970). Visual experience modifies distribution of horizontal and vertical oriented receptive fields in cats. Science (N.Y.) 168, 869–871.CrossRefGoogle ScholarPubMed
Hirsch, H.V.B. & Spinelli, D.N. (1971). Modification of the distribution of receptive-field orientation in cats by selected visual experiences during development. Experimental Brain Research 13, 509–527.Google Scholar
Hubel, D.H. & Wiesel, T. (1962). Receptive fields, binocular interaction, and functional architecture of cat striate cortex. Journal of Physiology (London) 160, 106–154.CrossRefGoogle Scholar
Hubel, D.H. & Wiesel, T. (1968). Receptive fields and functional architecture of monkey striate cortex. Journal of Physiology (London) 195, 215–243.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1972). Laminar and columnar distribution of geniculo-cortical fibers in the macaque monkey. Journal of Comparative Neurology 146, 421–450.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1974 a). Sequence regularity and geometry of orientation columns in the monkey striate cortex. Journal of Comparative Neurology 158, 267–294.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1974 b). Uniformity of monkey striate cortex: A parallel relationship between field size, scatter, and magnification factor. Journal of Comparative Neurology 158, 295–306.CrossRefGoogle ScholarPubMed
Kiorpes, L. & Blasdel, G.G. (1987). Optical studies of macaque striate cortex during development. Neuroscience Abstract 13, 11243.Google Scholar
LeVay, S., Hubel, D.H. & Wiesel, T.N. (1975). The pattern of ocular dominance columns in macaque striate cortex revealed by a reduced silver stain. Journal of Comparative Neurology 159, 559–576.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
Obermayer, K. – Blasdel, G.G. (1993). Geometry of orientation and ocular dominance columns in monkey striate cortex. Journal of Neuroscience 13, 4114–4129.CrossRefGoogle ScholarPubMed
Obermayer, K., Blasdel, G.G. & Schulten, K. (1991). A neural network model for the formation and for the spatial structure of retinotopic maps, orientation and ocular dominance columns. In Artificial Neural Networks, ed. Kohonen, T., et al., pp. 505–511. Amsterdam, The Netherlands: Elsevier (North Holland).Google Scholar
Obermayer, K., Blasdel, G.G. & Schulten, K. (1992 a). A statistical mechanical analysis of self-organization and pattern formation during the development of visual maps. Physiological Reviews A 45, 7568–7589.CrossRefGoogle ScholarPubMed
Obermayer, K., Schulten, K. & Blasdel, G.G. (1992 b). A comparison of a neural network model for the formation of brain maps with experimental data. In Advance in Neural Information Processing Systems, ed. Touretzky, D.S. & Lippman, R., pp. 83–90. San Mateo, CA: Morgan Kaufmann Publishers.Google Scholar
Obermayer, K., Kiorpes, L. & Blasdel, G.G. (1994). Development of orientation and ocular dominance columns in infant macaques. In Advances in Neural Information Processing Systems 6, ed. Cowan, J., Tesauro, G., & Alspector, J., pp. 543–550. San Mateo: CA: Morfan Kaufmann Publishers.Google Scholar
Pettet, M.W. & Gilbert, C.D. (1992). Dynamic changes in receptive field size in cat primary visual cortex. Proceedings of the National Academy of the Sciences of the U.S.A. 89, 8366–8370.CrossRefGoogle ScholarPubMed
Pettigrew, J.D., Cooper, M.L. & Blasdel, G.G. (1979). Improved use of tapetal reflection for eye position monitoring. Investigative Ophthalmology and Visual Science 18, 490–495.Google ScholarPubMed
Press, W.H., Flannery, B.P., Teukolsky, S.A. & Vetterling, W.T. (1988). Numerical Recipes in C. Cambridge, MA: Cambridge University Press.Google Scholar
Purves, D. & Lamantia, A. (1993). Development of blobs in the visual cortex of macaques. Journal of Comparative Neurology 332, 1–7.Google Scholar
Rakic, P. (1976). Prenatal genesis of connections subserving ocular dominance in the rhesus monkey. Nature (London) 261, 467–471.CrossRefGoogle ScholarPubMed
Stryker, M.P. & Sherk, H. (1975). Modification of cortical orientation-selectivity in the cat by restricted visual experience: A reexamination. Science 190, 904–906.CrossRefGoogle ScholarPubMed
Swindale, N.V. (1982). A model for the formation of orientation columns. Proceedings Royal Society B (London) 215, 211–230.Google Scholar
Swindale, N.V. (1992). A model for the coordinated development of columnar systems in primate striate cortex. Biological Cybernetics 66, 217–230.CrossRefGoogle Scholar
Tootell, R.H., Switkes, E., Silverman, M.S. & Hamilton, S.L. (1988). Functional anatomy of macaque striate cortex. II. Retino-topic organization. Journal of Neuroscience 8(5), 1531–1568.CrossRefGoogle Scholar
T'so, D.Y., Frostig, R.D., Lieke, E.E. & Grinvald, A. (1990). Functional organization of primate visual cortex revealed by high resolution optical imaging. Science 249, 417–420.Google Scholar
Van Essen, D.C., Newsome, W.T. & Maunsell, H.R. (1984). The visual field representation in striate cortex of the macaque monkey: Asymmetries, anisotropies, and individual variability. Vision Research 24, 429–448.CrossRefGoogle ScholarPubMed
Wiesel, T.N. & Hubel, D.H. (1974). Ordered arrangement of orientation columns in monkeys lacking visual experience. Journal of Comparative Neurology 158, 307–318.CrossRefGoogle ScholarPubMed
Wolbarsht, M.L., MacNichol, E.F. & Wagner, H.G. (1960). Glass insulated platinum microelectrode. Science 132, 1309–1310.CrossRefGoogle ScholarPubMed
Yoshioka, T., Blasdel, G., Levitt, J. & Lund, J.S. (1992). Patterns of lateral connections in macaque visual area VI revealed by biocytin histochemistry and functional imaging. Society for Neuroscience Abstracts 18, 299.Google Scholar
Yoshioka, T., Blasdel, G.G., Levitt, J.B. & Lund, J.S. (1995). Relation between patterns of intrinsic lateral connectivity, ocular dominance, and cytochrome oxidase-reactive regions in macaque monkey striate cortex. Cerebral cortex (in press).Google Scholar