Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-27T10:57:30.109Z Has data issue: false hasContentIssue false
  • English
  • Français

Ocular dominance columns in area 17 of Old World macaque and talapoin monkeys: Complete reconstructions and quantitative analyses

Published online by Cambridge University Press:  02 June 2009

S. L. Florence  and
J. H. Kaas
S. L. Florence
Affiliation:
Department of Psychology, Vanderbilt University, Nashville
J. H. Kaas
Affiliation:
Department of Psychology, Vanderbilt University, Nashville
Get access Rights & Permissions [Opens in a new window]

Abstract

The effects of monocular deprivation on cytochrome-oxidase (CO) expression were used to reveal ocular dominance columns in flatmounts of the striate cortex in macaque (Macaca fascicularis) and talapoin (Miopithecus talapoin) monkeys. This procedure allowed the first direct visualization of the complete pattern of ocular dominance bands in macaque monkeys, and less complete reconstructions in talapoin monkeys. In a second macaque monkey, the ocular dominance organization was revealed by injecting wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP) into one eye.

The organization of ocular dominance columns in the macaque monkeys conforms to previous descriptions, but the flat-mounted hemispheres provide accurate details on (1) the arrangement of columns, (2) the orientation of the representation of the optic disc, and (3) the breakdown of the bands in the cortex between the optic disc and monocular representations into a pattern of dots activated by the ipsilateral eye and larger surrounds related to the contralateral eye.

Talapoin monkeys, the smallest of Old World monkeys, have sharply segregated ocular dominance bands. The columns in talapoins are narrower than those in macaques, so that even with less striate cortex than macaques, talapoins have more ocular dominance hypercolumns.

Keywords

HypercolumnsStriate cortexCytochrome oxidase
Type
Research Articles
Information
Visual Neuroscience , Volume 8 , Issue 5 , May 1992 , pp. 449 - 462
Copyright
Copyright © Cambridge University Press 1992

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

Anderson, P.A., Olavarria, J. & Van, Sluyters R.C. (1988). The overall pattern of ocular dominance bands in cat visual cortex. Journal of Neuroscience 8, 2183–2200.Google Scholar
Blasdel, G.G. & Salama, G. (1986). Voltage sensitive dyes reveal a modular organization in monkey striate cortex. Nature 321, 579–585.CrossRefGoogle ScholarPubMed
Brodmann, K. (1909). Vergleichende Lokalisationslehre der Grosshirnrinde. Barth: Leipzig.Google Scholar
Casagrande, V.A. & Debruyn, E.J. (1982). The galago visual system: Aspects of normal organization and developmental plasticity. In The Lesser Bushbaby (Galago) as an Animal Model: Selected Topics, ed. Haines, D.E., pp. 137–168. Boca Raton, Florida: CRC Press.Google Scholar
Casagrande, V.A. & Harting, J.K. (1975). Transneuronal transport of tritiated fucose and proline in the visual pathways of tree shrew, Tupaia glis. Brain Research 96, 367–372.CrossRefGoogle ScholarPubMed
Casagrande, V.A. & Skeen, L.C. (1980). Organization of ocular dominance columns in galago demonstrated by autoradiographic and deoxyglucose methods. Society for Neuroscience Abstracts 6, 315.Google Scholar
Condo, G.J. & Casagrande, V.A. (1990). Organization of cytochrome oxidase staining in the visual cortex of nocturnal primates (Galago crassicaudatus and Galago senegalensis): I. Adult patterns. Journal of Comparative Neurology 293, 632–645.Google Scholar
Conley, M., Fitzpatrick, D. & Diamond, I.T. (1984). The laminar organization of the lateral geniculate body and striate cortex in the tree shrew (Tupaia glis). Journal of Neuroscience 4, 171–198.CrossRefGoogle ScholarPubMed
Connolly, M. & Van, Essen D.C. (1984). The representation of the visual field in parvicellular and magnocellular laminae of the lateral geniculate nucleus in the macaque monkey. Journal of Comparative Neurology 226, 544–564.CrossRefGoogle ScholarPubMed
Constantine-Paton, M. (1982). The retinotectal hookup: The process of neural mapping. In Developmental Order: Its Origin and Regulation, ed. Substelny, S., pp. 317–349. New York: Alan R. Liss, Inc.Google Scholar
Dandona, L., Hendrickson, A. & Quigley, H.A. (1991). Selective effects of experimental glaucoma on axonal transport by retinal ganglion cells to the dorsal lateral geniculate nucleus. Investigative Ophthalmology and Visual Science 32, 1593–1599.Google Scholar
Debruyn, E.J. & Casagrande, V.A. (1981). Demonstration of ocular dominance columns in a New World primate by means of monocular deprivation. Brain Research 207, 453–458.CrossRefGoogle Scholar
Diamond, I.T., Conley, M., Itoh, K. & Fitzpatrick, D. (1985). Laminar organization of geniculocortical projections in Galago senegalensis and Aotus trivirgatus. Journal of Comparative Neurology 242, 584–610.CrossRefGoogle ScholarPubMed
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
Fleagle, J.G. (1988). Primate Adaptation and Evolution. New York: Academic Press, Inc.Google Scholar
Florence, S.L., Conley, M. & Casagrande, V.A. (1986). Ocular dominance columns and retinal projections in New World spider monkeys (Ateles ater). Journal of Comparative Neurology 243, 234–248.CrossRefGoogle ScholarPubMed
Florence, S.L. & Kaas, J.H. (1990). Ocular dominance segregation in the New World talapoin monkey. Investigative Ophthalmology and Visual Science 31, 272.Google Scholar
Gallyas, F. (1979). Silver straining of myelin by means of physical development. Neurology Research 1, 203–291.CrossRefGoogle Scholar
Glendenning, K.K., Kofron, E.A. & Diamond, I.T. (1976). Laminar organization of projections of the lateral geniculate nucleus to the striate cortex in Galago. Brain Research 105, 538–546.Google Scholar
Grehn, F. & Prost, M. (1983). Function of retinal nerve fibers depends on perfusion pressure: Neurophysiologic investigations during acute intraocular pressure elevation. Investigative Ophthalmology and Visual Science 24, 347.Google ScholarPubMed
Haseltine, E.C., Debruyn, E.J. & Casagrande, V.A. (1979). Demonstration of ocular dominance columns in Nissl-stained sections of monkey visual cortex following enucleation. Brain Research 176, 153–158.CrossRefGoogle ScholarPubMed
Fiassler, R. (1966). Comparative anatomy in the central visual systems in day- and night-active primates. In Evolution of the Forebrain, ed. Hassler, R. & Stephen, H., Stuttgart: Thieme.Google Scholar
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.Google Scholar
Hendrickson, A.E., Wilson, J.R. & Ogren, M.P. (1978). The neuro-anatomical organization of pathways between the dorsal lateral geniculate nucleus and visual cortex in Old World and New World Primates. Journal of Comparative Neurology 182, 123–136.CrossRefGoogle Scholar
Hess, D.T. & Edwards, M.A. (1987). Anatomical demonstration of ocular dominance segregation in the retinogeniculocortical pathway of the New World capuchin monkey (Cebus apella). Journal of Comparative Neurology 264, 409–420.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Hitchcock, P.F. & Hickey, T.L. (1980). Ocular dominance columns: Evidence for their presence in humans. Brain Research 182, 176–179.CrossRefGoogle ScholarPubMed
Horton, J.C. & Hedley-Whyte, E.T. (1984). Mapping of cytochrome oxidase patches and ocular dominance columns in human visual cortex. Philosophical Transactions of the Royal Society (London) 304, 255–272.Google Scholar
Horton, J.C. & Hubel, D.H. (1981). Regular patch distribution of cytochrome oxidase staining in primary visual cortex of macaque monkey. Nature 292, 762–764.CrossRefGoogle Scholar
Horton, J.C., Dagi, L.R., Mccrane, E.P. & De, Monasterio F.M. (1990). Arrangement of ocular dominance columns in human visual cortex. Archives of Ophthalmology 108, 1025–1031.CrossRefGoogle ScholarPubMed
Hubel, D.H. (1975). An autoradiographic study of the retino-cortical projections in the tree shrew (Tupaia glis). Brain Research 96, 41–50.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1968). Receptive fields and functional architecture of monkey striate cortex. Journal of Physiology (London) 195, 215–243.Google Scholar
Hubel, D.H. & Wiesel, T.N. (1972). Laminar and columnar distribution of geniculocortical fibers in macaque monkey. Journal of Comparative Neurology 146, 421–450.Google Scholar
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.Google Scholar
Hubel, D.H. & Wiesel, T.N. (1977). Functional architecture of macaque monkey visual cortex. Proceedings of the Royal Society (London) 198, 1–59.Google Scholar
Hubel, D.H. & Wiesel, T.N. (1978). Distribution of inputs from the two eyes to striate cortex of squirrel monkeys. Society for Neuroscience Abstracts 4, 632.Google Scholar
Hubel, D.H., Wiesel, T.N. & Levay, S. (1976). Functional architecture of area 17 in normal and monocularly deprived macaque monkeys. Cold Springs Harbor Symposium in Quantitative Biology 40, 581–589.CrossRefGoogle ScholarPubMed
Hubel, D.H., Wiesel, T.N. & Levay, S. (1977). Plasticity of ocular dominance columns in monkey striate cortex. Philosophical Transactions of the Royal Society (London) 278, 377–409.Google Scholar
Hubel, D.H., Wiesel, T.N. & Stryker, M.P. (1978). Anatomical demonstration of orientation columns in macaque monkey. Journal of Comparative Neurology 177, 361–380.CrossRefGoogle ScholarPubMed
Huerta, M.F. & Harting, J.K. (1984). The mammalian superior colliculus: Studies of its morphology and connections. In Comparative Neurology of the Optic Tectum, ed. Vanegas, H., pp. 687–773. New York: Plenum Press.CrossRefGoogle Scholar
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
Itaya, S.K., Itaya, P.W. & Van, Hoesen G.W. (1984). Intracortical termination of the retino-geniculo-striate pathway studied with trans-synaptic tracer (wheat germ agglutinin-horseradish peroxidase) and cytochrome oxidase staining in the macaque monkey. Brain Research 304, 303–310.Google Scholar
Itaya, S.K. & Van, Hoesen G.W. (1982). WGA-HRP as a transneuronal marker in the visual pathways of monkey and rat. Brain Research 236, 199–204.CrossRefGoogle ScholarPubMed
Kaas, J.H. (1990). Processing areas and modules in the sensory-perceptual cortex. In Signal and Sense: Local and Global Order in Perceptual Maps, ed. Edelman, G.M., Gall, W.E. & Cowan, W.M., pp. 67–82. New York: John Wiley & Sons.Google Scholar
Kaas, J.H., Lin, C.-S. & Casagrande, V.A. (1976). The relay of ipsilateral and contralateral retinal input from the lateral geniculate nucleus to striate cortex in the owl monkey: A transneuronal transport study. Brain Research 106, 371–378.Google Scholar
Kaas, J.H., Huerta, M.F. & Harting, J.K. (1978). Patterns of retinal terminations and laminar organization in the lateral geniculate nucleus of primates. Journal of Comparative Neurology 182, 517–554.Google Scholar
Kaas, J.H. & Krubitzer, L.A. (1990). The Organization Of Visual Cortex In Old World Monkeys: Studies On Miniature Species, Miopithecus talapoin. Investigative Ophthalmology and Visual Science 31, 398.Google Scholar
Kaas, J.H. & Preuss, T.M. (1991). Archontan affinities as reflected in the visual system. In Mammal Phylogeny, ed. Szalay, F., Novacek, M. & Mckenna, M.New York: Springer-Verlag (in press).Google Scholar
Kennedy, C., Des, Rosiers M.H., Jehle, J.W., Reivich, M., Sharp, F. & Sokoloff, L. (1975). Mapping of functional neural pathways by autoradiographic survey of local metabolic rate with [14C]deoxyglucose. Science 187, 850–853.CrossRefGoogle ScholarPubMed
Krubitzer, L.A. & Kaas, J.H. (1990). Cortical connections of MT in four species of primates: Areal, modular, and retinotopic patterns. Visual Neuroscience 5, 165–204.Google Scholar
Lachica, E.A. & Casagrande, V.A. (1988). Development of primate retinogeniculate axon arbors. Visual Neuroscience 1, 103–123.CrossRefGoogle ScholarPubMed
Levay, S., Connolly, M., Houde, J. & Van, Essen D.C. (1985). The complete pattern of ocular dominance stripes in the striate cortex and visual field of the macaque monkey. Journal of Neuroscience 5, 486–501.Google Scholar
Levay, S., Hubel, D.H. & Wiesel, T.N. (1975). The pattern of ocular dominance columns in macaque visual cortex revealed by a reduced silver stain. Journal of Comparative Neurology 159, 559–576.Google Scholar
Levay, S., Styker, M.P. & Shatz, C.J. (1978). Ocular dominance columns and their development in layer IV of cat's visual cortex: A quantitative study. Journal of Comparative Neurology 179, 223–244.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.Google Scholar
Lowel, S. & Singer, W. (1987). The pattern of ocular dominance columns in flat-mounts of the cat visual cortex. Experimental Brain Research 68, 661–666.CrossRefGoogle ScholarPubMed
Malpeli, J.G. & Baker, F.H. (1975). The representation of the visual field in the lateral geniculate nucleus of Macaca mullata. Journal of Comparative Neurology 161, 569–594.Google Scholar
Martin, R.D. (1990). Primate Origins and Evolution: A Phylogenetic Reconstruction. Princeton: Princeton University Press.Google Scholar
Mesulam, M.-M (1978). Tetramethylbenzidine for horseradish peroxidase neurohistochemistry: A non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. Journal of Histochemistry and Cytochemistry 26, 106–117.Google Scholar
Olavarria, J. & Van, Sluyters R.C. (1985). Unfolding and flattening the cortex of gyrencephalic brains. Journal of Neuroscience Methods 15, 191–202.CrossRefGoogle ScholarPubMed
Purves, D. & Lamantia, A-S. (1990). Numbers of “blobs” in the primary visual cortex of neonatal and adult monkeys. Proceedings of the National Academy of Science of the U.S.A. 87, 5764–5767.Google Scholar
Rakic, P. (1977). Prenatal development of the visual system in rhesus monkey. Philosophical Transactions of the Royal Society (London) 278, 245–260.Google Scholar
Rosa, M.G.P., Gattass, R. & Fiorani, M. Jr. (1988a). Complete pattern of ocular dominance stripes in VI of the New World monkey, Cebus apella. Experimental Brain Research 72, 645–648.CrossRefGoogle Scholar
Rosa, M.G.P., Sousa, A.P.B. & Gattass, R. (1988b). Representation of the visual field in the second visual area in the cebus monkey. Journal of Comparative Neurology 275, 326–345.CrossRefGoogle ScholarPubMed
Rowe, M.H., Benevento, L.A. & Rezak, M. (1978). Some observations on the patterns of segregated geniculate inputs to the visual cortex in New World primates: An autoradiographic study. Brain Research 159, 371–378.Google Scholar
Shou, T. & Zhou, Y. (1989). Y Cells in the cat retina are more tolerant than X cells to brief elevation of IOP. Investigative Ophthalmology and Visual Science 30, 2093.Google Scholar
Spatz, W.B. (1979). The retino-geniculo-cortical pathway in Callithrix. II. The geniculo-cortical projection. Experimental Brain Research 36, 401–410.CrossRefGoogle ScholarPubMed
Spatz, W.B. (1989). Loss of ocular dominance columns with maturity in the monkey, Callithrix jacchus. Brain Research 488, 376–380.Google Scholar
Stensaas, S.S., Eddington, D.K. & Dobelle, W.H. (1974). The topography and variability of the primary visual cortex in man. Journal of Neurosurgery 40, 747–755.CrossRefGoogle ScholarPubMed
Stone, J. & Johnson, E. (1981). The topography of primate retina: A study of the human, bushbaby, and New- and Old-World monkeys. Journal of Comparative Neurology 196, 205–223.Google Scholar
Swindale, N.V. (1980). A model for the formation of ocular dominance stripes. Proceedings of the Royal Society (London) 208, 243–264.Google Scholar
Szaley, F.S. & Delson, E. (1979). Evolutionary History of the Primates. New York: Academic Press.Google Scholar
Tanaka, S. (1991). Theory of ocular dominance column formation. Biological Cybernetics 64, 263–272.CrossRefGoogle ScholarPubMed
Tigges, M., Hendrickson, A.E. & Tigges, J. (1984). Anatomical consequences of long-term monocular eyelid closure on lateral geniculate nucleus and striate cortex in squirrel monkey. Journal of Comparative Neurology 227, 1–13.Google Scholar
Tigges, J. & Tigges, M. (1979). Ocular dominance columns in the striate cortex of chimpanzee (Pan troglodytes). Brain Research 166, 386–390.Google Scholar
Tigges, J., Tigges, M. & Perachio, A.A. (1977). Complementary laminar termination of afferents to area 17 originating in area 18 and in the lateral geniculate nucleus in squirrel monkey. Journal of Comparative Neurology 176, 87–100.Google Scholar
Tooteli, R.B., Hamilton, S.L., Silverman, M.S. & Switkes, E. (1988). Functional anatomy of macaque striate cortex. I. Ocular dominance, binocular interactions, and baseline conditions. Journal of Neuroscience 8, 1500–1530.CrossRefGoogle Scholar
Van, Essen D.C., Newsome, W.T. & Maunsell, J.H.R. (1984). The visual field representation in striate cortex of the macaque monkey: Asymmetries, anisotropies, and individual variability. Vision Research 24, 429–448.Google Scholar
Von, Der Malsburg C. (1979). Development of ocularity domains and growth behavior of axon terminals. Biological Cybernetics 32, 49–62.Google Scholar
Weber, J.T., Casagrande, V.A. & Harting, J.K. (1977). Transneuronal transport of [3H]proline within the visual system of the grey squirrel. Brain Research 129, 346–352.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.Google Scholar
Weller, R. & Kaas, J.H. (1983). Retinotopic patterns of connections of area 17 with visual areas V-II and MT in macaque monkeys. Journal of Comparative Neurology 220, 253–279.Google Scholar
Wiesel, T.N., Hubel, D.H., & Lam, D.M.-K. (1974). Autoradiographic demonstration of ocular dominance columns in the monkey striate cortex by means of transneuronal transport. Brain Research 79, 273–279.Google Scholar