Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-25T06:00:04.325Z Has data issue: false hasContentIssue false

Binocular competition affects the pattern and intensity of ocular activation columns in the visual cortex of cats

Published online by Cambridge University Press:  02 June 2009

N. Tumosa
Affiliation:
Neurobiology Research Center and Department of Biological Sciences, State University of New York, Albany
S. B. Tieman
Affiliation:
Neurobiology Research Center and Department of Biological Sciences, State University of New York, Albany
D. G. Tieman
Affiliation:
Neurobiology Research Center and Department of Biological Sciences, State University of New York, Albany

Abstract

The effect of binocular competition on the development of ocular activation columns in areas 17 and 18 of cats was studied using the 14C-2-deoxyglucose (14C-2DG) technique to visualize the regions of cortex activated by one eye in cats reared with equal alternating monocular exposure (equal AME), unequal AME, or monocular deprivation (MD). The average size of the ocular activation columns of the eye stimulated during administration of 2DG was positively correlated with the competitive advantage during rearing. In order of increasing percentage of visual cortex activated, the eyes were (1) deprived eye of MD cats, (2) less experienced eye of unequal AME cats, (3) either eye of equal AME cats, (4) more experienced eye of unequal AME cats, and (5) experienced eye of MD cats. In area 17, the shape of the activation columns also was affected by the relative experience of the eye. The columns of the deprived eye of MD cats were widest in layer IV, where they were about the same width as those of the less experienced eye of the unequal AME cats; in other layers they were narrower, sometimes disappearing altogether. In contrast, the activation columns of the less experienced eye of the unequal AME cats were about the same width in all layers. These results suggest that when one eye is placed at a severe disadvantage and receives no patterned input, as in MD, both geniculocortical connections and intracortical connections may be disrupted, but when the disadvantage is less, as in unequal AME, only the geniculocortical connections are disrupted.

Binocular competition also affected the intensity of activation within columns in area 17. We used video densitometry to determine ratios of the amount of label in cortical and thalamic structures. Both the ratio of label in area 17 to that in the lateral geniculate nucleus (LGN) and the ratio of label in the binocular segment of area 17 to that in the monocular segment were significantly less for the deprived eye of MD cats than for any other group. These results suggest that even within the smaller activation columns, deprived geniculocortical afferents are relatively ineffective at driving cortical cells. This finding is consistent with earlier reports that the synapses from the deprived pathway are both morphologically abnormal and reduced in number. The cortical labeling for the less experienced eye of the unequal AME cats and the experienced eye of the MD cats were also significantly less than that in equal AME cats. The decreased labeling for the experienced eye activation columns suggests that, in order to cover an abnormally large area, afferents representing the experienced eye must make fewer synaptic contacts within that area and that there are intrinsic limits on the number of synapses that one axon can make.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1989

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, 21832200.CrossRefGoogle ScholarPubMed
Bienenstock, E.L., Cooper, L. N. & Munro, P.W. (1982). Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. Journal of Neuroscience 2, 3248.CrossRefGoogle ScholarPubMed
Blake, R. & Hirsch, H.V.B. (1975). Deficits in binocular depth perception in cats after alternating monocular deprivation. Science 19, 11141116.CrossRefGoogle Scholar
Blakemore, C. (1976). The conditions required for the maintenance of binocularity in kitten's visual cortex. Journal of Physiology (London) 261, 423444.CrossRefGoogle ScholarPubMed
Bonds, A.B., Silverman, M.S., Sclar, G. & Tootell, R.B. (1980). Visually evoked potentials and deoxyglucose studies of monocularly deprived cats. Investigative Ophthalmology and Visual Science (Suppl.) 19, 225.Google Scholar
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, 447449.CrossRefGoogle Scholar
Devor, M. & Schneider, G.E. (1975). Neuroanatomical plasticity: the principle of conservation of total axonal arborization. In Aspects of Neuronal Plasticity, ed. Vital-Durand, F. & Jeannerod, M., pp. 191201. Paris, France: INSERM.Google Scholar
Dreher, B., Leventhal, A.G. & Hale, P.T. (1980). Geniculate input to cat visual cortex: a comparison of area 19 with areas 17 and 18. Journal of Neurophysiology 44, 804826.CrossRefGoogle Scholar
Freeman, R.D. (1978). Visuomotor restrictions of one eye in kittens reared with alternate monocular deprivation. Experimental Brain Research 33, 5163.CrossRefGoogle ScholarPubMed
Friedlander, M.J. & Stanford, L.R. (1984). Effects of monocular deprivation on the distribution of cell types in the LGNd. A sampling study with fine-tipped micropipettes. Experimental Brain Research 53, 451461.CrossRefGoogle ScholarPubMed
Friedlander, M.J., Stanford, L.R. & Sherman, S.M. (1982). Effects of monocular deprivation on the structure-function relationship of individual neurons in the cat's lateral geniculate nucleus. Journal of Neuroscience 2, 321330.CrossRefGoogle ScholarPubMed
Friedland, M.J., Stanford, L.R. & Sherman, S.M. (1982). Effects of monocular deprivation on the structure-function relationship of individual neurons in the cat's lateral geniculate nucleus. Journal of Neuroscience 2, 321330.CrossRefGoogle Scholar
Freund, T.F., Martin, K.A.C. & Whitteridge, D. (1985). Innervation of cat visual areas 17 and 18 by physiologically identified X-and Y-type thalamic afferents. I. Arborization patterns and quantitative distribution of postsynaptic elements. Journal of Comparative Neurology 242, 263274.CrossRefGoogle ScholarPubMed
Ganz, L., Fitch, M. & Satterberg, J.A. (1968). The selective effect of visual deprivation on receptive-field shape determined neu-rophysiologically. Experimental Neurology 22, 614637.CrossRefGoogle Scholar
Ganz, L., Hirsch, H.V.B. & Tieman, S.B. (1972). The nature of perceptual deficits in visually deprived cats. Brain Research 44, 547568.CrossRefGoogle ScholarPubMed
Garey, L.J. & Blakemore, C. (1977). Monocular deprivation, morphological effects on different classes of neurons in the lateral geniculate nucleus. Science 195, 414416.CrossRefGoogle ScholarPubMed
Geisert, E.E. (1987). Effects of monocular deprivation on the cat's geniculate neurons projecting to both areas 17 and 18. Journal of Comparative Neurology 255, 416424.CrossRefGoogle Scholar
Hickey, T.L., Spear, P.D. & Kratz, K.E. (1977). Quantitative studies of cell size in the cat's dorsal lateral geniculate nucleus following visual deprivation. Journal of Comparative Neurology 172, 265282.CrossRefGoogle ScholarPubMed
Hirsch, H.V.B., Tieman, D.G., Tieman, S.B. & Tumosa, N. (1987). Unequal alternating exposure: effects during and after the classical critical period. In Imprinting and Cortical Plasticity, ed. Raus-Checker, J.P. & Marler, P., pp. 286320, New York: Wiley.Google Scholar
Hubel, D.H. (1959). Single unit activity in striate cortex of unrestrained cats. Journal of Physiology (London) 147, 226238.CrossRefGoogle ScholarPubMed
Hubel, D.H. (1960). Single unit activity in lateral geniculate body and optic tract of unrestrained cats. Journal of Physiology (London) 150, 91104.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1965 a). Receptive fields and functional architecture in two nonstriate visual areas (18 and 19) of the cat. Journal of Neurophysiology 28, 229289.CrossRefGoogle Scholar
Hubel, D.H. & Wiesel, T.N. (1965 b). Binocular interaction in striate cortex of kittens reared with artificial squint. Journal of Neurophysiology 28, 10411059.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1970). The period of susceptibility to the physiological effects of unilateral eye closure in kittens. Journal of Physiology (London) 206, 419436.CrossRefGoogle Scholar
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, 377409.Google 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, 345358.CrossRefGoogle ScholarPubMed
Humphrey, A.L., Sur, M., Uhlrich, D.J. & Sherman, S.M. (1985). Projection patterns of individual X- and Y-cell axons from the lateral geniculate nucleus to cortical area 17 in the cat. Journal of Comparative Neurology 233, 158189.Google ScholarPubMed
Kelly, P.A.T. & McCulloch, J. (1983). A critical appraisal of semi-quantitative analysis of 2-deoxyglucose autoradiograms. Brain Research 269, 165167.CrossRefGoogle ScholarPubMed
Kennedy, C, DesRosiers, M.H., Sakurada, O., Shinohara, M., Reivich, M., Jehle, J.W. & Sokoloff, L. (1976). Metabolic mapping of the primary visual system of the monkey by means of the autoradiographic [14C]-deoxyglucose technique. Proceedings of the National Academy of Sciences of the U.S.A. 73, 42304234.CrossRefGoogle ScholarPubMed
Kossut, M., Thompson, I.D. & Blakemore, C. (1983). Ocular dominance columns in cat striate cortex and effects of monocular deprivation: a 2-deoxyglucose study. Acta Neurobiologiae Experimentalis 43, 273282.Google ScholarPubMed
Kratz, K.E., Spear, P.D. & Smith, D.C. (1976). Postcritical-period reversal of effects of monocular deprivation on striate cortex cells in the cat. Journal of Neurophysiology 39, 501511.CrossRefGoogle ScholarPubMed
LeVay, S. & Ferster, D. (1977). Relay cell classes in the lateral geniculate nucleus of the cat and the effects of visual deprivation. Journal of Comparative Neurology 172, 563584.CrossRefGoogle Scholar
LeVay, S., Stryker, M.P. & Shatz, C.J. (1978). Ocular dominance columns and their development in layer IV of the cat's visual cortex: a quantitative study. Journal of Comparative Neurology 179, 223244.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 190, 151.Google Scholar
Lin, C.-S. & Sherman, S.M. (1978). Effects of early monocular eyelid suture upon development of relay cell classes in the cat's lateral geniculate nucleus. Journal of Comparative Neurology 181, 809832.CrossRefGoogle ScholarPubMed
Malsburg, C. Von Der (1979). Development of ocularity domains and growth behavior of axon terminals. Biological Cybernetics 32, 4962.CrossRefGoogle ScholarPubMed
Mitchell, D.E., Cynader, M. & Movshon, J.A. (1977). Recovery from the effects of monocular deprivation in kittens. Journal of Comparative Neurology 395, 639660.Google Scholar
Mitchell, I.J. & Crossman, A.R. (1984). In defence of optical density ratios in 2-deoxyglucose autoradiography. Brain Research 298, 191192.CrossRefGoogle ScholarPubMed
Movshon, J.A. & Dürsteler, M.R. (1977). Effects of brief periods of unilateral eye closure on the kitten's visual system. Journal of Neurophysiology 40, 12551265.CrossRefGoogle ScholarPubMed
Mustari, M. & Cynader, M. (1981). Prior strabismus protects kitten cortical neurons from the effects of monocular deprivation. Brain Research 211, 165170.CrossRefGoogle ScholarPubMed
Olson, C.R. & Freeman, R.D. (1980). Profile of the sensitive period for monocular deprivation in kittens. Experimental Brain Research 39, 1721.CrossRefGoogle ScholarPubMed
Otsuka, R. & Hassler, R. (1962). Über Aufbau und Gliederung der corticalen Sehsphäre bei der Katze. Archiv für Psychiatrie und Zeit-schrift für die Gesamte Neurologie 203, 212234.CrossRefGoogle Scholar
Page, E.B. (1963). Ordered hypotheses for multiple treatments: a significance test for linear ranks. Journal of the American Statistical Association 58, 216230.CrossRefGoogle Scholar
Peck, C.K. & Blakemore, C. (1975). Modification of single neurons in the kitten's visual cortex after brief periods of monocular visual exposure. Experimental Brain Research 22, 5768.CrossRefGoogle Scholar
Presson, J. & Gordon, B. (1979). Critical period and minimum exposure required for the effects of alternating monocular occlusion in cat visual cortex. Vision Research 19, 807811.CrossRefGoogle ScholarPubMed
Rauschecker, J.P. & Singer, W. (1981). The effects of early visual experience on the cat's visual cortex and their possible explanation by Hebb synapses. Journal of Physiology (London) 310, 215239.CrossRefGoogle ScholarPubMed
Reiter, H.O. & Stryker, M.P. (1988). Neural plasticity without post-synaptic action potentials: less-active inputs become dominant when kitten visual cortical cells are pharmacologically inhibited. Proceedings of the National Academy of Sciences of the U.S.A. 85, 36233627.CrossRefGoogle Scholar
Sanides, F. & Hoffmann, J. (1969). Cyto- and myeloarchitecture of the visual cortex of the cat and of the surrounding integration cortices. Journal für Hirnforschung 11, 79104.Google Scholar
Schecter, P. & Murphy, E.H. (1976). Brief monocular visual experience and kitten cortical binocularity. Brain Research 109, 165168.CrossRefGoogle Scholar
Sharp, F.R., Kilduff, T.S., Bzorgchami, S., Heller, H.C. & Ryan, A.F. (1983). The relationship of local cerebral glucose utilization to optical density ratios. Brain Research 263, 97103.CrossRefGoogle ScholarPubMed
Shatz, C.J. & Stryker, M.P. (1978). Ocular dominance in layer IV of the cat's visual cortex and the effects of monocular deprivation. Journal of Physiology (London) 281, 267283.CrossRefGoogle ScholarPubMed
Shatz, C.J., Lindstrom, S. & Wiesel, T.N. (1977). The distribution of afferents representing the right and left eyes in the cat's visual cortex. Brain Research 131, 103116.CrossRefGoogle ScholarPubMed
Sherman, S.M., Hoffmann, K.-P. & Stone, J. (1972). Loss of a specific cell type from dorsal lateral geniculate nucleus in visually deprived cats. Journal of Neurophysiology 35, 532541.CrossRefGoogle ScholarPubMed
Sherman, S.M. & Spear, P.D. (1982). Organization of visual pathways in normal and visually deprived cats. Physiological Reviews 62, 738855.CrossRefGoogle ScholarPubMed
Sherman, S.M., Wilson, J.R. & Guillery, R.W. (1975). Evidence that binocular competition affects the postnatal development of Y cells in the cat's lateral geniculate nucleus. Brain Research 100, 441444.CrossRefGoogle ScholarPubMed
Stent, G.S. (1973). A physiological mechanism for Hebb's postulate of learning. Proceedings of the National Academy of Sciences of the U.S.A. 70, 9971001.CrossRefGoogle ScholarPubMed
Stone, J. & Dreher, B. (1973). Projection of X and Y cells of the cat's lateral geniculate nucleus to areas 17 and 18 of visual cortex. Journal of Neurophysiology 36, 551567.CrossRefGoogle ScholarPubMed
Sur, M., Humphrey, A.L. & Sherman, S.M. (1982). Monocular deprivation affects X- and Y-cell retinogeniculate terminations in cats. Nature 300, 183185.CrossRefGoogle ScholarPubMed
Swindale, N.V. (1980). A model for the formation of ocular dominance stripes. Proceedings of the Royal Society B (London) 208, 243264.Google Scholar
Tieman, D.G. (1989). Video enhancement techniques. In Computer Techniques in Neuroanatomy, ed. Capowski, J.J., New York: Plenum Publishing (in press).Google Scholar
Tieman, D.G., McCall, M. & Hirsch, H.V.B. (1983). The physiological effects of unequal alternating monocular exposure. Journal of Neurophysiology 49, 804818.CrossRefGoogle ScholarPubMed
Tieman, S.B. (1984). Effects of monocular deprivation on geniculocor-tical synapses in the cat. Journal of Comparative Neurology 222, 166176.CrossRefGoogle ScholarPubMed
Tieman, S.B. (1985). The anatomy of geniculocortical connections in monocularly deprived cats. Cellular and Molecular Neurobiology 5, 3545.CrossRefGoogle ScholarPubMed
Tieman, S.B. & Hirsch, H.V.B. (1983). Removal of the more experienced eye decreases visual-field deficits in cats reared with unequal alternating monocular exposure. Brain Research 271, 170173.CrossRefGoogle ScholarPubMed
Tieman, S.B. & Tumosa, N. (1983). [14C]-2-deoxyglucose demonstration of the organization of ocular dominance in areas 17 and 18 of the normal cat. Brain Research 267, 3546.CrossRefGoogle Scholar
Tumosa, N. & Tieman, S.B. (1981). Binocular competition determines the size and shape of ocular dominance columns in cats. Society for Neuroscience Abstracts 7, 674.Google Scholar
Tumosa, N. & Tieman, S.B. (1982). Binocular competition determines the size of ocular dominance columns in area 18 of cat. Investigative Ophthalmology and Visual Science (Suppl.) 22, 243.Google Scholar
Tumosa, N., Tieman, S.B. & Hirsch, H.V.B. (1980 a). Unequal alternating monocular deprivation causes asymmetric visual fields in cats. Science 208, 421423.CrossRefGoogle ScholarPubMed
Tumosa, N., Tieman, S.B. & Hirsch, H.V.B. (1980 b). Anatomical effect of unequal alternating monocular deprivation. Investigative Ophthalmology and Visual Science (Suppl.) 21, 59.Google Scholar
Tumosa, N., Tieman, S.B. & Hirsch, H.V.B. (1982). Visual field deficits in cats reared with unequal alternating monocular exposure. Experimental Brain Research 47, 119129.CrossRefGoogle ScholarPubMed
Tusa, R.J., Palmer, L.A. & Rosenquist, A.C. (1978). The retinotopic organization of area 17 (striate cortex) in the cat. Journal of Comparative Neurology 177, 213236.CrossRefGoogle ScholarPubMed
Tusa, R.J., Rosenquist, A.C. & Palmer, L.A. (1979). Retinotopic organization of areas 18 and 19 in the cat. Journal of Comparative Neurology 185, 657678.CrossRefGoogle Scholar
Wiesel, T.N. & Hubel, D.H. (1963). Single-cell responses in striate cortex of kittens deprived of vision in one eye. Journal of Neurophysiology 26, 10031017.CrossRefGoogle ScholarPubMed
Wiesel, T.N. & Hubel, D.H. (1965). Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. Journal of Neurophysiology 28, 10291040.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, 1128.CrossRefGoogle ScholarPubMed