Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-06T09:46:51.680Z Has data issue: false hasContentIssue false
  • English
  • Français

Alternating monocular exposure increases the spacing of ocularity domains in area 17 of cats

Published online by Cambridge University Press:  02 June 2009

Suzannah Bliss Tieman  and
Nina Tumosa
Suzannah Bliss Tieman
Affiliation:
Neurobiology Research Center and Department of Biological Sciences, State University of New York, Albany
Nina Tumosa
Affiliation:
School of Optometry, University of Missouri-St. Louis, St. Louis
Get access Rights & Permissions [Opens in a new window]

Abstract

Goodhill (1993) has recently suggested that the spacing of ocularity domains in visual cortex is not solely an intrinsic property of cortex, but is determined, at least in part, by the degree of correlation in the activity of the two eyes. In support of this model, Löwel (1994) has shown that strabismus, which decorrelates the activity of the two eyes, increases the spacing of ocular dominance columns in area 17, but not area 18, of the cat. As a further test of Goodhill's model, in this paper we examine the effects of another rearing procedure that decorrelates the activity of the two eyes, namely alternating monocular exposure (AME). Cats were reared either normally (9 cats) or with AME (21 cats). We labeled their ocularity domains by one of three methods: ocular dominance columns by 2-deoxyglucose (14 cats), and ocular dominance patches by transneuronal transport (14 cats), or by injections of tracer into single layers of the lateral geniculate nucleus (LGN; 2 cats). The spacing of ocular dominance was 11% greater in the AME cats than in the normal cats (0.976 vs. 0.877 mm). These results are similar to those previously reported for strabismic cats, although the effect is less striking. We thus confirm that decorrelating the activity of the two eyes increases the spacing of cortical ocularity domains. Our results further suggest that the degree of decorrelation affects the extent of that increase.

Keywords

DevelopmentVisual cortexActivity-dependent regulationOcular dominance
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 5 , September 1997 , pp. 929 - 938
Copyright
Copyright © Cambridge University Press 1997

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.CrossRefGoogle ScholarPubMed
Arnett, D.W. (1978). Statistical dependence between neighboring retinal ganglion cells in goldfish. Experimental Brain Research 32, 49–53.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, 32–48.CrossRefGoogle ScholarPubMed
Blake, R., Crawford, M.L.J. & Hirsch, H.V.B. (1974). Consequences of alternating monocular deprivation on eye alignment and convergence in cats. Investigative Ophthalmology 13, 121–126.Google ScholarPubMed
Constantine-Paton, M. (1983). Position and proximity in the development of maps and stripes. Trends in Neurosciences 6, 33–36.CrossRefGoogle Scholar
Cowan, W.M., Fawcett, J.W., O'Leary, D.D.M. & Stanfield, B.B. (1984). Regressive events in neurogenesis. Science 225, 1258–1265.CrossRefGoogle ScholarPubMed
Cynader, M.S., Swindale, N.V. & Matsubara, J.A. (1987). Functional topography in cat area 18. Journal of Neuroscience 7, 1401–1413.CrossRefGoogle ScholarPubMed
Des Rosiers, M.H., Sakurada, O., Jehle, J.W., 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 ScholarPubMed
Diao, Y., Jia, W., Swindale, N.V. & Cynader, M.S. (1990). Functional organization of the cortical 17/18 border region in the cat. Experimental Brain Research 79, 271–282.CrossRefGoogle ScholarPubMed
Goodhill, G.J. (1993). Topography and ocular dominance: A model exploring positive correlations. Biological Cybernetics 69, 109–118.CrossRefGoogle Scholar
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. Rauschecker, J.P. & Marler, P., pp. 286–320. New York: Wiley.Google Scholar
Horton, J.C. & Hocking, D.R. (1996). An adult-like pattern of ocular dominance columns in striate cortex of newborn monkeys prior to visual experience. Journal of Neuroscience 16, 1791–1807.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 B (London) 278, 377–409.Google 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, 229–289.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, 1041–1059.CrossRefGoogle ScholarPubMed
Jones, D.G., Murphy, K.M. & Van Sluyters, R.C. (1996). Spacing of ocular dominance columns is not changed by monocular deprivation or strabismus. Investigative Ophthalmology and Visual Science 37, S425.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.CrossRefGoogle ScholarPubMed
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, 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 190, 1–51.Google Scholar
Löwel, S. (1994). Ocular dominance column development: Strabismus changes the spacing of adjacent columns in cat visual cortex. Journal of Neuroscience 14, 7451–7468.CrossRefGoogle ScholarPubMed
Löwel, 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
Mastronarde, D.N. (1989). Correlated firing of retinal ganglion cells. Trends in Neurosciences 12, 75–79.CrossRefGoogle ScholarPubMed
Miller, K.D., Keller, J.B. & Stryker, M.P. (1989). Ocular dominance column development: Analysis and simulation. Science 245, 605–615.CrossRefGoogle ScholarPubMed
Mower, C.D., Caplan, C.J., Christen, W.G. & Duffy, F.H. (1985). Dark rearing prolongs physiological but not anatomical plasticity of the cat visual cortex. Journal of Comparative Neurology 235, 448–466.CrossRefGoogle Scholar
Murphy, K.M., Pegado, V.D., Fenstemaker, S.B., Jones, D.G., Kiorpes, L. & Movshon, J.A. (1996). Periodicity of visual cortical modules in normal and strabismic monkeys. Investigative Ophthalmology and Visual Science 13. S424.Google Scholar
O'Leary, D.D.M., Stanfield, B.B. & Cowan, W.M. (1981). Evidence that the early postnatal restriction of the cells of origin of the callosal projection is due to the elimination of axonal collaterals rather than to the death of neurons. Brain Research 227, 607–617.CrossRefGoogle Scholar
O'Leary, D.D.M. (1992). Development of connectional diversity and specificity in the mammalian brain by the pruning of collateral projections. Current Opinions in Neurobiology 2, 70–77.CrossRefGoogle ScholarPubMed
Otsuka, R. & Hassler, R. (1962). Über Aufbau und Gliederung der corticalen Sehsphäre bei der Katze. Archivfür Psychiatrie und Zeitschrift für die Cesamte Neurologie 203, 212–234.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, 807–811.CrossRefGoogle ScholarPubMed
Rakic, P. (1976). Prenatal genesis of connections subserving ocular dominance in the rhesus monkey. Nature (London) 261, 467–471.CrossRefGoogle ScholarPubMed
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, 79–104.Google Scholar
Schmidt, J.T. (1985). Formation of retinotopic connections: Selective stabilization by an activity-dependent mechanism. Cellular and Molecular Neurobiology 5, 65–83.CrossRefGoogle ScholarPubMed
Schmidt, J.T. & Buzzard, M. (1993). Activity-driven sharpening of the ret-inotectal projection in goldfish: Development under stroboscopic illumination prevents sharpening. Journal of Neurobiology 24, 384–399.CrossRefGoogle ScholarPubMed
Schmidt, J.T. & Edwards, D.L. (1983). Activity sharpens the map during the regeneration of the retinotectal projection in goldfish. Brain Research 269, 29–39.CrossRefGoogle ScholarPubMed
Schmidt, J.T. & Tieman, S.B. (1985). Eye-specific segregation of optic afferents in mammals, fish, and frogs: The role of activity. Cellular and Molecular Neurobiology 5, 5–34.CrossRefGoogle ScholarPubMed
Shatz, C.J., Lindström, S. & Wiesel, T.N. (1977). The distribution of afferents representing the right and left eyes in the cat's visual cortex. Brain Research 131, 103–116.CrossRefGoogle ScholarPubMed
Shatz, C.J. (1990). Competitive interactions between retinal ganglion cells during prenatal development. Journal of Neurobiology 21, 197–211.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, 267–283.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, 997–1001.CrossRefGoogle ScholarPubMed
Stryker, M.P. & Harris, W.A. (1986). Binocular impulse blockade prevents the formation of ocular dominance columns in cat visual cortex. Journal of Neuroscience 60, 2117–2133.CrossRefGoogle Scholar
Swindale, N.V. (1980). A model for the formation of ocular dominance stripes. Proceedings of the Royal Society B (London) 208, 243–264.Google Scholar
Swindale, N.V. (1981). Absence of ocular dominance patches in dark reared cats. Nature (London) 290, 332–333.CrossRefGoogle ScholarPubMed
Swindale, N.V. (1988). Role of visual experience in promoting segregation of eye dominance patches in the visual cortex of the cat. Journal of Comparative Neurology 267, 472–488.CrossRefGoogle ScholarPubMed
Tieman, D.G., McCall, M.A. & Hirsch, H.V.B. (1983). Physiologial effects of unequal alternating monocular exposure. Journal of Neurophysiology 49, 804–818.CrossRefGoogle Scholar
Tieman, S.B. (1984). Effects of monocular deprivation on geniculocortical synapses in the cat. Journal of Comparative Neurology 222, 166–176.CrossRefGoogle ScholarPubMed
Tieman, S.B., Nickla, D.L., Gross, K., Hickey, T.L. & Tumosa, N. (1984). Effects of unequal alternating monocular exposure on the sizes of cells in the cat's lateral geniculate nucleus. Journal of Comparative Neurology 225, 119–128.CrossRefGoogle ScholarPubMed
Tieman, S.B. & Hirsch, H.V.B. (1982). Exposure to lines of only one orientation modifies dendritic morphology of cells in the visual cortex of the cat. Journal of Comparative Neurology 211, 353–362.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, 35–46.CrossRefGoogle Scholar
Tieman, S.B. & Tumosa, N. (1996). Alternating monocular exposure increases the spacing of ocularity domains in area 17 of cats. Investigative Ophthalmology and Visual Science 37, S425.Google Scholar
Tumosa, N., Tieman, S.B. & Hirsch, H.V.B. (1980). Unequal alternating monocular deprivation causes asymmetric visual fields in cats. Science 208, 421–423.CrossRefGoogle ScholarPubMed
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, 119–129.CrossRefGoogle ScholarPubMed
Tumosa, N., Nunberg, S., Hirsch, H.V.B. & Tieman, S.B. (1983). Binocular exposure causes suppression of the less experienced eye in cats previously reared with unequal alternating monocular exposure. Investigative Ophthalmology and Visual Science 24, 496–506.Google ScholarPubMed
Tumosa, N., Tieman, S.B. & Tieman, D.G. (1989). Binocular competition affects the pattern and intensity of ocular activation columns in the visual cortex of cats. Visual Neuroscience 2, 391–407.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, 213–236.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, 657–678.CrossRefGoogle Scholar
von der Malsburg, C. (1979). Development of ocularity domains and growth behavior of axon terminals. Biological Cybernetics 32, 49–62.CrossRefGoogle ScholarPubMed
von der Malsburg, C. & Willshaw, D.J. (1976). A mechanism for producing continuous neural mappings: Ocularity dominance stripes and ordered retinotectal projections. Experimental Brain Research (Suppl) 1, 463–469.Google Scholar
von Grünau, M.W. & Singer, W. (1979). The role of binocular neurons in the cat striate cortex in combining information from the two eyes. Experimental Brain Research 34, 133–142.CrossRefGoogle ScholarPubMed
Wiesel, T.N., Hubel, D.H. & Lam, D.M.K. (1974). Autoradiographic demonstration of ocular dominance in the monkey striate cortex by means of transneuronal transport. Brain Research 79, 273–279.CrossRefGoogle ScholarPubMed
Willshaw, D. & von der Malsburg, C. (1976). How patterned neural connections can be set up by organization. Proceedings of the Royal Society B (London) 194, 431–445.Google ScholarPubMed
Wong, R.O.L., Meister, M. & Shatz, C.J. (1993). Transient period of correlated bursting activity during development of the mammalian retina. Neuron 11, 923–938.CrossRefGoogle ScholarPubMed