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Unilateral paralytic strabismus in the adult cat induces plastic changes in interocular disparity along the visual midline: Contribution of the corpus callosum

Published online by Cambridge University Press:  02 August 2005

C. MILLERET
Affiliation:
Laboratoire de Physiologie de la Perception et de l'Action, UMR CNRS—Collège de France, Paris, France
P. BUSER
Affiliation:
FRE 2371 CNRS & Université Pierre et Marie Curie, Paris, France
L. WATROBA
Affiliation:
Laboratoire de Physiologie de la Perception et de l'Action, UMR CNRS—Collège de France, Paris, France

Abstract

Neurones activated through the corpus callosum (CC) in the cat visual cortex are known to be almost entirely located at the 17/18 border. They are orientation selective and display receptive fields (RFs) distributed along the central vertical meridian of the visual field (“visual midline”). Most of these cells are binocular, and many of them are activated both from the contralateral eye through the CC, and from the ipsilateral eye via the direct retino-geniculo-cortical (GC) pathway. These two pathways do not carry exactly the same information, leading to interocular disparity between pairs of RFs along the visual midline. Recently, we have demonstrated that a few weeks of unilateral paralytic strabismus surgically induced at adulthood does not alter the cortical distribution of these units but leads to a loss of their orientation selectivity and an increase of their RF size, mainly toward the ipsilateral hemifield when transcallosally activated (Watroba et al., 2001). To investigate interocular disparity, here we compared these RF changes to those occurring in the same neurones when activated through the ipsilateral direct GC route. The 17/18 transition zone and the bordering medial region within A17 were distinguished, as they display different interhemispheric connectivity. In these strabismics, some changes were noticed, but were basically identical in both recording zones. Ocular dominance was not altered, nor was the spatial distribution of the RFs with respect to the visual midline, nor the amplitude of position disparity between pairs of RFs. On the other hand, strabismus induced a loss of orientation selectivity regardless of whether neurones were activated directly or through the CC. Both types of RFs also widened, but in opposite directions with respect to the visual midline. This led to changes in incidences of the different types of position disparity. The overlap between pairs of RFs also increased. Based on these differences, we suggest that the contribution of the CC to binocular vision along the midline in the adult might be modulated through several intrinsic cortical mechanisms.

Type
Research Article
Copyright
2005 Cambridge University Press

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References

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.Google Scholar
Berlucchi, G. & Rizzolatti, G. (1968). Binocular driven neurons in the visual cortex of split-chiasm cats. Science 159, 308310.Google Scholar
Berman, N. & Payne, B.R. (1983). Alterations in connections of the corpus callosum following convergent and divergent strabismus. Brain Research 274, 201212.Google Scholar
Berman, N. & Grant, S. (1992). Topographic organization, number, and laminar distribution of callosal cells connecting visual cortical areas 17 and 18 of normally pigmented and Siamese cats. Visual Neuroscience 9, 119.Google Scholar
Berman, N., Murphy, E.H., & Salinger, W. (1979). Monocular paralysis in the cat does not change cortical ocular dominance. Brain Research 164, 290293.Google Scholar
Bishop, P.O. & Henry, G.H. (1971). Spatial vision. Annual Review of Psychology 22, 119160.Google Scholar
Blakemore, C. (1969). Binocular depth discrimination and the nasotemporal division. Journal of Physiology (London) 205, 471497.Google Scholar
Blakemore, C. (1970). Binocular depth perception and the optic chiasm. Vision Research 10, 4347.Google Scholar
Boothe, R.G., Dobson, V., & Teller, D. (1985). Postnatal development of vision in humans and nonhuman primates. Annual Review of Neuroscience 8, 495545.Google Scholar
Bourdet, C., Olavarria, J.F., & Van Sluyters, R.C. (1996). Distribution of visual callosal neurons in normal and strabismic cats. Journal of Comparative Neurology 366, 259269.Google Scholar
Bringuier, V., Chavane, F., Glaeser, L., & Frégnac, Y. (1999). Horizontal propagation of visual activity in the synaptic integration field of area 17 neurons. Science 283, 695699.Google Scholar
Choudhury, B.P., Whitteridge, D., & Wilson, M.E. (1965). The function of the callosal connections of the visual cortex. Quarterly Journal of Experimental Physiology 50, 214219.Google Scholar
Crook, J.M. & Eysel, U.T. (1992). GABA-induced inactivation of functionally characterized sites in cat visual cortex (Area 18): Effects on orientation tuning. Journal of Neuroscience 12, 18161825.Google Scholar
Cynader, M., Gardner, J., Dobbins, A., Leporé, F., & Guillemot, J.P. (1986). Interhemispheric communication and binocular vision: Functional and developmental aspects. In Two Hemispheres—One Brain: Functions of the Corpus Callosum, ed. Leporé, F., Ptito, M. & Jasper, H.H., pp. 189209. New York: A.R. Liss.
Das, A. & Gilbert, C.D. (1995). Long-range horizontal connections and their role in cortical reorganization revealed by optical recording of cat primary visual cortex. Nature 375, 780784.Google Scholar
Elberger, A.J., Smith, E.L., & White, J.M. (1983). Spatial dissociation of visual inputs alters the origin of the corpus callosum. Neuroscience Letters 35, 1924.Google Scholar
Ferster, D.A. (1981). A comparison of binocular depth mechanisms in areas 17 and 18 of the cat visual cortex. Journal of Physiology (London) 311, 623655.Google Scholar
Gardner, J.C. & Cynader, M. (1987). Mechanisms for binocular depth sensitivity along the vertical meridian of the visual field. Brain Research 413, 6074.Google Scholar
Gilbert, C.D. (1998). Adult cortical plasticity. Physiological Review 78, 467485.Google Scholar
Gilbert, C.D. & Wiesel, T.N. (1992). Receptive field dynamics in adult primary visual cortex. Nature 356, 150152.Google Scholar
Harvey, A.R. (1980). A physiological analysis of subcortical and commissural projections of areas 17 and 18 in the cat. Journal of Physiology (London) 302, 507534.Google Scholar
Hendry, S.H.C. & Jones, E.G. (1986). Reduction in number of immunostained GABAergic neurones in deprived-eye dominance columns of monkey area 17. Nature 320, 750753.Google Scholar
Hirsch, J.A. & Gilbert, C.D. (1991). Synaptic physiology of horizontal connections in the cat's visual cortex. Journal of Neuroscience 11, 18001809.Google Scholar
Houzel, J.C., Milleret, C., & Innocenti, G.M. (1994). Morphology of callosal axons interconnecting areas 17 and 18 of the cat. European Journal of Neuroscience 6, 898917.Google Scholar
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.Google Scholar
Imbert, M. & Buisseret, P. (1975). Receptive field characteristics and plastic properties of visual cortical cells in kittens reared with and without visual experience. Experimental Brain Research 22, 2536.Google Scholar
Innocenti, G.M. (1980). The primary visual pathway through the corpus callosum: Morphological and functional aspects in the cat. Archives Italiennes de Biologie 118, 124188.Google Scholar
Innocenti, G.M. (1986). General organization of callosal connections in the cerebral cortex. In Cerebral Cortex, ed. Jones, E.G. & Peters, A., pp. 291353. New York: Plenum Publishing Corporation.
Innocenti, G.M. & Frost, D.O. (1979). Effects of visual experience on the maturation of the efferent system to the corpus callosum. Nature 280, 231233.Google Scholar
Jacobs, D.S., Perry, V.H., & Hawken, M.J. (1984). The postnatal reduction of the uncrossed projection from the nasal retina in the cat. Journal of Neuroscience 4, 24252433.Google Scholar
Jeeves, M.A. (1991). Stereo perception in callosal agenesis and partial callosotomy. Neuropsychologia 29, 1934.Google Scholar
Kaas, J.H. (1995). The reorganization of sensory and motor maps in adult mammals. In The Cognitive Neurosciences, ed. Gazzaniga, M.S., pp. 5171. Cambridge, Massachusetts: MIT Press.
Kirk, D.L., Levick, W.R., Cleland, B.G., & Wassle, H. (1976a). Crossed and uncrossed representation of the visual field by brisk-sustained and brisk-transient cat retinal ganglion cells. Vision Research 16, 225231.Google Scholar
Kirk, D.L., Levick, W.R., & Cleland, B.G. (1976b). The crossed or uncrossed destination of axons of sluggish-concentric and non-concentric cat retinal ganglion cells, with an overall synthesis of the visual field representation. Vision Research 16, 233236.Google Scholar
Kisvarday, Z.F., Bonhoeffer, T., Kim, D.S., & Eysel, U.T. (1996). Functional topography of horizontal neuronal networks in cat visual cortex (A18). In Brain Theory—Biological Basis and Computational Principles, ed. Aertsen, A. & Braitenberg, V., pp. 97122. Amsterdam: Elsevier Science B.V.
Lassonde, M., Perenin, M.T., Tassinari, G., Corbetta, M., & Cavanagh, P. (1988). Central mechanisms of stereopsis in man. Advances in Bioscience 70, 9598.Google Scholar
Leporé, F. & Guillemot, J.P. (1982). Visual receptive field properties of cells innervated through the corpus callosum in the cat. Experimental Brain Research 46, 413424.Google Scholar
Leporé, F., Ptito, M., & Guillemot, J.P. (1986a). The role of the corpus callosum in midline fusion. In Two Hemispheres—One Brain: Functions of the Corpus Callosum, ed. Leporé, F., Ptito, M. & Jasper, H.H., pp. 211229. New York: A.R. Liss.
Leporé, F., Ptito, M., & Lassonde, M. (1986b). Stereoperception in cats following section of the corpus callosum and/or the optic chiasm. Experimental Brain Research 61, 258264.Google Scholar
Leporé, F., Samson, A., Paradis, M.C., Ptito, M., & Guillemot, J.P. (1992). Binocular interaction and disparity coding at the 17–18 border: Contribution of the corpus callosum. Experimental Brain Research 90, 129140.Google Scholar
LeVay, S. & Voigt, T. (1988). Ocular dominance and disparity coding in cat visual cortex. Vision Neuroscience 1, 395414.Google Scholar
Löwel, S. & Singer, W. (1992). Selection of intrinsic horizontal connections in the visual cortex by correlated neuronal activity. Science 255, 209212.Google Scholar
Löwel, S. & Singer, W. (1993). Squint affects synchronization of oscillatory responses in cat visual cortex. European Journal of Neuroscience 5, 501508.Google Scholar
Lund, R.D. & Mitchell, D.E. (1979). Asymmetry in the visual callosal connections of strabismic cats. Brain Research 167, 176179.Google Scholar
Lund, R.D., Mitchell, D.E., & Henry, G.H. (1978). Squint-induced modification of callosal connections in cats. Brain Research 144, 169172.Google Scholar
McCourt, M.E., Thalluri, J., & Henry, G.H. (1990). Properties of area 17/18 border neurons contributing to the visual transcallosal pathway in the cat. Visual Neuroscience 5, 8398.Google Scholar
Melvill Jones, G., Guitton, G., & Berthoz, A. (1988). Changing in patterns of eye-head coordination during 6 h of optically reversed vision. Experimental Brain Research 69, 531544.Google Scholar
Milleret, C. & Buser, P. (1984). Receptive field sizes and responsiveness to light in area 18 of adult cat after chiasmotomy. Postoperative evolution; role of visual experience. Experimental Brain Research 57, 7381.Google Scholar
Milleret, C. & Buser, P. (1993). Reorganization processes in the visual cortex also depends on visual experience in the adult cat. Progress in Brain Research 95, 257269.Google Scholar
Milleret, C. & Houzel, J.C. (2001). Visual interhemispheric transfer to areas 17 and 18 in cats with convergent strabismus. European Journal of Neuroscience 13, 137152.Google Scholar
Milleret, C., Houzel, J.C., & Buser, P. (1994). Pattern of development of the callosal transfer of visual information to cortical areas 17 and 18 in the cat. European Journal of Neuroscience 6, 193202.Google Scholar
Mitchell, D.E. & Blakemore, C. (1970). Binocular depth perception and the corpus callosum. Vision Research 10, 4954.Google Scholar
Mitchell, D.E. & Timney, B. (1982). Behavioural measurements of normal and abnormal development of vision in the cat. In Analysis of Visual Behavior, ed. Ingle, J.D., Goodale, M.A. & Mansfield, J.W., pp. 483523. Cambridge, Massachusetts: MIT Press.
Nikara, T., Bishop, P.O., & Pettigrew, J.D. (1968). Analysis of retinal correspondence by studying receptive fields of binocular single units in cat striate cortex. Experimental Brain Research 6, 353372.Google Scholar
Olavarria, J.F. (1996). Non-mirror-symmetric patters of callosal linkages in areas 17 and 18 in cat visual cortex. Journal of Comparative Neurology 366, 643655.Google Scholar
Olavarria, J.F. (2001). Callosal connections correlate preferentially with ipsilateral cortical domains in cat areas 17 and 18, and with contralateral domains in the 17/18 transition zone. Journal of Comparative Neurology 433, 441457.Google Scholar
Orban, G.A., Kennedy, H., & Maes, H. (1981). Responses to movement of neurons in area 17 and 18 of the cat: Velocity sensitivity. Journal of Neurophysiology 45, 10431058.Google Scholar
Payne, B.R. (1990). Representation of the ipsilateral visual field in the transition zone between areas 17 and 18 of the cat's cerebral cortex. Visual Neuroscience 4, 445474.Google Scholar
Payne, B.R. (1991). Visual-field map in the transcallosal sending zone of area 17 in the cat. Visual Neuroscience 7, 201219.Google Scholar
Payne, B.R. & Siwek, D.F. (1991). Visual-field map in the callosal recipient zone at the border between areas 17 and 18 in the cat. Visual Neuroscience 7, 221236.Google Scholar
Payne, B.R., Elberger, A.J., Berman, N., & Murphy, E.H. (1980). Binocularity in the cat visual cortex is reduced by sectioning the corpus callosum. Science 207, 10971099.Google Scholar
Payne, B.R., Berman, N., & Murphy, E.H. (1981). A quantitative assessment of eye alignment in cats after corpus callosum transection. Experimental Brain Research 43, 371376.Google Scholar
Payne, B.R., Pearson, H.E., & Berman, N. (1984). Role of corpus callosum in functional organization of cat striate cortex. Journal of Neurophysiology 52, 570594.Google Scholar
Payne, B.R., Siwek, D.F., & Lomber, S.G. (1991). Complex transcallosal interactions in visual cortex. Visual Neuroscience 6, 283289.Google Scholar
Pettigrew, J.D. (1986). The evolution of binocular vision. In Visual Neuroscience, eds. Pettigrew, J.D., Sanderson, K.J., Levick, W.R., pp. 208222. Cambridge, London, and New Rochelle, New York: Cambridge University Press.
Poggio, G.F. & Fisher, B. (1977). Binocular interaction and depth sensitivity of striate and pre-striate cortical neurons of the behaving rhesus monkey. Journal of Neurophysiology 40, 13931407.Google Scholar
Saint-Amour, D., Leporé, F., Lassonde, M., & Guillemot, J.P. (2004). Effective binocular integration at the midline requires the corpus callosum. Neuropsychology 42, 164174.Google Scholar
Schmued, L.C. (1990). A rapid, sensitive histochemical stain for myelin in frozen brain sections. Journal of Histochemistry and Cytochemistry 38, 717720.Google Scholar
Shatz, C.J. (1977). Anatomy of interhemispheric connections in the visual system of Boston Siamese and ordinary cats. Journal of Comparative Neurology 173, 497518.Google Scholar
Shatz, C.J., Lindstrom, S., & Wiesel, T.N. (1977). The distribution of afferents representing the right and the left eyes in the cat's visual cortex. Brain Research 131, 103116.Google Scholar
Sherman, S.M. (1972). Development of interocular alignment in cats. Brain Research 37, 187203.Google Scholar
Sugita, Y. (1996). Global plasticity in adult visual cortex following reversal of visual input. Nature 380, 523526.Google Scholar
Terao, N., Inatomi, A., & Maeda, T. (1982). Anatomical evidence for the overlapped distribution of ipsilaterally and contralaterally projecting ganglion cells to the lateral geniculate nucleus in the cat retina: A morphologic study with fluorescent tracers. Investigative Ophthalmology and Vision Science 23, 796798.Google Scholar
Timney, B., Elberger, A., & Vanderwater, M.L. (1985). Binocular depth perception in the cat following early corpus callosum section. Experimental Brain Research 60, 1926.Google Scholar
Tusa, R.J., Palmer, L.A., & Rosenquist, A.C. (1981). Multiple cortical visual areas: Visual field topography in the cat. In Cortical Sensory Organization. 2. Multiple Visual Areas, ed. Woolsey, C.N., pp. 131. Clifton, New Jersey: Humana Press.
Vakkur, G.J., Bishop, P.O., & Kozak, W. (1963). Visual optics in the cat including posterior nodal distance and retinal landmarks. Vision Research 3, 289314.Google Scholar
Watroba, L., Buser, P., & Milleret, C. (2001). Impairment of binocular vision in the adult cat induces plastic changes in the callosal cortical map. European Journal of Neuroscience 14, 10211029.Google Scholar
Westheimer, G. & Mitchell, D.E. (1969). The sensory stimulus for disjunctive eye movements. Vision Research 9, 749755.Google Scholar
Wong-Riley, M. (1979). Changes in the visual system of monocularly sutured or enucleated cats demonstrated with cytochrome oxidase histochemistry. Brain Research 171, 1128.Google Scholar
Yinon, U. (1976). Age dependence of the effect of squint on cells in kittens visual cortex. Experimental Brain Research 26, 151157.Google Scholar
Yinon, U. (1978). Chronic asymmetry in the extraocular muscles of adult cats: Stability in binocularity of cortical neurons. Experimental Brain Research 32, 275285.Google Scholar