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Binocular depth perception following early experience with interocular torsional disparity

Published online by Cambridge University Press:  02 June 2009

Paul G. Shinkman
Affiliation:
Department of Psychology and Brain and Development Research Center, University of North Carolina, Chapel Hill
Brian Timney
Affiliation:
Department of Psychology, University of Western Ontario, London, Canada
Michael R. Isley
Affiliation:
Department of Psychology and Brain and Development Research Center, University of North Carolina, Chapel Hill

Abstract

The relationship between the behavioral and physiological consequences of rearing with optically induced cyclotropia was assessed. Beginning at the age of 4 weeks, kittens wore goggles that rotated the visual field in opposite directions in each eye for several hours each day over a period of several weeks. The amounts of interocular rotation were 0 deg (control), 16 deg, and 32 deg. Subsequently, they were tested to determine their monocular and binocular depth thresholds and, in some cases, visual acuity. In several kittens recordings were also made from the visual cortex. Binocular performance of all kittens in the 0-deg condition and three out of six kittens in the 16-deg condition was comparable to, although slightly lower than, that of normally reared kittens. In contrast, none of the 32-deg kittens showed any evidence of the binocular superiority that would suggest the presence of stereopsis. Extracellular unit recordings from the visual cortex confirmed our earlier results with goggle-reared kittens. In 16-deg kittens, the distribution of the cells' preferred interocular disparities (IOD) in receptive-field orientation showed a compensating shift so that the mean matched the experienced rotational disparity. In the 32-deg kittens, binocularity was greatly disrupted and there was no compensatory shift in the IOD distribution. Two 32-deg kittens were afforded 3 years of subsequent normal visual experience. Both the behavioral and the physiological findings were unaffected by normal visual exposure in adulthood. Control measurements of acuity indicated that any deficits in depth perception were not due to reduced spatial-resolution abilities. The data indicate that the kitten visual system is able to maintain functional binocularity sufficient to subserve a moderate level of stereoacuity with interocular rotations of up to at least 16 deg.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1992

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References

Altmann, L., Luhmann, H.J., Greuel, J.M. & Singer, W. (1987). Functional and neuronal binocularity in kittens raised with rapidly alternating monocular occlusion. Journal of Neurophysiology 58, 965980.Google ScholarPubMed
Blake, R. & Hirsch, H.V.B. (1975). Deficits in binocular depth perception in cats after alternating monocular deprivation. Science 190, 11141116.Google ScholarPubMed
Blakemore, C., Van Sluyters, R.C., Peck, C.K. & Hein, A. (1975). Development of cat visual cortex following rotation of one eye. Nature 257, 584586.CrossRefGoogle ScholarPubMed
Bruce, C.J., Isley, M.R. & Shinkman, P.G. (1981). Visual experience and development of interocular orientation disparity in visual cortex. Journal of Neurophysiology 46, 215228.CrossRefGoogle ScholarPubMed
Crewther, S.G., Crewther, D.P., Peck, C.K. & Pettigrew, J.D. (1980). Visual cortical effects of rearing cats with monocular or binocular cyclotorsion. Journal of Neurophysiology 44, 97118.CrossRefGoogle ScholarPubMed
Cynader, M. (1979). Interocular alignment following visual deprivation in the cat. Investigative Ophthalmology and Visual Science 18, 726741.Google ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1962). Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. Journal of Physiology 160, 106154.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1965). 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 206, 419436.CrossRefGoogle Scholar
Isley, M.R., Plummer, K.R. & Shinkman, P.G. (1979). Cortical binocular receptive fields after visual field rotation in developing kittens: Effects of subsequent normal visual exposure during adulthood. Society for Neuroscience Abstracts 5, 790.Google Scholar
Isley, M.R., Rogers-Ramachandran, D.C. & Shinkman, P.G. (1990). Interocular torsional disparity and visual cortical development in the cat. Journal of Neurophysiology 64, 13521360.CrossRefGoogle ScholarPubMed
Kaye, M., Mitchell, D.E. & Cynader, M. (1982). Depth perception, eye alignment and cortical ocular dominance of dark-reared cats. Developmental Brain Research 2, 3754.CrossRefGoogle Scholar
Mitchell, D.E., Kaye, M. & Timney, B. (1979). Assessment of depth perception in cats. Perception 8, 389396.CrossRefGoogle ScholarPubMed
Olson, C. & Freeman, R.D. (1978). Eye alignment in kittens. Journal of Neurophysiology 41, 848859.CrossRefGoogle ScholarPubMed
Packwood, J. & Gordon, B. (1975). Stereopsis in normal domestic cat, Siamese cat, and cat raised with alternating monocular occlusion. Journal of Neurophysiology 38, 14851499.Google Scholar
Pettigrew, J.D. (1983). Teleology of the critical period for binocular vision. Presented at the satellite symposium on Development of Visual Pathways in Mammals, International Union of Physiological Sciences, Newport, Australia.Google Scholar
Podell, M., Isley, M.R., Shinkman, P.G. & Rogers, D.C. (1982). Visual development: Early experience with torsionally disparate images. Metabolic, Pediatric and Systemic Ophthalmology 6, 273283.Google ScholarPubMed
Shinkman, P.G. (1983). Effects of interocular torsional image disparity on visual cortical development. Invited presentation, Australasian Winter Conference on Brain Research, Queenstown, New Zealand.Google Scholar
Shinkman, P.G. & Bruce, C.J. (1977). Binocular differences in cortical receptive fields of kittens after rotationally disparate binocular experience. Science 197, 285287.Google ScholarPubMed
Shinkman, P.G., Isley, M.R. & Rogers, D.C. (1980). Cortical binocular receptive fields in developing kittens: Effects of early visual field rotation followed by normal visual exposure during adulthood. Proceedings of the International Union of Physiological Sciences 14, 700.Google Scholar
Shinkman, P.G., Isley, M.R. & Rogers, D.C. (1983a). Prolonged dark rearing and development of interocular orientation disparity in visual cortex. Journal of Neurophysiology 49, 717729.CrossRefGoogle ScholarPubMed
Shinkman, P.G., Isley, M.R. & Rogers, D.C. (1985). Development of interocular relationships in visual cortex. In Advances in Neural and Behavioral Development, Vol. 1, ed. Aslin, R., pp. 187268. New Jersey: Ablex Publishing Corp.Google Scholar
Shinkman, P.G., Timney, B. & Isley, M.R. (1986a). Binocular depth perception and pupillographic changes in kittens reared with interocular torsional disparity. Society for Neuroscience Abstracts 12, 785.Google Scholar
Shinkman, P.G., Timney, B. & Isley, M.R. (19866). Perceptual, pupillographic, and physiological effects in cats reared with interocular torsional disparity. Presented at First International Congress of Neuroethology, Tokyo, Japan.Google Scholar
Shinkman, P.G., Timney, B., Isley, M.R. & Rogers, D.C. (19836). Physiological and behavioral consequences of optically-induced interocular torsional disparity in early visual input. Proceedings of the International Union of Physiological Sciences 15, 445.Google Scholar
Timney, B. (1985). Visual experience and the development of depth perception. In Brain Mechanisms and Spatial Vision, ed. Ingle, D.J., Jeannerod, M. & Lee, D., pp. 147174. The Netherlands: M. Nijhoff.CrossRefGoogle Scholar
Timney, B. (1988). The development of depth perception. In Advances in Neural and Behavioral Development, Vol. 3, ed. Shinkman, P.G., pp. 153208. Norwood, New Jersey: Ablex Publishing Corp.Google Scholar
Timney, B. (1990). Effects of brief monocular deprivation on binocular depth perception in the cat: A sensitive period for the loss of stereopsis. Visual Neuroscience 5, 273280.CrossRefGoogle Scholar
Von Grunau, M.W. (1979). The role of maturation and visual experience in the development of eye alignment in cats. Experimental Brain Research 37, 4147.CrossRefGoogle ScholarPubMed
Washington, I.M., Isley, M.R. & Shinkman, P.G. (1977). Effects of large interocular rotational disparities on the development of binocularity in kitten visual cortical neurons. Society for Neuroscience Abstracts 3, 580.Google Scholar
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