Hostname: page-component-7c8c6479df-r7xzm Total loading time: 0 Render date: 2024-03-17T11:59:03.977Z Has data issue: false hasContentIssue false

Ocular dominance columns in strabismus

Published online by Cambridge University Press:  04 October 2006

DANIEL L. ADAMS
Affiliation:
Beckman Vision Center, University of California San Francisco, San Francisco, California
JONATHAN C. HORTON
Affiliation:
Beckman Vision Center, University of California San Francisco, San Francisco, California

Abstract

During development, the projection from the lateral geniculate nucleus to striate cortex becomes segregated into monocular regions called ocular dominance columns. Prior studies in cats have suggested that experimental strabismus or alternating monocular occlusion increases the width and segregation of columns. In the squirrel monkey, strabismus has been reported to induce the formation of ocular dominance columns. However, these studies are difficult to interpret because no animal can serve as its own control and the degree of inter-individual variability among normal subjects is considerable. We have re-examined the effect of strabismus on ocular dominance columns in a large group of strabismic and normal squirrel monkeys. Five animals rendered strabismic at age one week had well-developed, widely spaced columns. Among 16 control animals, a wide spectrum of column morphology was encountered. Some control animals lacked ocular dominance columns, whereas others had columns similar to those observed in strabismic animals. Natural variation in column expression in normal squirrel monkeys, and potential uncontrolled genetic influences, made it impossible to determine if strabismus affects ocular dominance columns. It was evident however, that strabismus does not affect the binocular projection from the lateral geniculate nucleus to each CO patch in the upper layers. In strabismic monkeys, just as in normal animals, each patch received input from geniculate afferents serving both the left eye and the right eye. In addition, in strabismic monkeys, as in normal animals, patches were not aligned with ocular dominance columns.

Type
Research Article
Copyright
2006 Cambridge University Press

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

REFERENCES

Adams, D.L. & Horton, J.C. (2002). Shadows cast by retinal blood vessels mapped in primary visual cortex. Science 298, 572576.Google Scholar
Adams, D.L. & Horton, J.C. (2003a). Capricious expression of cortical columns in the primate brain. Nature Neuroscience 6, 113114.Google Scholar
Adams, D.L. & Horton, J.C. (2003b). The representation of retinal blood vessels in primate striate cortex. Journal of Neuroscience 23, 59845997.Google Scholar
Adams, D.L. & Horton, J.C. (2006). Monocular cells without ocular dominance columns. Journal of Neurophysiology: In Press.Google Scholar
Campos-Ortega, J.A. & Glees, P. (1967). The subcortical distribution of optic fibers in Saimiri sciureus (squirrel monkey). Journal Comparative Neurology 131, 131142.Google Scholar
Chino, Y.M., Smith, E.L., 3rd., Yoshida, K., Cheng, H., & Hamamoto, J. (1994). Binocular interactions in striate cortical neurons of cats reared with discordant visual inputs. Journal of Neuroscience 14, 50505067.Google Scholar
Crawford, M.L. (1998). Column spacing in normal and visually deprived monkeys. Experimental Brain Research 123, 282288.Google Scholar
Crawford, M.L. & Harwerth, R.S. (2004). Ocular dominance column width and contrast sensitivity in monkeys reared with strabismus or anisometropia. Investigative Ophthalmology & Visual Science 45, 30363042.Google Scholar
Doty, R.W., Glickstein, M., & Calvin, W.H. (1966). Lamination of the lateral geniculate nucleus in the squirrel monkey, Saimiri sciureus. Journal of Comparative Neurology 127, 335340.Google Scholar
Fenstemaker, S.B., Kiorpes, L., & Movshon, J.A. (2001). Effects of experimental strabismus on the architecture of macaque monkey striate cortex. Journal of Comparative Neurology 438, 300317.Google Scholar
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, 673702.Google Scholar
Goodhill, G.J. (1993). Topography and ocular dominance: a model exploring positive correlations. Biological Cybernetics 69, 109118.Google Scholar
Goodhill, G.J. & Willshaw, D.J. (1990). Application of the elastic net algorithm to the formation of ocular dominance stripes. Network 1, 4159.Google Scholar
Goodhill, G.J. & Löwel, S. (1995). Theory meets experiment: correlated neural activity helps determine ocular dominance column periodicity. Trends in Neuroscience 18, 437439.Google Scholar
Harris, A.E., Ermentrout, G.B., & Small, S.L. (1997). A model of ocular dominance column development by competition for trophic factor. Proceedings of the National Academy of Science USA 94, 99449949.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, 340344.Google Scholar
Hendrickson, A.E., Wilson, J.R., & Ogren, M.P. (1978). The neuroanatomical organization of pathways between the dorsal lateral geniculate nucleus and visual cortex in Old World and New World primates. Journal of Comparative Neurology 182, 123136.Google Scholar
Hershkovitz, P. (1984). Taxonomy of squirrel monkeys genus Saimiri (Cebidae, Platyrrhini): A preliminary report with description of a hitherto unnamed form. American Journal of Primatology 7, 155210.Google Scholar
Horton, J.C. (1984). Cytochrome oxidase patches: A new cytoarchitectonic feature of monkey visual cortex. Philosophical Transactions of the Royal Society of London Series B Biological Sciences 304, 199253.Google Scholar
Horton, J.C. & Hubel, D.H. (1981). Regular patchy distribution of cytochrome oxidase staining in primary visual cortex of macaque monkey. Nature 292, 762764.Google Scholar
Horton, J.C. & Hocking, D.R. (1996a). Intrinsic variability of ocular dominance column periodicity in normal macaque monkeys. Journal of Neuroscience 16, 72287239.Google Scholar
Horton, J.C. & Hocking, D.R. (1996b). An adult-like pattern of ocular dominance columns in striate cortex of newborn monkeys prior to visual experience. Journal of Neuroscience 16, 17911807.Google Scholar
Horton, J.C. & Hocking, D.R. (1996c). Anatomical demonstration of ocular dominance columns in striate cortex of the squirrel monkey. Journal of Neuroscience 16, 55105522.Google Scholar
Hubel, D.H. & Wiesel, T.N. (1965). Binocular interaction in striate cortex of kittens reared with artificial squint. Journal of Neurophysiology 28, 10411059.Google Scholar
Hubel, D.H., Wiesel, T.N., & LeVay, S. (1976). Functional architecture of area 17 in normal and monocularly deprived macaque monkeys. Cold Spring Harbor Symposia on Quantitative Biology 40, 581589.Google Scholar
Itaya, S.K., Itaya, P.W., & Van Hoesen, G.W. (1984). Intracortical termination of the retino-geniculo-striate pathway studied with transsynaptic tracer (wheat germ agglutinin-horseradish peroxidase) and cytochrome oxidase staining in the macaque monkey. Brain Research 304, 303310.Google Scholar
Jacobs, G.H. (1969). Transneuronal changes in the lateral geniculate nucleus of the squirrel monkey, Saimiri sciureus. Journal of Comparative Neurology 135, 8184.Google Scholar
Jones, D.G., Van Sluyters, R.C., & Murphy, K.M. (1991). A computational model for the overall pattern of ocular dominance. Journal of Neuroscience 11, 37943808.Google Scholar
Kaschube, M., Wolf, F., Geisel, T., & Löwel, S. (2002). Genetic influence on quantitative features of neocortical architecture. Journal of Neuroscience 22, 72067217.Google Scholar
Kaschube, M., Wolf, F., Puhlmann, M., Rathjen, S., Schmidt, K.F., Geisel, T., & Löwel, S. (2003). The pattern of ocular dominance columns in cat primary visual cortex: intra- and interindividual variability of column spacing and its dependence on genetic background. European Journal of Neuroscience 18, 32513266.Google Scholar
Livingstone, M.S. (1996). Ocular dominance columns in New World monkeys. Journal of Neuroscience 16, 20862096.Google Scholar
Livingstone, M.S. & Hubel, D.H. (1982). Thalamic inputs to cytochrome oxidase-rich regions in monkey visual cortex. Proceedings of the National Academy of Science of the USA 79, 60986101.Google Scholar
Livingstone, M.S., Nori, S., Freeman, D.C., & Hubel, D.H. (1995). Stereopsis and binocularity in the squirrel monkey. Vision Research 35, 345354.Google Scholar
Löwel, S. (1994). Ocular dominance column development: Strabismus changes the spacing of adjacent columns in cat visual cortex. Journal of Neuroscience 14, 74517468.Google Scholar
Mason, W.A. & Mendoza, S.P. (1998). Generic aspects of primate attachments: Parents, offspring and mates. Psychoneuroendocrinology 23, 765778.Google Scholar
Miller, K.D., Keller, J.B., & Stryker, M.P. (1989). Ocular dominance column development: analysis and simulation. Science 245, 605615.Google Scholar
Murphy, K.M., Jones, D.G., Fenstemaker, S.B., Pegado, V.D., Kiorpes, L., & Movshon, J.A. (1998). Spacing of cytochrome oxidase blobs in visual cortex of normal and strabismic monkeys. Cerebral Cortex 8, 237244.Google Scholar
Quick, M.W. & Boothe, R.G. (1989). Measurement of binocular alignment in normal monkeys and in monkeys with strabismus. Investigative Ophthalmology & Visual Science 30, 11591168.Google Scholar
Rathjen, S., Schmidt, K.E., & Löwel, S. (2002). Two-dimensional analysis of the spacing of ocular dominance columns in normally raised and strabismic kittens. Experimental Brain Research 145, 158165.Google Scholar
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, 371378.Google Scholar
Sengpiel, F., Blakemore, C., Kind, P.C., & Harrad, R. (1994). Interocular suppression in the visual cortex of strabismic cats. Journal of Neuroscience 14, 68556871.Google Scholar
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, 103116.Google Scholar
Smith, E.L., 3rd., Chino, Y.M., Ni, J., Cheng, H., Crawford, M.L., & Harwerth, R.S. (1997). Residual binocular interactions in the striate cortex of monkeys reared with abnormal binocular vision. Journal of Neurophysiology 78, 13531362.Google Scholar
Stryker, M.P. & Harris, W.A. (1986). Binocular impulse blockade prevents the formation of ocular dominance columns in cat visual cortex. Journal of Neuroscience 6, 21172133.Google Scholar
Swindale, N.V. (1980). A model for the formation of ocular dominance stripes. Proceedings of the Royal Society of London Series B Biological Sciences 208, 243264.Google Scholar
Tieman, S.B. & Tumosa, N. (1997). Alternating monocular exposure increases the spacing of ocularity domains in area 17 of cats. Visual Neuroscience 14, 929938.Google Scholar
Tigges, J., Tigges, M., & Perachio, A.A. (1977). Complementary laminar terminations of afferents to area 17 originating in area 18 and in the lateral geniculate nucleus in squirrel monkey. Journal of Comparative Neurology 176, 87100.Google Scholar
Tychsen, L. & Burkhalter, A. (1995). Neuroanatomic abnormalities of primary visual cortex in macaque monkeys with infantile esotropia: Preliminary results. Journal of Pediatric Ophthalmology and Strabismus 32, 323328.Google Scholar
Van Sluyters, R.C. & Levitt, F.B. (1980). Experimental strabismus in the kitten. Journal of Neurophysiology 43, 686699.Google Scholar
von der Malsburg, C. & Willshaw, D.J. (1976). A mechanism for producing continuous neural mappings: ocularity dominance stripes and ordered retino-tectal projections. Experimental Brain Research Supp. 1, 463469.Google Scholar
Von Noorden, G.K. & Dowling, J.E. (1970). Experimental amblyopia in monkeys. II. Behavioral studies in strabismic amblyopia. Archives of Ophthalmology 84, 215220.Google Scholar
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, 135145.Google Scholar