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Strabismus does not prevent recovery from monocular deprivation: A challenge for simple Hebbian models of synaptic modification

Published online by Cambridge University Press:  02 June 2009

Rafael Malach  and
Richard C. Van Sluyters
Rafael Malach
Affiliation:
School of Optometry, University of California, Berkeley
Richard C. Van Sluyters
Affiliation:
School of Optometry, University of California, Berkeley
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Abstract

It has been suggested that development of central connections in the mammalian visual system is governed by a simple Hebbian rule of synaptic modifiability. Under such a rule, simultaneity of presynaptic and postsynaptic action potentials is a prerequisite for enhanced synaptic efficacy. The present paper reports the results of a study designed to test whether this hypothesis is applicable to the development of the thalamo-cortical visual pathway.

In four-week-old kittens, exposure to a 2-d period of monocular deprivation was used to render the vast majority of cortical cells capable of being activated only by the nondeprived eye. During a subsequent 3–5 month recovery period, both eyes were open but surgically misaligned. This combination of conditions was chosen so that during the recovery period presynaptic activity originating from the initially deprived eye would be decorrelated from postsynaptic action potentials in cortical neurons. If synaptic modification is regulated by a simple Hebbian mechanism, then in this situation the deprived eye should be unable to recover control of cortical cells.

In fact, the present results indicate that during the recovery period the proportion of cortical neurons dominated by the deprived eye rose to a level equal to that of the nondeprived eye – a result contrary to that predicted by a simple Hebbian rule of development. Histological analysis indicated that a similar level of recovery was present both within and outside of cortical layer IV, the main thalamo-recipient layer. As expected, the induced strabismus resulted in a failure of cortical binocularity to recover in these kittens.

Although these results argue against a simple Hebbian mechanism of development, they are compatible with the hypothesis that synaptic modifiability is dependent upon correlations between presynaptic activity and local, subthreshold, postsynaptic changes. This alternative hypothesis has the advantage of allowing modification of local synaptic circuits within the dendritic arbors of a single neuron.

Keywords

Hebb synapsesOcular dominance columnsVisual cortexMonocular deprivationStrabismus
Type
Research Article
Information
Visual Neuroscience , Volume 3 , Issue 3 , September 1989 , pp. 267 - 273
Copyright
Copyright © Cambridge University Press 1989

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References

Bear, M.F., Cooper, L.N. & Ebner, F.F. (1987). A physiological basis for a theory of synapse modification. Science 237, 42–48.CrossRefGoogle ScholarPubMed
Blakemore, C. (1974). Developmental factors in the formation of feature extracting neurons. In The Neurosciences, Third Study Program, ed. Worden, F.G. & Schmitt, F.O., pp. 105–133. Cambridge, Massachusetts: MIT Press.Google Scholar
Blakemore, C. & Van Sluyters, R.C. (1974). Reversal of the physiological effects of monocular deprivation in kittens: further evidence for a sensitive period. Journal of Physiology (London) 237, 195–216.CrossRefGoogle ScholarPubMed
Blakemore, C. & Van Sluyters, R.C. (1975). Innate and environmental factors in the development of the kitten's visual cortex. Journal of Physiology (London) 248, 663–716.CrossRefGoogle ScholarPubMed
Blakemore, C, Garey, L.J. & Vital-Durand, F. (1978). The physiological effects of monocular deprivation and their reversal in the monkey's visual cortex. Journal of Physiology (London) 283, 223–262.CrossRefGoogle ScholarPubMed
Cottrell, M. & Fort, J. C. (1986). A stochastic model of retinotopy: a self organizing process. Biological Cybernetics 53, 405–411.CrossRefGoogle ScholarPubMed
Cynader, M. & Mitchell, D.E. (1977). Monocular astigmatism effects on kitten visual cortex development. Nature (London) 270, 177–178.CrossRefGoogle ScholarPubMed
Frohn, H., Geigger, H. & Singer, W. (1987). A self-organizing neural network sharing features of the mammalian visual system. Biological Cybernetics 55, 333–343.CrossRefGoogle ScholarPubMed
Gustaffson, B. & Wigstrom, H. (1988). Physiological mechanisms underlying long-term potentiation. Trends in Neuroscience 11, 156–162.CrossRefGoogle Scholar
Hebb, D.O. (1949). The Organization of Behavior. New York: John Wiley.Google Scholar
Hirsch, H.V. B. & Spinelli, D.N. (1970). Visual experience modifies the distribution of horizontally and vertically oriented receptive fields in cats. Science 168, 869–871.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1962). Receptive fields, binocular interaction, and functional architecture in the cat's visual cortex. Journal of Physiology (London) 160, 106–154.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1965). Binocular interaction in striate cortex of kittens reared with artificial squint. Journal of Neurophys-iology 28, 1041–1059.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
Katz, L.C. & Constantine-Paton, M. (1988). Relationships between segregated afferents and postsynaptic neurons in the optic tectum of three-eyed frog. Journal of Neuroscience 8, 3160–3180.CrossRefGoogle Scholar
Levitt, F.B. & Van Sluyters, R.C. (1982). Recovery of binocular function in kitten visual cortex. Journal of Neurophysiology 48, 1336–1345.CrossRefGoogle ScholarPubMed
Linsker, R. (1986 a). From basic network principles to neural architecture: emergence of spatial opponent cells. Proceedings of the National Academy of Sciences of the U.S.A. 83, 7508–7512.CrossRefGoogle ScholarPubMed
Linsker, R. (1986 b). From basic network principles to neural architecture: emergence of orientation selective cells. Proceedings of the National Academy of Sciences of the U.S.A. 83, 8390–8394.CrossRefGoogle ScholarPubMed
Linsker, R. (1986 C). From basic network principles to neural architecture: emergence of orientation columns. Proceedings of the National Academy of Sciences of the U.S.A. 83, 8779–8783.CrossRefGoogle ScholarPubMed
Malach, R., Ebert, R. & Van Sluyters, R.C. (1984). Recovery from effects of brief monocular deprivation in the kitten. Journal of Neurophysiology 51, 538–551.CrossRefGoogle ScholarPubMed
Movshon, J.A. & Van Sluyters, R.C. (1981). Visual neural development. Annual Review of Psychology 32, 477–522.CrossRefGoogle ScholarPubMed
Palm, G. (1982). Neural assemblies, an alternative approach to artificial intelligence. In Studies of Brain Function, Vol. 7, ed. Braiten-Berg, V., Berlin/New York: Springer-Verlag.Google Scholar
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, 215–239.CrossRefGoogle ScholarPubMed
Reiter, H.O. & Stryker, M.P. (1988). Neural plasticity without postsynaptic 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, 3623–3627.CrossRefGoogle ScholarPubMed
Singer, W., Rauschecker, J. & Werth, R. (1977). Effect of monocular exposure to temporal contrasts on ocular dominance in kittens. Brain Research 134, 568–572.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., Sherk, H., Leventhal, A.G. & Hirsch, H.V.B. (1978). Physiological consequences for the cat's visual cortex of effectively restricting early visual experience with oriented contours. Journal of Neurophysiology 4, 896–909.CrossRefGoogle Scholar
Sluyters, R.C.Van (1978). Reversal of the physiological effects of brief periods of monocular deprivation in the kitten. Journal of Physiology (London) 284, 1–17.CrossRefGoogle ScholarPubMed
Sluyters, R.C.Van & Levitt, F.B. (1980). Experimental strabismus in the kitten. Journal of Neurophysiology 43, 686–699.CrossRefGoogle ScholarPubMed
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, 1003–1017.CrossRefGoogle ScholarPubMed
Wilson, J.R., Webb, S.V. & Sherman, S.M. (1977). Conditions for dominance of one eye during competitive development of central connections in visually deprived cats. Brain Research 136, 277–287.CrossRefGoogle ScholarPubMed