Advertisement

Orientation-dependent Changes in Response Properties of Neurons in the Kitten’s Visual Cortex

  • J. P. Rauschecker
Part of the NATO Advanced Study Institutes Series book series (NSSA, volume 27)

Abstract

Kittens were reared wearing goggles with cylindrical lenses, which restricted the visual experience of one eye to a very narrow range of orientations. The other eye was either occluded or allowed normal vision. Physiological changes caused by the selective exposure were assessed by means of single-cell recording from striate cortex.

In all cases the majority of neurons driven by the “cylinder eye” preferred the experienced orientation. When the second eye had been covered during the exposure, most units were dominated by the cylinder eye and had receptive field orientations in register with the orientation experienced by this eye. Neurons with other orientation preferences were shared between the two eyes.

When the second eye was allowed to view normally, the cylinder eye became strongly inferior. In this case many binocular cells were found, almost all of which preferred that orientation experienced by both eyes together. Neurons with other orientation preferences were dominated by the normal eye.

In a two-stage experiment, restricted vision of one eye (using the cylinder lens) followed normal experience of the other eye. Polar plots of preferred orientations for the two eyes show complementary distributions: the cylinder eye had selectively taken over neurons with corresponding receptive field orientations from the previously normal eye.

These experiments support the hypothesis that circuit changes in the visual cortex do not depend solely on asymmetries in the activation level of the afferents from the two eyes, but also on the response properties of the cortical target cells. Such a mechanism can account for both maintaining and specifying influences of visual experience on cortical response properties during early development.

Keywords

Visual Experience Cylindrical Lens Polar Plot Striate Cortex Ocular Dominance 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Barlow, H. B. (1975). Visual experience and cortical development. Nature 258:199–204.PubMedCrossRefGoogle Scholar
  2. Barlow, H. B., and J. D. Pettigrew (1971). Lack of specificity of neurones in the visual cortex of young kittens. J. Physiol. 218:98–100P.Google Scholar
  3. Blakemore, C., and G. F. Cooper (1970). Development of the brain depends on the visual environment. Nature 228:477–478.PubMedCrossRefGoogle Scholar
  4. Blakemore, C., and R. C. Van Sluyters (1974). Reversal of the physiological effects of monocular deprivation in kittens: further evidence for a sensitive period. J. Physiol. 237:19–216.Google Scholar
  5. Blakemore, C., and R. C. Van Sluyters (1975). Innate and environmental factors in the development of the kitten’s visual cortex. J. Physiol. 248:663–716.PubMedGoogle Scholar
  6. Buisseret, P., and M. Imbert (1976). Visual cortical cells: their developmental properties in normal and dark-reared kittens. J. Physiol. 255:511–525.PubMedGoogle Scholar
  7. Campbell, F. W., and J. G. Robson (1968). Application of Fourier analysis to the visibility of gratings. J. Physiol. 197:551–566.PubMedGoogle Scholar
  8. Campbell, F. W., L. Maffei, and M. Piccolino (1973). The contrast sensitivity of the cat. J. Physiol. 229:719–731.PubMedGoogle Scholar
  9. Cynader, M., and D. E. Mitchell (1977). Monocular astigmatism effects on kitten visual cortex development. Nature 270:177–178.PubMedCrossRefGoogle Scholar
  10. Freeman, R. D., and J. D. Pettigrew (1973). Alteration of visual cortex from environmental asymmetries. Nature 246:359–360.PubMedCrossRefGoogle Scholar
  11. Fregnac, Y., and M. Imbert (1978). Early development of visual cortical cells in normal and dark-reared kittens: relationship between orientation selectivity and ocular dominance. J. Physiol. 278:27–44.PubMedGoogle Scholar
  12. Hebb, D. O. (1949). The Organization of Behavior. New York, Wiley.Google Scholar
  13. Hirsch, H. V. B., and D. N. Spinelli (1970). Visual experience modifies distribution of horizontally and vertically oriented receptive fields in cats. Science 168:869–871.PubMedCrossRefGoogle Scholar
  14. Hubel, D. H., and T. N. Wiesel (1963). Receptive fields of cells in striate cortex of very young, visually inexperienced kittens. J. Neurophysiol. 26:994–1002.PubMedGoogle Scholar
  15. Imbert, M., and P. Buisseret (1975). Receptive field characteristics and plastic properties of visual cortical cells in kittens reared with or without visual experience. Exp. Brain Res. 22:25–36.PubMedCrossRefGoogle Scholar
  16. Movshon, J. A. (1976). Reversal of the physiological effects of monocular deprivation in the kitten’s visual cortex. J. Physiol. 261:125–174.PubMedGoogle Scholar
  17. Pettigrew, J. D. (1974). The effect of visual experience on the development of stimulus specificity by kitten cortical neurones. J. Physiol. 237:49–74.PubMedGoogle Scholar
  18. Pettigrew, J. D. (1978). The paradox of the critical period for striate cortex. In: Neuronal Plasticity. C. W. Cotman (ed.). Raven Press, New York, pp. 311–330.Google Scholar
  19. Rauschecker, J. P., and W. Singer (1978). Experience-dependent modification of response properties in striate cortex: instructive versus selective mechanisms. Neuroscience Letters, Suppl. 1, S395.Google Scholar
  20. Rauschecker, J. P., and W. Singer (1978). Changes in the circuitry of the kitten’s visual cortex are gated by postsynaptic activity. Nature (submitted).Google Scholar
  21. Rauschecker, J. P., and W. Singer (1979b). Selective and instructive effects of early visual experience on the cat’s cortex: the same neural mechanism. In preparation.Google Scholar
  22. Sherk, H., and M. P. Stryker (1976). Quantitative study of cortical orientation selectivity in visually inexperienced kittens. J. Neurophysiol. 39:63–70.PubMedGoogle Scholar
  23. Sherman, S. M., R. W. Guillery, J. H. Kaas, and K. J. Sanderson (1974). Behavioral, electrophysiological, and morphological studies of binocular competition in the development of the geniculo-cortical pathways of cats. J. comp. Neurol. 158:1–18.PubMedCrossRefGoogle Scholar
  24. Singer, W. (1976). Modification of orientation and direction selectivity of cortical cells in kittens with monocular vision. Brain Res. 118:460–468.PubMedCrossRefGoogle Scholar
  25. Singer, W., and F. Tretter (1976). Receptive-field properties and neuronal connectivity in striate and parastriate cortex of contour-deprived cats. J. Neurophysiol. 39:613–630.PubMedGoogle Scholar
  26. Singer, W., J. P. Rauschecker, and R. Werth (1977). The effect of monocular exposure to temporal contrasts on ocular dominance in kittens. Brain Res. 134:568–572.PubMedCrossRefGoogle Scholar
  27. Stent, G. S. (1973). A physiological mechanism for Hebb’s postulate of learning. Proc. Nat. Acad. Sci. (U.S.A.) 70:997–1001.CrossRefGoogle Scholar
  28. Stryker, M. P., and H. Sherk (1975). Modification of cortical orientation selectivity in the cat by restricted visual experience: a reexamination. Science 190:904–906.PubMedCrossRefGoogle Scholar
  29. Stryker, M. P., H. Sherk, A. G. Leventhal, and H. V. B. Hirsch (1978). Physiological consequences for the cat’s visual cortex of effectively restricting early visual experience with oriented contours. J. Neurophysiol. 41:896–909.PubMedGoogle Scholar
  30. Tretter, F., M. Cynader, and W. Singer (1975). Modification of direction selectivity of neurons in the visual cortex of kittens. Brain Res. 84:143–149.PubMedCrossRefGoogle Scholar
  31. Wiesel, T. N., and D. H. Hubel (1963). Single-cell responses in striate cortex of kittens deprived of vision in one eye. J. Neurophysiol. 26:1003–1017.PubMedGoogle Scholar
  32. Wiesel, T. N., and D. H. Hubel (1965a). Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. J. Neurophysiol. 28:1029–1040.PubMedGoogle Scholar
  33. Wiesel, T. N., and D. H. Hubel (1965b). Extent of recovery from the effects of visual deprivation in kittens. J. Neurophysiol. 28:1060–1072.PubMedGoogle Scholar

Copyright information

© Plenum Press, New York 1979

Authors and Affiliations

  • J. P. Rauschecker
    • 1
  1. 1.Max-Planck-Institut für PsychiatrieMunichGermany

Personalised recommendations