Cellular analogs of visual cortical epigenesis. II. Plasticity of binocular integration

Two differential pairing procedures were applied in the primary visual cortex of anesthetized and paralyzed kittens and cats, to produce changes in ocular dominance and interocular orientation disparity (IOD) during the time of recording of a single neuron. A first experiment was devised to demonstrate plasticity in the balance of monocular responses. The visual activity of the cell was driven iontophoretically to either a “high” or a “low” level, depending on the ocularity of the visual stimulation. Ocular dominance measurements before and after pairing revealed significant long-lasting changes in 33% of cases. Relative ocular preference shifted in most cases (87.5%) in favor of the reinforced eye. Similar proportions of significant changes were observed in kitten and adult cortex. The amplitude of the functional modifications was not significantly related with age, although the largest changes in ocular dominance were recorded at the peak of the critical period. The second experiment more specifically addressed the plasticity of binocular interaction. The activity of a binocular cell was driven iontophoretically to either a “high” or a “low” level, depending on the orientation disparity between two oriented stimuli, presented simultaneously and separately in the receptive field of each eye. Significant long-lasting changes in binocular responses were induced in 40% of cases. The relative IOD preference generally shifted (67%) in favor of the reinforced disparity. In half of the modified cells, functional changes were expressed only in the dichoptic viewing condition used during the pairing procedure. These functional modifications of binocular integration, demonstrated at the cellular level, are analogous to those induced by global manipulations of the visual environment (Hubel and Wiesel, 1970; Shinkman and Bruce, 1977). They are interpreted as evidence for synaptic plasticity. Our results support the hypothesis that covariance levels between pre- and postsynaptic activities determine the sign and the amplitude of changes in synaptic efficacy.

[1]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[2]  D. Hubel,et al.  SINGLE-CELL RESPONSES IN STRIATE CORTEX OF KITTENS DEPRIVED OF VISION IN ONE EYE. , 1963, Journal of neurophysiology.

[3]  D. Hubel,et al.  Binocular interaction in striate cortex of kittens reared with artificial squint. , 1965, Journal of neurophysiology.

[4]  D. Hubel,et al.  The period of susceptibility to the physiological effects of unilateral eye closure in kittens , 1970, The Journal of physiology.

[5]  P. O. Bishop,et al.  Binocular interaction fields of single units in the cat striate cortex , 1971, The Journal of physiology.

[6]  C. Blakemore,et al.  A second neural mechanism of binocular depth discrimination , 1972, The Journal of physiology.

[7]  H. Barlow,et al.  Kitten Visual Cortex: Short-Term, Stimulus-Induced Changes in Connectivity , 1973, Science.

[8]  G. Stent A physiological mechanism for Hebb's postulate of learning. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[9]  C. Blakemore,et al.  Reversal of the physiological effects of monocular deprivation in kittens: further evidence for a sensitive period , 1974, The Journal of physiology.

[10]  C. Blakemore,et al.  Innate and environmental factors in the development of the kitten's visual cortex. , 1975, The Journal of physiology.

[11]  C. Blakemore,et al.  Synaptic competition in the kitten's visual cortex. , 1976, Cold Spring Harbor symposia on quantitative biology.

[12]  P. B. Schechter,et al.  Brief monocular visual experience and kitten cortical binocularity , 1976, Brain Research.

[13]  D. Mitchell,et al.  Monocular astigmatism effects on kitten visual cortex development , 1977, Nature.

[14]  J. Movshon,et al.  Effects of brief periods of unilateral eye closure on the kitten's visual system. , 1977, Journal of neurophysiology.

[15]  C. Bruce,et al.  Binocular differences in cortical receptive fields of kittens after rotationally disparate binocular experience. , 1977, Science.

[16]  P. O. Bishop,et al.  Discrimination of orientation and position disparities by binocularly activated neurons in cat straite cortex. , 1977, Journal of neurophysiology.

[17]  S. Levay,et al.  Ocular dominance columns and their development in layer IV of the cat's visual cortex: A quantitative study , 1978, The Journal of comparative neurology.

[18]  M. Imbert,et al.  Ocular motility and recovery of orientational properties of visual cortical neurones in dark-reared kittens , 1978, Nature.

[19]  T. Tsumoto,et al.  Cross-depression: an electrophysiological manifestation of binocular competition in the developing visual cortex , 1979, Brain Research.

[20]  R. Freeman,et al.  Is there a ‘consolidation’ effect for monocular deprivation? , 1979, Nature.

[21]  D E Mitchell,et al.  Prolonged sensitivity to monocular deprivation in dark-reared cats. , 1980, Journal of neurophysiology.

[22]  R. C. Van Sluyters,et al.  Experimental strabismus in the kitten. , 1980, Journal of neurophysiology.

[23]  W. Singer,et al.  The effects of early visual experience on the cat's visual cortex and their possible explanation by Hebb synapses. , 1981, The Journal of physiology.

[24]  P. O. Bishop,et al.  Binocular interaction on monocularly discharged lateral geniculate and striate neurons in the cat. , 1981, Journal of neurophysiology.

[25]  J. Movshon,et al.  Visual neural development. , 1981, Annual review of psychology.

[26]  E. Bienenstock,et al.  Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  M. Isley,et al.  Prolonged dark rearing and development of interocular orientation disparity in visual cortex. , 1983, Journal of neurophysiology.

[28]  R. von der Heydt,et al.  Plasticity in the binocular correspondence of striate cortical receptive fields in kittens. , 1983, The Journal of physiology.

[29]  Professor Dr. Guy A. Orban Neuronal Operations in the Visual Cortex , 1983, Studies of Brain Function.

[30]  Y. Frégnac,et al.  Development of neuronal selectivity in primary visual cortex of cat. , 1984, Physiological reviews.

[31]  P. D. Spear,et al.  Critical periods for effects of monocular deprivation: differences between striate and extrastriate cortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  M. Cynader,et al.  Somatosensory cortical map changes following digit amputation in adult monkeys , 1984, The Journal of comparative neurology.

[33]  M. Cynader,et al.  Disruption of cortical activity prevents ocular dominance changes in monocularly deprived kittens , 1984, Nature.

[34]  T. Kasamatsu,et al.  Plasticity in cat visual cortex restored by electrical stimulation of the locus coeruleus , 1985, Neuroscience Research.

[35]  V. Casagrande,et al.  Advances in neural and behavioral development , 1985 .

[36]  Robert M. Douglas,et al.  A time-based stereoscopic depth mechanism in the visual cortex , 1985, Brain Research.

[37]  Norman M. Weinberger,et al.  Classical conditioning rapidly induces specific changes in frequency receptive fields of single neurons in secondary and ventral ectosylvian auditory cortical fields , 1986, Brain Research.

[38]  M. Stryker,et al.  Ocular dominance shift in kitten visual cortex caused by imbalance in retinal electrical activity , 1986, Nature.

[39]  Y Trotter,et al.  The period of susceptibility of visual cortical binocularity to unilateral proprioceptive deafferentation of extraocular muscles. , 1987, Journal of neurophysiology.

[40]  T. Tsumoto,et al.  NMDA receptors in the visual cortex of young kittens are more effective than those of adult cats , 1987, Nature.

[41]  W. Singer,et al.  Long-term potentiation and NMDA receptors in rat visual cortex , 1987, Nature.

[42]  Y. Frégnac,et al.  A cellular analogue of visual cortical plasticity , 1988, Nature.

[43]  M. Stryker,et al.  Neural plasticity without postsynaptic action potentials: less-active inputs become dominant when kitten visual cortical cells are pharmacologically inhibited. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[44]  W. Singer,et al.  Pharmacological induction of use-dependent receptive field modifications in the visual cortex. , 1988, Science.

[45]  K Toyama,et al.  Long-term potentiation of synaptic transmission in kitten visual cortex. , 1988, Journal of neurophysiology.

[46]  W Singer,et al.  Chronic recordings from single sites of kitten striate cortex during experience-dependent modifications of receptive-field properties. , 1989, Journal of neurophysiology.

[47]  N. Daw,et al.  The location and function of NMDA receptors in cat and kitten visual cortex , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[48]  I. Ohzawa,et al.  On the neurophysiological organization of binocular vision , 1990, Vision Research.

[49]  M. Isley,et al.  Interocular torsional disparity and visual cortical development in the cat. , 1990, Journal of Neurophysiology.

[50]  Y. Komatsu,et al.  Postnatal development of neuronal connections in cat visual cortex studied by intracellular recording in slice preparation , 1991, Brain Research.

[51]  E. Capaldi,et al.  The organization of behavior. , 1992, Journal of applied behavior analysis.

[52]  Y. Frégnac,et al.  Cellular analogs of visual cortical epigenesis. I. Plasticity of orientation selectivity , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[53]  M. Bear,et al.  Hebbian synapses in visual cortex , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[54]  Dynamic properties of visual cortical cells , 1994 .