Lack of lateral inhibitory interactions in visual cortex of monocularly deprived cats

To gain new insight into the effects of monocular deprivation, we studied the visual cortex of adult cats deprived of vision in one eye. Local field potentials were recorded in response to contrast reversal of square-wave gratings modulated in time either by pseudorandom, m-sequences or periodically. We have found that: (1) stimulation of the retinotopic locus of the recording site elicits responses with abnormal waveforms and long latencies from the deprived eye; (2) stimulation of a remote, non-retinotopic locus elicits responses from the non-deprived eye but not from the deprived eye; (3) the monocularly deprived cortex lacks lateral inhibitory interactions which are characteristic of the normal cortex; and (4) steady-state responses showed little difference in spatial-frequency tuning and contrast sensitivity between the deprived and non-deprived eye, mostly conforming to earlier field-potential data in monocular deprivation. Functional lateral interactions appear to be greatly reduced in monocularly deprived cortex.

[1]  Colin Blakemore,et al.  The role of GABAergic inhibition in the cortical effects of monocular deprivation , 1981, Nature.

[2]  J A Solomon,et al.  Texture interactions determine perceived contrast , 1989, Proceedings of the National Academy of Sciences of the United States of America.

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

[4]  T. Kasamatsu,et al.  Retinotopic and nonretinotopic field potentials in cat visual cortex , 1994, Visual Neuroscience.

[5]  T. Wiesel,et al.  Lateral interactions in visual cortex. , 1990, Cold Spring Harbor symposia on quantitative biology.

[6]  T. Wiesel,et al.  Morphology and intracortical projections of functionally characterised neurones in the cat visual cortex , 1979, Nature.

[7]  T. Wiesel,et al.  Clustered intrinsic connections in cat visual cortex , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  J. L. Conway,et al.  Bicuculline reversal of deprivation amblyopia in the cat , 1976, Nature.

[9]  M. Wong-Riley Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry , 1979, Brain Research.

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

[11]  J. Nelson,et al.  Orientation-selective inhibition from beyond the classic visual receptive field , 1978, Brain Research.

[12]  M. Stryker,et al.  Ocular dominance in layer IV of the cat's visual cortex and the effects of monocular deprivation. , 1978, The Journal of physiology.

[13]  R. B. Pinter,et al.  Nonlinear Vision: Determination of Neural Receptive Fields, Function, and Networks , 1992 .

[14]  A. L. Humphrey,et al.  Anatomical banding of intrinsic connections in striate cortex of tree shrews (Tupaia glis) , 1982, The Journal of comparative neurology.

[15]  J. Pettigrew,et al.  A role for extraocular afferents in post‐critical period reversal of monocular deprivation. , 1978, The Journal of physiology.

[16]  Mark W. Cannon,et al.  Spatial interactions in apparent contrast: Inhibitory effects among grating patterns of different spatial frequencies, spatial positions and orientations , 1991, Vision Research.

[17]  K. Tanaka,et al.  Organization of cat visual cortex as investigated by cross-correlation technique. , 1981, Journal of neurophysiology.

[18]  T. Wiesel,et al.  Relationships between horizontal interactions and functional architecture in cat striate cortex as revealed by cross-correlation analysis , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  T. Tsumoto,et al.  Evidence for excitatory connections from the deprived eye to the visual cortex in monocularly deprived kittens , 1978, Brain Research.

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

[21]  S. Sherman,et al.  Organization of visual pathways in normal and visually deprived cats. , 1982, Physiological reviews.

[22]  Ee Sutter,et al.  A deterministic approach to nonlinear systems analysis , 1992 .

[23]  H. J. Luhmann,et al.  Horizontal Interactions in Cat Striate Cortex: I. Anatomical Substrate and Postnatal Development , 1990, The European journal of neuroscience.

[24]  T. Wiesel,et al.  Columnar specificity of intrinsic horizontal and corticocortical connections in cat visual cortex , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  C. Li,et al.  Extensive integration field beyond the classical receptive field of cat's striate cortical neurons--classification and tuning properties. , 1994, Vision research.

[26]  H. Berg Cold Spring Harbor Symposia on Quantitative Biology.: Vol. LII. Evolution of Catalytic Functions. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, 1987, ISBN 0-87969-054-2, xix + 955 pp., US $150.00. , 1989 .

[27]  R E Weller,et al.  Structural correlates of functionally distinct X‐cells in the lateral geniculate nucleus of the cat , 1988, The Journal of comparative neurology.

[28]  C. Gilbert,et al.  Improvement in visual sensitivity by changes in local context: Parallel studies in human observers and in V1 of alert monkeys , 1995, Neuron.

[29]  D. Whitteridge,et al.  Form, function and intracortical projections of spiny neurones in the striate visual cortex of the cat. , 1984, The Journal of physiology.

[30]  I. Ohzawa,et al.  Monocularly deprived cats: binocular tests of cortical cells reveal functional connections from the deprived eye , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  S. Sherman,et al.  Spatial and temporal sensitivity of normal and amblyopic cats. , 1982, Journal of neurophysiology.

[32]  Anthony M. Norcia,et al.  Measurement of spatial contrast sensitivity with the swept contrast VEP , 1989, Vision Research.

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

[34]  U. Polat,et al.  Lateral interactions between spatial channels: Suppression and facilitation revealed by lateral masking experiments , 1993, Vision Research.

[35]  C. Gilbert,et al.  Synaptic physiology of horizontal connections in the cat's visual cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  M. Stryker,et al.  Relation of cortical cell orientation selectivity to alignment of receptive fields of the geniculocortical afferents that arborize within a single orientation column in ferret visual cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[37]  S. Sherman Functional organization of the W-, X-, and Y- cell pathways in the cat: A review and hypothesis , 1985 .

[38]  Tanaka The role of , 2000, Journal of insect physiology.

[39]  D. V. van Essen,et al.  Neuronal responses to static texture patterns in area V1 of the alert macaque monkey. , 1992, Journal of neurophysiology.

[40]  Erich E. Sutter,et al.  The Fast m-Transform: A Fast Computation of Cross-Correlations with Binary m-Sequences , 1991, SIAM J. Comput..

[41]  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.

[42]  C. Blakemore,et al.  The neural mechanism of binocular depth discrimination , 1967, The Journal of physiology.

[43]  U. Polat,et al.  Abnormal Long-range Spatial Interactions in Amblyopia , 1997, Vision Research.

[44]  An electrophysiological comparison of convergent and divergent strabismus in the cat: visual evoked potentials. , 1983, Journal of neurophysiology.

[45]  S. Bisti,et al.  Monocular deprivation in kittens differently affects crossed and uncrossed visual pathways , 1986, Vision Research.

[46]  L. Spillmann,et al.  Long-range interactions in visual perception , 1996, Trends in Neurosciences.

[47]  D. Hubel,et al.  The development of ocular dominance columns in normal and visually deprived monkeys , 1980, The Journal of comparative neurology.

[48]  K. Tanaka,et al.  Cross-Correlation Analysis of Interneuronal Connectivity in cat visual cortex. , 1981, Journal of neurophysiology.

[49]  R. Douglas,et al.  Opening the grey box , 1991, Trends in Neurosciences.

[50]  U. Polat,et al.  The architecture of perceptual spatial interactions , 1994, Vision Research.

[51]  P. D. Spear,et al.  Postcritical-period reversal of effects of monocular deprivation on striate cortex cells in the cat. , 1976, Journal of neurophysiology.

[52]  T. Kasamatsu,et al.  Cortical recovery from effects of monocular deprivation caused by diffusion and occlusion , 1991, Brain Research.

[53]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.