Receptive-field properties of deafferentated visual cortical neurons after topographic map reorganization in adult cats

When neurons in primary visual cortex of adult cats and monkeys are deprived of their normal sources of activation by matching lesions in the two retinas, they are capable of acquiring new receptive fields based on inputs from regions of intact retina around the lesions. Although these “reactivated” neurons respond to visual stimuli, quantitative studies of their response characteristics have not been attempted. Thus, it is not known whether these neurons have normal or abnormal features that could contribute to or disrupt an analysis of a visual scene. In this study, we used extracellular single-unit recording methods to investigate their stimulus selectivity and responsiveness. Specifically, we measured the sensitivity of individual neurons to stimulus orientation, direction of drift, spatial frequency, and contrast. Over 98% of all units in the denervated zone of cortex acquired new receptive fields after 3 months of recovery. Newly activated units exhibited strikingly normal orientation tuning, direction selectivity, and spatial frequency tuning when high-contrast (< 40%) stimuli were used. However, contrast thresholds of most neurons were abnormally elevated, and the maximum response amplitude under optimal stimulus conditions was significantly reduced. The results suggest that the striate cortical neurons reactivated during topographic reorganization are capable of sending functionally meaningful signals to more central structures provided that the visual scene contains relatively high contrast images.

[1]  Earl L. Smith,et al.  Binocular interactions in striate cortical neurons of cats reared with discordant visual inputs , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  Dennis M. Levi,et al.  Long-range dichoptic interactions in the human visual cortex in the region corresponding to the blind spot , 1994, Vision Research.

[3]  C. Gilbert,et al.  Axonal sprouting accompanies functional reorganization in adult cat striate cortex , 1994, Nature.

[4]  M Sur,et al.  Competitive interactions influencing the development of retinal axonal arbors in cat lateral geniculate nucleus. , 1993, Physiological reviews.

[5]  A. Burkhalter,et al.  Development of local circuits in human visual cortex , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  Rick J. Brown,et al.  Preattentive and cognitive effects on perceptual completion at the blind spot , 1993, Perception & psychophysics.

[7]  A. L. Humphrey,et al.  Evidence of input from lagged cells in the lateral geniculate nucleus to simple cells in cortical area 17 of the cat. , 1992, Journal of neurophysiology.

[8]  J. Kaas,et al.  Rapid reorganization of cortical maps in adult cats following restricted deafferentation in retina , 1992, Vision Research.

[9]  T. Wiesel,et al.  Receptive field dynamics in adult primary visual cortex , 1992, Nature.

[10]  R. Shapley,et al.  Directional selectivity and spatiotemporal structure of receptive fields of simple cells in cat striate cortex. , 1991, Journal of neurophysiology.

[11]  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.

[12]  R. L. Gregory,et al.  Perceptual filling in of artificially induced scotomas in human vision , 1991, Nature.

[13]  J. Rauschecker,et al.  Mechanisms of visual plasticity: Hebb synapses, NMDA receptors, and beyond. , 1991, Physiological reviews.

[14]  Y. Chino,et al.  Disruption of binocularly correlated signals alters the postnatal development of spatial properties in cat striate cortical neurons. , 1991, Journal of neurophysiology.

[15]  E. Callaway,et al.  Effects of binocular deprivation on the development of clustered horizontal connections in cat striate cortex. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[16]  T. Wiesel,et al.  The influence of contextual stimuli on the orientation selectivity of cells in primary visual cortex of the cat , 1990, Vision Research.

[17]  B. Payne,et al.  Representation of the ipsilateral visual field in the transition zone between areas 17 and 18 of the cat's cerebral cortex , 1990, Visual Neuroscience.

[18]  J. Kaas,et al.  Reorganization of retinotopic cortical maps in adult mammals after lesions of the retina. , 1990, Science.

[19]  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.

[20]  D. Ts'o,et al.  The organization of chromatic and spatial interactions in the primate striate cortex , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  J Sergent,et al.  An investigation into perceptual completion in blind areas of the visual field. , 1988, Brain : a journal of neurology.

[22]  D. Ferster Spatially opponent excitation and inhibition in simple cells of the cat visual cortex , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  E Kaplan,et al.  Contrast affects the transmission of visual information through the mammalian lateral geniculate nucleus. , 1987, The Journal of physiology.

[24]  D. Ferster Origin of orientation-selective EPSPs in simple cells of cat visual cortex , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  D. Ferster Orientation selectivity of synaptic potentials in neurons of cat primary visual cortex , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  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.

[27]  D. Whitteridge,et al.  Innervation of cat visual areas 17 and 18 by physiologically identified X‐ and Y‐ type thalamic afferents. I. Arborization patterns and quantitative distribution of postsynaptic elements , 1985, The Journal of comparative neurology.

[28]  A. L. Humphrey,et al.  Projection patterns of individual X‐ and Y‐cell axons from the lateral geniculate nucleus to cortical area 17 in the cat , 1985, The Journal of comparative neurology.

[29]  J Bullier,et al.  Branching and laminar origin of projections between visual cortical areas in the cat , 1984, The Journal of comparative neurology.

[30]  Y. Chino,et al.  Effects of rearing kittens with convergent strabismus on development of receptive-field properties in striate cortex neurons. , 1983, Journal of neurophysiology.

[31]  J. Lund,et al.  Intrinsic laminar lattice connections in primate visual cortex , 1983, The Journal of comparative neurology.

[32]  U. Eysel,et al.  Functional reconnections without new axonal growth in a partially denervated visual relay nucleus , 1982, Nature.

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

[34]  J. Pettigrew,et al.  Improved use of tapetal reflection for eye-position monitoring. , 1979, Investigative ophthalmology & visual science.

[35]  J. Movshon,et al.  Spatial and temporal contrast sensitivity of neurones in areas 17 and 18 of the cat's visual cortex. , 1978, The Journal of physiology.

[36]  H. Barlow,et al.  The effects of remote retinal stimulation on the responses of cat retinal ganglion cells. , 1977, The Journal of physiology.

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

[38]  M. Calford,et al.  Reorganization in the primary visual-cortex (V1) of adult cats occurs immediately following monocular retinal lesions , 1994 .

[39]  W. Singer Synchronization of cortical activity and its putative role in information processing and learning. , 1993, Annual review of physiology.

[40]  C. Milleret,et al.  Reorganization processes in the visual cortex also depend on visual experience in the adult cat. , 1993, Progress in brain research.

[41]  L C Katz,et al.  Development of local circuits in mammalian visual cortex. , 1992, Annual review of neuroscience.

[42]  J. Kaas Plasticity of sensory and motor maps in adult mammals. , 1991, Annual review of neuroscience.

[43]  M. Merzenich,et al.  Functional reorganization of primary somatosensory cortex in adult owl monkeys after behaviorally controlled tactile stimulation. , 1990, Journal of neurophysiology.

[44]  Lynne Kiorpes,et al.  The role of experience in visual development , 1990 .

[45]  James R. Coleman,et al.  Development of sensory systems in mammals , 1990 .

[46]  M. Wong-Riley,et al.  Quantitative light and electron microscopic analysis of cytochrome oxidase‐rich zones in V II prestriate cortex of the squirrel monkey , 1984, The Journal of comparative neurology.

[47]  J. Kaas,et al.  The reorganization of somatosensory cortex following peripheral nerve damage in adult and developing mammals. , 1983, Annual review of neuroscience.

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

[49]  U. Eysel,et al.  Reorganization of Retino-Geniculate Connections After Retinal Lesions in the Adult Cat , 1981 .

[50]  P. O. Bishop NEURAL MECHANISMS FOR BINOCULAR DEPTH DISCRIMINATION , 1981 .

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