Auditory compensation for early blindness in cat cerebral cortex

Single-neuron activity was recorded in the caudal part of the anterior ectosylvian (AE) cortex of cats that had been deprived of vision for several years by means of binocular lid suture shortly after birth and in normal control animals. Over 300 neurons were tested in each group with auditory, visual, and somatosensory stimuli. We confirmed the existence of an anterior ectosylvian visual area (AEV) in the fundus and ventral bank of the AE sulcus. Neurons in AEV had purely visual responses in normal cats. In visually deprived cats, by contrast, only a minority of cells in this area still responded to visual stimulation. Instead, most cells reacted vigorously to auditory and, to some extent, somatosensory stimuli. The few remaining visual neurons were also driven by auditory or somatosensory stimuli. No increase in the number of unresponsive neurons was found. It appears, therefore, that a cortical region that normally represents visual activity can become driven by auditory or somatosensory activity as a result of visual deprivation. Our results imply that early blindness causes compensatory increases in the amount of auditory cortical representation, possibly by an expansion of nonvisual areas into previously visual territory. In particular, they provide evidence for the existence of neural mechanisms for intermodal compensatory plasticity in the cerebral cortex of young animals. The changes described here may also provide the neural basis for a behavioral compensation for early blindness described elsewhere.

[1]  Markus Lappe,et al.  A Neural Network for the Processing of Optic Flow from Ego-Motion in Man and Higher Mammals , 1993, Neural Computation.

[2]  J. Rauschecker,et al.  Crossmodal changes in the somatosensory vibrissa/barrel system of visually deprived animals. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[3]  M. Mishkin,et al.  Massive cortical reorganization after sensory deafferentation in adult macaques. , 1991, Science.

[4]  D. O'Leary,et al.  Potential of visual cortex to develop an array of functional units unique to somatosensory cortex , 1991, Science.

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

[6]  M. Sur,et al.  A map of visual space induced in primary auditory cortex. , 1990, Science.

[7]  D. Irvine,et al.  The anterior ectoylvian sulcal auditory field in the cat: II. A horseradisha peroxidase study of its thalamic and cortical connections , 1990 .

[8]  D. Irvine,et al.  The anterior ectosylvian sulcal auditory field in the cat: I. An electrophysiological study of its relationship to surrounding auditory cortical fields , 1990, The Journal of comparative neurology.

[9]  J. Rauschecker,et al.  Centrifugal motion bias in the cat's lateral suprasylvian visual cortex is independent of early flow field exposure. , 1990, The Journal of physiology.

[10]  H. R. Clemo,et al.  Auditory cortical projection from the anterior ectosylvian sulcus (Field AES) to the superior colliculus in the cat: an anatomical and electrophysiological study. , 1989, The Journal of comparative neurology.

[11]  P. Rakic Specification of cerebral cortical areas. , 1988, Science.

[12]  C. Olson,et al.  Ectosylvian visual area of the cat: Location, retinotopic organization, and connections , 1987, The Journal of comparative neurology.

[13]  H. Tanila,et al.  Late effects of early binocular visual deprivation on the function of Brodmann's area 7 of monkeys (Macaca arctoides). , 1987, Brain research.

[14]  Giancarlo Tassinari,et al.  Visual and somatosensory integration in the anterior ectosylvian cortex of the cat , 1987, Brain Research.

[15]  J. Rauschecker,et al.  Centrifugal organization of direction preferences in the cat's lateral suprasylvian visual cortex and its relation to flow field processing , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  D. Irvine,et al.  Auditory response properties of neurons in the anterior ectosylvian sulcus of the cat , 1986, Brain Research.

[17]  S. Clarke,et al.  Bilateral transitory projection to visual areas from auditory cortex in kittens. , 1984, Brain research.

[18]  H. R. Clemo,et al.  Organization of a fourth somatosensory area of cortex in cat. , 1983, Journal of neurophysiology.

[19]  J. Hyvärinen,et al.  Early visual deprivation alters modality of neuronal responses in area 19 of monkey cortex , 1981, Neuroscience Letters.

[20]  Trichur Raman Vidyasagar,et al.  Possible plasticity in the rat superior colliculus , 1978, Nature.

[21]  H. Hirsch,et al.  Physiological consequences for the cat's visual cortex of effectively restricting early visual experience with oriented contours. , 1978, Journal of neurophysiology.

[22]  P. Knight,et al.  Representation of the cochlea within the anterior auditory field (AAF) of the cat , 1977, Brain Research.

[23]  E. Chapman The Effects of Blindness and Other Impairments on Early Development , 1976 .

[24]  W. Singer,et al.  Receptive-field properties and neuronal connectivity in striate and parastriate cortex of contour-deprived cats. , 1976, Journal of neurophysiology.

[25]  L. Hartlage Development of Spatial Concepts in Visually Deprived Children , 1976, Perceptual and motor skills.

[26]  G. F. Cooper,et al.  Development of the Brain depends on the Visual Environment , 1970, Nature.

[27]  D. Hubel,et al.  Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. , 1965, Journal of neurophysiology.

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

[29]  W. N. Kellogg,et al.  Sonar system of the blind. , 1962, Science.

[30]  A. L. Berman Interaction of cortical responses to somatic and auditory stimuli in anterior ectosylvian gyrus of cat. , 1961, Journal of neurophysiology.

[31]  J. Lebensohn Effects of Early Blindness , 1959 .

[32]  D. Frost,et al.  Visual responses of neurons in somatosensory cortex of hamsters with experimentally induced retinal projections to somatosensory thalamus. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[33]  O D Creutzfeldt,et al.  Anterior ectosylvian visual area (AEV) of the cat: physiological properties. , 1988, Progress in brain research.

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

[35]  C R Olson,et al.  An outlying visual area in the cerebral cortex of the cat. , 1983, Progress in brain research.

[36]  R. Andersen,et al.  Auditory Forebrain Organization , 1982 .

[37]  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.

[38]  W Niemeyer,et al.  Do the blind hear better? Investigations on auditory processing in congenital or early acquired blindness. II. Central functions. , 1981, Audiology : official organ of the International Society of Audiology.

[39]  W Niemeyer,et al.  Do the blind hear better? Investigations on auditory processing in congenital or early acquired blindness. I. Peripheral functions. , 1981, Audiology : official organ of the International Society of Audiology.

[40]  M. Carreras,et al.  Functional properties of neurons of the anterior ectosylvian gyrus of the cat. , 1963, Journal of neurophysiology.

[41]  Seymour Axelrod,et al.  Effects of early blindness : performance of blind and sighted children on tactile and auditory tasks , 1959 .

[42]  P. Worchel,et al.  Space Perception and Orientation by the Blind , 1951 .

[43]  C. Seashore,et al.  The comparative sensitiveness of blind and seeing persons. , 1918 .