The role of visual experience in the development of cat striate cortex

Summary1.By the third postnatal week, intrinsic developmental programs have established a framework within the cat visual system; this will be used to guide the course of subsequent experience-dependent development. Key elements in this framework are precociously mature cells in visual cortex area 17. These orientation-selective cells are predominantly first-order neurons, they are concentrated in layers IV and VI of area 17, most of them are activated monocularly, many may receive their direct excitatory input from lateral geniculate nucleus X cells, and the distribution of their preferred orientations is biased toward horizontal and vertical.2.Between the third and the sixth postnatal week, most of the remaining cells in area 17 develop orientation selectivity; this extension of orientation selectivity is blocked or delayed if kittens are deprived of normal patterned visual stimulation. Furthermore, exposure to a limited range of stimulus orientations can lead to an increase in the proportion of orientation-selective cells, and the range of orientation preferences that the cells acquire is restricted by the range of orientations to which the animal is exposed. This occurs with no apparent change in the physiology or morphology of intrinsically selective area 17 cells. Thus selective exposure may have its effect by influencing the connections between the intrinsically selective cells and higher-order neurons in area 17.3.Experience-dependent changes in the visual system may function to “fine-tune” sensory processing and thus optimize the system's response to the dominant features of the environment. This experience-dependent process could help the young animal to focus its “attention” on those features of its environment that are critical to its survival.

[1]  D. Burr,et al.  Functional implications of cross-orientation inhibition of cortical visual cells. I. Neurophysiological evidence , 1982, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[2]  M. Stryker,et al.  Modification of cortical orientation selectivity in the cat by restricted visual experience: a reexamination , 1975, Science.

[3]  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.

[4]  B. Gordon,et al.  Orientation deprivation in cat: What produces the abnormal cells? , 2004, Experimental Brain Research.

[5]  D. Mitchell,et al.  Behavioral deficits in cats following early selected visual exposure to contours of a single orientation , 1975, Brain Research.

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

[7]  H. Hirsch,et al.  Cortical effect of selective visual experience: degeneration or reorganization? , 1973, Brain research.

[8]  H. Hirsch Visual perception in cats after environmental surgery , 2004, Experimental Brain Research.

[9]  K. Kratz Spatial and temporal sensitivity of lateral geniculate cells in dark-reared cats , 1982, Brain Research.

[10]  R L Meyer,et al.  Tetrodotoxin blocks the formation of ocular dominance columns in goldfish. , 1982, Science.

[11]  A. Kendon,et al.  Organization of behavior in face-to-face interaction , 1975 .

[12]  H. Barlow,et al.  MAINTAINED ACTIVITY IN THE CAT'S RETINA IN LIGHT AND DARKNESS , 1957, The Journal of general physiology.

[13]  M. Imbert,et al.  Visual cortical cells: their developmental properties in normal and dark reared kittens. , 1976, The Journal of physiology.

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

[15]  W. R. Levick,et al.  Astigmatic visual deprivation in cat: Behavioral, optical and retinophysiological consequences , 1982, Vision Research.

[16]  G. Henry,et al.  The afferent connections and laminar distribution of cells in the cat striate cortex , 1979, The Journal of comparative neurology.

[17]  R. C. Tees,et al.  Effect of controlled rearing on the development of stimulus-seeking behavior in rats. , 1980, Journal of comparative and physiological psychology.

[18]  H. Hirsch,et al.  Cortical effect of early selective exposure to diagonal lines , 1975, Science.

[19]  D. Hubel,et al.  Shape and arrangement of columns in cat's striate cortex , 1963, The Journal of physiology.

[20]  J. Pettigrew,et al.  The effect of visual experience on the development of stimulus specificity by kitten cortical neurones , 1974, The Journal of physiology.

[21]  H. Wässle,et al.  The structural correlate of the receptive field centre of alpha ganglion cells in the cat retina. , 1983, The Journal of physiology.

[22]  O. D. Creutzfeldt,et al.  Representation of complex visual stimuli in the brain , 1978, Naturwissenschaften.

[23]  W. Levick,et al.  Orientation bias of cat retinal ganglion cells , 1980, Nature.

[24]  J. Schmidt,et al.  The re-establishment of synaptic transmission by regenerating optic axons in goldfish: Time course and effects of blocking activity by intraocular injection of tetrodotoxin , 1983, Brain Research.

[25]  M Imbert,et al.  Plasticity in the kitten's visual cortex: effects of the suppression of visual experience upon the orientational properties of visual cortical cells. , 1982, Brain research.

[26]  D. Ferster,et al.  The axonal arborizations of lateral geniculate neurons in the striate cortex of the cat , 1978, The Journal of comparative neurology.

[27]  L. Maffei,et al.  Selective impairment of contrast sensitivity in kittens exposed to periodic gratings. , 1978, The Journal of physiology.

[28]  R L Meyer,et al.  Tetrodotoxin inhibits the formation of refined retinotopography in goldfish. , 1983, Brain research.

[29]  Helmut V. B. Hirsch,et al.  Functional Modification of the Developing Visual System , 1978 .

[30]  H. Hirsch,et al.  Effects of early experience upon orientation sensitivity and binocularity of neurons in visual cortex of cats. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[31]  C. Blakemore The conditions required for the maintenance of binocularity in the kitten's visual cortex. , 1976, The Journal of physiology.

[32]  K. Toyama,et al.  An intracellular study of neuronal organization in the visual cortex , 2004, Experimental Brain Research.

[33]  S. Sherman,et al.  Lateral geniculate nucleus in dark-reared cats: loss of Y cells without changes in cell size. , 1979, Science.

[34]  M. Colonnier THE TANGENTIAL ORGANIZATION OF THE VISUAL CORTEX. , 1964, Journal of anatomy.

[35]  A. Leventhal,et al.  Structural basis of orientation sensitivity of cat retinal ganglion cells , 1983, The Journal of comparative neurology.

[36]  C. Blakemore,et al.  Experimental Creation of Unusual Neuronal Properties in Visual Cortex of Kitten , 1973, Nature.

[37]  J Bullier,et al.  Comparison of response of properties of three types of monosynaptic S-cell in cat striate cortex. , 1982, Journal of Neurophysiology.

[38]  G. Henry,et al.  Ordinal position of neurons in cat striate cortex. , 1979, Journal of neurophysiology.

[39]  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.

[40]  A. Leventhal,et al.  Relationship between preferred orientation and receptive field position of neurons in cat striate cortex , 1983, The Journal of comparative neurology.

[41]  C. Gilbert Microcircuitry of the visual cortex. , 1983, Annual review of neuroscience.

[42]  D. N. Spinelli,et al.  Visual Experience Modifies Distribution of Horizontally and Vertically Oriented Receptive Fields in Cats , 1970, Science.

[43]  J. Pettigrew,et al.  Biases for oriented moving bars in lateral geniculate nucleus neurons of normal and stripe-reared cats , 1977, Experimental Brain Research.

[44]  R. Hess,et al.  The horizontal spread of intracortical inhibition in the visual cortex , 1975, Experimental Brain Research.

[45]  S. Kaplan The Physiology of Thought , 1950 .

[46]  J. Z. YOUNG,et al.  The Visual System of Octopus : (1)Regularities in the Retina and Optic Lobes of Octopus in Relation to Form Discrimination , 1960, Nature.

[47]  Y. Frégnac,et al.  Early development of visual cortical cells in normal and dark‐reared kittens: relationship between orientation selectivity and ocular dominance. , 1978, The Journal of physiology.

[48]  L. Garey,et al.  The thalamic projection to cat visual cortex: Ultrastructure of neurons identified by golgi impregnation or retrograde horseradish peroxidase transport , 1981, Neuroscience.

[49]  H. Hirsch,et al.  Receptive-field properties of different classes of neurons in visual cortex of normal and dark-reared cats. , 1980, Journal of neurophysiology.

[50]  J. Bacon,et al.  Receptive fields of cricket giant interneurones are related to their dendritic structure. , 1984, The Journal of physiology.

[51]  D. N. Spinelli,et al.  Visual experience as a determinant of the response characteristics of cortical receptive fields in cats , 2004, Experimental Brain Research.

[52]  A. B. Bonds Development of Orientation Tuning in the Visual Cortex of Kittens , 1979 .

[53]  M. Cynader,et al.  Recovery of function in cat visual cortex following prolonged deprivation , 1976, Experimental Brain Research.

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

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

[56]  G. Henry,et al.  Anatomical organization of the primary visual cortex (area 17) of the cat. A comparison with area 17 of the macaque monkey , 1979, The Journal of comparative neurology.

[57]  Frank H. Duffy,et al.  Comparison of the effects of dark rearing and binocular suture on development and plasticity of cat visual cortex , 1981, Brain Research.

[58]  Trichur Raman Vidyasagar,et al.  Orientation sensitivity of cat LGN neurones with and without inputs from visual cortical areas 17 and 18 , 2004, Experimental Brain Research.

[59]  W. Singer,et al.  Restriction of visual experience to a single orientation affects the organization of orientation columns in cat visual cortex , 1981, Experimental Brain Research.

[60]  Behavioral consequences of early visual exposure to contours of a single orientation. , 1982, Brain research.

[61]  D. Mitchell,et al.  A physiological and behavioural study in cats of the effect of early visual experience with contours of a single orientation. , 1977, The Journal of physiology.

[62]  W. Singer,et al.  Organization of cat striate cortex: a correlation of receptive-field properties with afferent and efferent connections. , 1975, Journal of neurophysiology.

[63]  F. Duffy,et al.  The effects of dark-rearing on the development and plasticity of the lateral geniculate nucleus. , 1981, Brain research.

[64]  A. Sillito,et al.  A re-evaluation of the mechanisms underlying simple cell orientation selectivity , 1980, Brain Research.

[65]  W. Levick,et al.  Analysis of orientation bias in cat retina , 1982, The Journal of physiology.

[66]  D E Mitchell,et al.  Visual Resolution and Experience: Acuity Deficits in Cats Following Early Selective Visual Deprivation , 1973, Science.

[67]  A. Sillito The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat. , 1975, The Journal of physiology.

[68]  B. Dreher,et al.  Geniculate input to cat visual cortex: a comparison of area 19 with areas 17 and 18. , 1980, Journal of neurophysiology.

[69]  K. Albus,et al.  Effects of interacting visual patterns on single cell responses in cat's striate cortex , 1977, Vision Research.

[70]  J. Villablanca,et al.  Neurological development of kittens. , 1979, Developmental psychobiology.

[71]  D. W. Watkins,et al.  Receptive-field properties of neurons in binocular and monocular segments of striate cortex in cats raised with binocular lid suture. , 1978, Journal of neurophysiology.

[72]  B. B. Lee,et al.  The responses of magno- and parvocellular cells of the monkey's lateral geniculate body to moving stimuli , 1979, Experimental Brain Research.

[73]  S. W. Kuffler Discharge patterns and functional organization of mammalian retina. , 1953, Journal of neurophysiology.

[74]  P. Hammond Cat retinal ganglion cells: size and shape of receptive field centres , 1974, The Journal of physiology.

[75]  H. Hirsch,et al.  Effects of exposure to lines of one or two orientations on different cell types in striate cortex of cat. , 1983, The Journal of physiology.

[76]  D. Mastronarde Correlated firing of cat retinal ganglion cells. I. Spontaneously active inputs to X- and Y-cells. , 1983, Journal of neurophysiology.

[77]  D. N. Spinelli,et al.  Modification of the distribution of receptive field orientation in cats by selective visual exposure during development , 1971, Experimental Brain Research.

[78]  H. Hirsch,et al.  Principal components analysis of cells in cat visual cortex , 1982, Brain Research.

[79]  D. V. van Essen,et al.  Cell structure and function in the visual cortex of the cat , 1974, The Journal of physiology.

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

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

[82]  T. Tsumoto,et al.  GABAergic inhibition already operates on a group of neurons in the kitten visual cortex at the time of eye opening. , 1984, Brain research.

[83]  R. C. Emerson,et al.  Spatial sampling by dendritic trees in visual cortex , 1981, Brain Research.

[84]  J. Pettigrew,et al.  Visual Experience without Lines: Effect on Developing Cortical Neurons , 1973, Science.

[85]  H. Hirsch,et al.  Exposure to lines of only one orientation modifies dendritic morphology of cells in the visual cortex of the cat , 1982, The Journal of comparative neurology.

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

[87]  G. Henry,et al.  Different geniculate inputs to B and C cells of cat striate cortex , 2004, Experimental Brain Research.

[88]  K. Fleischhauer,et al.  [The tangential organization of the cat motor cortex]. , 1978, Verhandlungen der Anatomischen Gesellschaft.

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

[90]  C. Blakemore,et al.  Lateral inhibition between orientation detectors in the cat's visual cortex , 2004, Experimental Brain Research.

[91]  R. Glantz,et al.  A quantitative correlation of contour sensitivity with dendritic density in an identified visual neuron , 1983, Brain Research.

[92]  K. Albus,et al.  The geniculocortical system in the early postnatal kitten: An electrophysiological investigation , 2004, Experimental Brain Research.

[93]  A. Sillito Inhibitory mechanisms influencing complex cell orientation selectivity and their modification at high resting discharge levels. , 1979, The Journal of physiology.

[94]  K. Albus,et al.  Early post‐natal development of neuronal function in the kitten's visual cortex: a laminar analysis. , 1984, The Journal of physiology.

[95]  S M Archer,et al.  Abnormal development of kitten retino-geniculate connectivity in the absence of action potentials. , 1982, Science.

[96]  J. Schmidt,et al.  Activity sharpens the map during the regeneration of the retinotectal projection in goldfish , 1983, Brain Research.

[97]  H. Hirsch,et al.  Receptive-field properties of neurons in different laminae of visual cortex of the cat. , 1978, Journal of neurophysiology.