Exposure to lines of only one orientation modifies dendritic morphology of cells in the visual cortex of the cat

To determine whether selective exposure to lines of one orientation modifies the shape of the dendritic fields of cells in visual cortex, we examined the dendritic morphology of neurons in area 17 of five normally reared cats, five cats reared viewing only vertical lines, and three cats reared viewing only horizontal lines. Kittens were placed with their mothers into a totally dark room before their eyes had opened. Beginning at 4 weeks of age, the kittens were brought out for daily periods of exposure wearing masks that limited the vision of each eye to a field of three vertical lines or three horizontal lines. After a minimum of 170 hours of exposure, the animals were killed and blocks of visual cortex were impregnated by the Golgi‐Kopsch procedure and cut tangential to the pial surface. Complete neurons from layers III and IV were drawn with the aid of a camera lucida, and the orientations of the dendritic fields were analyzed using Sholl diagrams. In normal cats, the distributions of the orientations of dendritic fields were uniform, whereas in stripe‐reared cats, the distributions for the layer III pyramidal cells were shifted. The direction of this shift varied with the experience of the cat: In cats reared viewing only vertical lines, the dendritic fields were oriented orthogonal to the representation of the vertical meridian, and in cats reared viewing only horizontal lines, the fields were oriented parallel to the representation of the vertical meridian. In contrast, the distribution of dendritic orientations for the stellate cells was not affected by stripe‐rearing. These results demonstrate a morphological effect of early visual experience that is specific to the particular stimulus presented during rearing and suggest that (1) cortical cells differ in the degree to which they can be modified by such experience, and (2) the dendritic morphology of cortical neurons is related to their preferred orientations.

[1]  J. O'leary,et al.  Structure of the area striata of the cat , 1941 .

[2]  S. A. Talbot,et al.  Physiological Studies on Neural Mechanisms of Visual Localization and Discrimination , 1941 .

[3]  Gray Eg.  Axo-somatic and axo-dendritic synapses of the cerebral cortex: An electron microscope study , 1959 .

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

[5]  A. Scheibel,et al.  Some Structural and Functional Substrates of Development in Young Cats , 1964 .

[6]  M. Colonnier.  The Structural Design of the Neocortex , 1965 .

[7]  G. S. Watson,et al.  Statistical methods for the analysis of problems in animal orientation and certain biological rhythms , 1966 .

[8]  A. Scheibel,et al.  The effect of visual deprivation on cortical neurons: a Golgi study. , 1967, Experimental neurology.

[9]  M. Colonnier.  Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study. , 1968, Brain research.

[10]  A. Ruiz-Marcos,et al.  Dynamic architecture of the visual cortex. , 1970, Brain research.

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

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

[13]  L. Garey.  A light and electron microscopic study of the visual cortex of the cat and monkey , 1971, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[14]  F. Volkmar,et al.  Rearing Complexity Affects Branching of Dendrites in the Visual Cortex of the Rat , 1972, Science.

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

[16]  S. Levay,et al.  Synaptic patterns in the visual cortex of the cat and monkey. Electron microscopy of Golgi Preparations , 1973, The Journal of comparative neurology.

[17]  P. O. Bishop,et al.  Orientation, axis and direction as stimulus parameters for striate cells. , 1974, Vision research.

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

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

[20]  P. Schiller,et al.  Quantitative studies of single-cell properties in monkey striate cortex. V. Multivariate statistical analyses and models. , 1976, Journal of neurophysiology.

[21]  B. V. Updyke,et al.  Chemical stabilization of Golgi silver chromate impregnations. , 1977, Stain technology.

[22]  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.

[23]  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.

[24]  R. Lund.  Development and plasticity of the brain , 1978 .

[25]  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.

[26]  L. Palmer,et al.  The retinotopic organization of area 17 (striate cortex) in the cat , 1978, The Journal of comparative neurology.

[27]  M. Berry,et al.  The effects of dark rearing on the development of the visual cortex of the rat , 1978, The Journal of comparative neurology.

[28]  B. Gordon,et al.  Alteration of cortical orientation selectivity: importance of asymmetric input. , 1979, Science.

[29]  A. Peters.  Thalamic input to the cerebral cortex , 1979, Trends in Neurosciences.

[30]  P. Coleman,et al.  Demonstration of orientation columns with [14C]2-deoxyglucose in a cat reared in a striped environment , 1979, Brain Research.

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

[32]  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.

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

[34]  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.

[35]  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.

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

[37]  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.