Effects of dark‐rearing on the development of area 18 of the cat's visual cortex.

1. We recorded extracellularly from 420 single units in area 18 in visually inexperienced kittens aged 7 days and dark‐reared kittens aged between 3 and 12 weeks and from 60 single units in area 17 in dark‐reared kittens aged 5 and 11 weeks. 2. Visual deprivation generally depressed the maturation of area 18, although some features were affected more than others and certain developmental improvements still occurred. The percentage of visually responsive units in area 18 increased from 40% in 7‐day‐old kittens to about 75% in dark‐reared animals 10‐12 weeks. At each age a proportion of cells was orientation biased (between 15 and 45%) and these neurones appeared to be arranged in a crude columnar fashion. However, dark‐rearing, from birth, prevented the development of a significant proportion of orientation‐selective cells in area 18; no more than 5% of neurones were orientation‐selective at any age. We found no major bias in the over‐all distribution of preferred orientations of cells in area 18 in dark‐reared kittens. 3. Simple cells, which are found in area 18 even in very young, visually inexperienced kittens, persisted after dark‐rearing, although most retained immature properties. Relatively few complex cells were found in area 18 in visually deprived animals. 4. The majority of neurones in area 18 of dark‐reared kittens were binocularly driven, many equally well by either eye; evidence for regional variation in ocular dominance (indicative of a columnar pattern) was found in these deprived animals. 5. A laminar analysis in area 18 showed that percentages of non‐oriented and orientation‐biased cells changed little, if at all, in lower laminae (IV, V, and VI) but increased substantially in upper layers (above layer IV) in the absence of visual stimulation, over the first 12 post‐natal weeks. 6. A comparison of the effects of dark‐rearing on areas 17 and 18 indicates that the normal development of visual responsiveness and specific receptive field properties is suppressed in both areas during the first 12 post‐natal weeks. It is possible that area 17 has a greater degree of orientation selectivity than area 18 in young visually deprived kittens and this may reflect a difference in the type of afferent inputs.

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

[2]  N. V. Swindale,et al.  Absence of ocular dominance patches in dark-reared cats , 1981, Nature.

[3]  C. Blakemore,et al.  Organization of the visual pathways in the newborn kitten , 1986, Neuroscience Research.

[4]  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.

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

[6]  Jonathan Stone,et al.  Parallel Processing in the Visual System , 1983, Perspectives in Vision Research.

[7]  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.

[8]  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.

[9]  C. Gilbert,et al.  Laminar patterns of geniculocortical projection in the cat , 1976, Brain Research.

[10]  T. Powell,et al.  An experimental study of the termination of the lateral geniculo–cortical pathway in the cat and monkey , 1971, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[11]  B. Cragg,et al.  Development of the extrinsic connections of the visual cortex in the cat , 1974, The Journal of comparative neurology.

[12]  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.

[13]  L. Palmer,et al.  Retinotopic organization of areas 18 and 19 in the cat , 1979, The Journal of comparative neurology.

[14]  C. Blakemore,et al.  The organization and post‐natal development of area 18 of the cat's visual cortex. , 1987, The Journal of physiology.

[15]  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.

[16]  P. D. Spear,et al.  Striate cortex neurons of binocularly deprived kittens respond to visual stimuli through the closed eyelids , 1978, Brain Research.

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

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

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

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

[21]  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.