Restriction of visual experience to a single orientation affects the organization of orientation columns in cat visual cortex. A study with deoxyglucose.

In six dark reared, 4-weak-old kittens visual experience was restricted to contours of a single orientation, horizontal or vertical, using cylindrical lenses. Subsequently, the deoxyglucose method was used to determine whether these artificial raising conditions had affected the development of orientation columns in the visual cortex. After application of the deoxyglucose pulse one hemifield was stimulated with vertical, the other with horizontal contours. Thus, from interhemispheric comparison, changes in columnar systems corresponding to experienced and inexperienced orientations could be determined. The following results were obtained: (1) Irrespective of the restrictions in visual experience, orientation columns develop in areas 17, 18, 19 and in the visual areas of the posterior suprasylvian sulcus. (2) Within area 17, spacing between columns encoding the same orientations is remarkably regular (1 mm), is not influenced by selective experience and shows only slight interindividual variation. (3) In non-striate areas the spacing of columns is less regular and the spatial frequency of the periodicity is lower. (4) The modifiability of this columnar pattern by selective experience is small within the granular layer of striate cortex but substantial in non-granular layers: Within layer IV columns whose preference corresponds to the experienced orientation are wider and more active than those encoding the orthogonal orientation but the columnar grid remains basically unaltered. Outside layer IV the columnar system is maintained only for columns encoding the experienced orientations. The deprived columns by contrast frequently fail to extend into non-granular layers and remain confined to the vicinity of layer IV. (5) These modifications in the columnar arrangement are more pronounced in striate cortex than in nonstriate visual areas and, within the former, more conspicuous in the central than in the peripheral representation of the visual field. It is concluded that within layer IV the blue print for the system of orientation columns is determined by genetic instructions: first order cells in layer IV develop orientation selectivity irrespective of experience whereby the preference for a particular orientation is predetermined by the position in the columnar grid. Dependent on experience is, however, the expansion of the columnar system from layer IV into non-granular layers. It is argued that all distortions following selective rearing can be accounted for by competitive interactions between intracortical pathways, the mechanisms being identical to those established for competitive processes in the domain of ocular dominance columns. It is proposed that such experience dependent modifiability of connections between first and second order cells is a necessary prerequisite for the development of orientation selectivity in cells with large and complex receptive fields.