Competitive Interactions in Postnatal Development of the Kitten’s Visual System

Abstract

Recent evidence indicates that many consequences of visual deprivation cannot be accounted for simply on the basis of disuse. Rather, accumulating evidence indicates that competition between different inputs may underly many deprivation effects. Monocular deprivation provides a striking example of a competitive interaction during development. If one eye is sutured shut during early life, the developmental consequences for the sutured eye at the level of the lateral geniculate body and visual cortex are much more severe if the other eye is allowed vision than they are if the other eye is also sutured. Two possible mechanisms for this effect have been proposed. According to one view, the principal competitive interactions occur at the lateral geniculate body, and cortical changes are secondary. Alternatively, the primary changes may occur at the cortical level with lateral geniculate alterations a secondary consequence of cortical changes. By rearing kittens with one eye viewing normally, while the other eye views through a cylindrical lens, we have been able to make binocular competition effects depend on the orientation preferences of cortical cells. Since orientation selectivity first occurs at the cortical level, the data indicate that the primary locus of the competition between the two eyes occurs at the orientation-selective cortical cell rather than at the lateral geniculate body.

Competitive interactions may also account for some of the effects of visual deprivation on the cat superior colliculus. In normal cats, single cells in the deeper layers of the colliculus receive auditory and somatosensory inputs, as well as visual afferents. In dark-reared cats, however, visual responses are markedly depressed relative to auditory and tactile responses. These data indicate that inputs from the different sense modalities compete during postnatal development in a fashion analogous to that which occurs with monocular deprivation at the cortical level. Since the visual input is at a competitive disadvantage relative to the auditory and tactile inputs, it loses the ability to influence the multimodal cells of the deep colliculus.

A central concept in postnatal development has been that of the critical period. This term underscores numerous observations which show that competitive interactions during postnatal development occur only during a certain period in the organism’s early development. We have found that the critical period for monocular deprivation can be prolonged, apparently indefinitely by rearing cats in total darkness and then suturing one eyelid shut when the animals are brought into the light. The extent and rapidity of these changes in cortical binocular connectivity in the previously dark-reared animal indicate that the visual system retains residual plasticity in these cats even if dark-rearing is prolonged well beyond the duration of the naturally occurring critical period.