Recovery from monocular deprivation in the monkey. I. Reversal of physiological effects in the visual cortex

Abstract

This is a study of the effects of monocular deprivation, reverse suturing (opening the deprived eye with closure of the other) and reopening of the deprived eye alone (without closing the other) on the physiological organization of the primary visual cortex in monkeys ( Erythrocebus patas ). All animals were initially monocularly deprived by suture of the lids of the right eye from soon after birth until about 4 weeks of age (24-29 days). In a monocularly deprived animal, recordings were taken from area 17 at 24 days. Already most neurons recorded outside layer IV c were strongly or completely dominated by functional input from the left eye. The non-oriented cells of layer IV c, where the bulk of the afferent input terminates, were also mainly dominated by the left eye. Although segregation of input from the two eyes was not complete, large areas of layer IV c were already monocularly dominated by the left eye. Four animals were reverse-sutured at about 4 weeks and recorded 3, 6, 15 and 126 days later. In each animal the pattern of ocular dominance was fairly similar within and outside layer IV c. Even with only 3 days of forced usage of the initially deprived right eye, about half of all cells recorded had become dominated by it, and the process of ‘recapture’ of cortical cells by the initially deprived eye was apparently complete within 15 days. In layer IV c, the recovery took the form of an expansion of zones dominated by the deprived eye, as if the originally shrunken stripes of afferent termination had become enlarged. Binocularly driven neurons were rare at all stages, in all layers, but when present and orientation-selective, they had similar preferred orientations in the two eyes. Likewise the ‘columnar’ sequences of preferred orientation continued without obvious disruption on shifting from regions dominated by one eye to those dominated by the other. Simply reopening the deprived eye at about 4 weeks, for 15 or 96 days caused no detectable change in the overall ocular dominance of cortical cells and, on average, no expansion of right-eye dominance columns in layer IV c. Therefore the recovery seen after reverse suturing depends not just on the restoration of normal activity to axons carrying information from the right eye, but on the establishment of a competitive advantage, through the right eye being made more active than the left.