Is the development of orientation selectivity instructed by activity?

Abstract

Is the development of orientation selectivity in visual cortex instructed by the patterns of neural activity of input neurons? We review evidence as to the role of activity, review models of activity-instructed development, and discuss how these models can be tested. The models can explain the normal development of simple cells with binocularly matched orientation preferences, the effects of monocular deprivation and reverse suture on the orientation map, and the development of a full intracortical circuit sufficient to explain mature response properties including the contrast-invariance of orientation tuning. Existing experiments are consistent with the models, in that (a) selective blockade of ON-center ganglion cells, which will degrade or eliminate the information predicted to drive development of orientation selectivity, in fact prevents development of orientation selectivity; and (b) the spontaneous activities of inputs serving the two eyes are correlated in the lateral geniculate nucleus at appropriate developmental times, as was predicted to be required to achieve binocular matching of preferred orientations. However, definitive tests remain to be done to firmly establish the instructive rather than simply permissive role of activity and determine whether the retinotopically and center type-specific patterns of activity predicted by the models actually exist. We conclude by critically examining alternative scenarios for the development of orientation selectivity and maps, including the idea that maps are genetically prespecified.