Premature vision drives aberrant development of response properties in primary visual cortex

Development of the mammalian visual system is thought to proceed in two stages. In the first stage, before birth in primates and before eye opening in altricial mammals, spontaneous activity generated by the retina and cortex shapes visual brain circuits in an activity-dependent but experience-independent manner. In the second stage, visual activity generated by sensory experience refines receptive fields. Here, we investigated the consequences of altering this sequence of events by prematurely opening one or both eyes of ferrets and examining visual receptive fields in monocular cortex after the closure of the critical period for ocular dominance plasticity. We observed that many cells in animals with prematurely opened eyes exhibited low-pass temporal frequency tuning and increased temporal frequency bandwidths, and these cells showed slightly increased orientation and direction selectivity index values. Spontaneous activity was greatly elevated in both hemispheres following the premature opening of one or both eyes, suggesting a global change in circuit excitability that was not restricted to cells that viewed the world through the prematurely opened eye. No major changes were noted in spatial frequency tuning. These results suggest that premature visual experience alters circuit excitability and visual receptive fields, in particular with respect to temporal processing. We speculate that closed lids in altricial mammals serve to prevent visual experience until circuits are initially established and are ready to be refined by visual experience.