Strabismus disrupts binocular synaptic integration in primary visual cortex

Abstract

Visual disruption early in development dramatically changes how primary visual cortex neurons integrate binocular inputs. The disruption is paradigmatic for investigating the synaptic basis of long-term changes in cortical function, because the primary visual cortex is the site of binocular convergence. The underlying alterations in circuitry by visual disruption remain poorly understood. Here we compare membrane potential responses, observed via whole-cell recordings in vivo, of primary visual cortex neurons in normal adult cats with those of cats in which strabismus was induced before the developmental critical period. In strabismic cats, we observed a dramatic shift in the ocular dominance distribution of simple cells, the first stage of visual cortical processing, toward responding to one eye instead of both, but not in complex cells, which receive inputs from simple cells. Both simple and complex cells no longer conveyed the binocular information needed for depth perception based on binocular cues. There was concomitant binocular suppression such that responses were weaker with binocular than with monocular stimulation. Our estimates of the excitatory and inhibitory input to single neurons indicate binocular suppression that was not evident in synaptic excitation, but arose de novo because of synaptic inhibition. Further constraints on circuit models of plasticity result from indications that the ratio of excitation to inhibition evoked by monocular stimulation decreased mainly for nonpreferred eye stimulation. Althoughwedocumented changes in synaptic input throughout primary visual cortex, a circuit model with plasticity at only thalamocortical synapses is sufficient to account for our observations. © 2013 the authors.