Binocular Disparity Selectivity Weakened after Monocular Deprivation in Mouse V1.

ABSTRACT

Experiences during the critical period sculpt the circuitry within the neocortex, leading to changes in the functional responses of sensory neurons. Monocular deprivation (MD) during the visual critical period causes shifts in ocular preference, or dominance, toward the open eye in primary visual cortex (V1) and disrupts the normal development of acuity. In carnivores and primates, MD also disrupts the emergence of binocular disparity selectivity, a cue resulting from integrating ocular inputs. This disruption may be a result of the increase in neurons driven exclusively by the open eye that follows deprivation or a result of a mismatch in the convergence of ocular inputs. To distinguish between these possibilities, we measured the ocular dominance (OD) and disparity selectivity of neurons from male and female mouse V1 following MD. Normal mouse V1 neurons are dominated by contralateral eye input and contralateral eye deprivation shifts mouse V1 neurons toward more balanced responses between the eyes. This shift toward binocularity, as assayed by OD, decreased disparity sensitivity. MD did not alter the initial maturation of binocularity, as disparity selectivity before the MD was indistinguishable from normal mature animals. Decreased disparity tuning was most pronounced in binocular and ipsilaterally biased neurons, which are the populations that have undergone the largest shifts in OD. In concert with the decline in disparity selectivity, we observed a shift toward lower spatial frequency selectivity for the ipsilateral eye following MD. These results suggest an emergence of novel synaptic inputs during MD that disrupt the representation of disparity selectivity.SIGNIFICANCE STATEMENT We demonstrate that monocular deprivation during the developmental critical period impairs binocular integration in mouse primary visual cortex. This impairment occurs despite an increase in the degree to which neurons become more binocular. We further demonstrate that our deprivation did not impair the maturation of disparity selectivity. Disparity selectivity has already reached a matured level before the monocular deprivation. The loss of disparity tuning is primarily observed in neurons dominated by the open eye, suggesting a link between altered inputs and loss of disparity sensitivity. These results suggest that new inputs following deprivation may not maintain the precise spatial relationship between the two eye inputs required for disparity selectivity.