Consequences of blindness for neural dynamics in mouse visual cortex

Abstract

ABSTRACTEarly-life blindness causes lasting visual impairment, for which the circuit basis is only partially understood. Degradation of visual connections as well as the network dynamics supporting neural oscillations and arousal states are likely contributors. To define how blindness affects dynamics, we examined the effects of two forms of blindness, bilateral loss of retinal input (enucleation) and degradation of visual input (eyelid-suture), on emergent network properties and their state-dependence in the visual cortex of awake head-fixed mice. Neither form of early visual deprivation fundamentally altered the state-dependent regulation of firing-rates or local field potential oscillations. However, each form of deprivation did cause a unique set of changes in network behavior. Enucleation caused a loss of low-frequency synchronization specifically during movement, suggesting a mouse model for human alpha oscillations. Neurons were also less correlated and fired more regularly, with no change in mean firing rates. Chronic lid-suture decreased firing rates during quiet-wakefulness, but not during movement, and had no effect on neural correlations or firing regularity. Sutured animals also had a broadband increase in LFP power and increased occurrence, but reduced central frequency, of narrowband gamma oscillations. The complementary, rather than additive, effects of lid-suture vs.enucleation suggest that the development of these emergent network properties does not require vision but is plastic to modified input. Our results suggest that the etiology of human blindness will be a crucial determinant of circuit pathology and its capacity to respond to clinical interventions.SIGNIFICANCE STATEMENTEarly life blindness alters brain circuits in a way that prevents a full return to normal vision even when sight is restored. We examined the circuit changes caused by two forms of blindness in the mouse as reflected in the spontaneous behavior (network dynamics) of the visual cortex. We found that, as in humans, vision is largely unnecessary for the establishment of cortical network dynamics and their modulation by cortical states like arousal. However, blindness did induce several important changes, such as loss of alpha rhythms. There was no overlap in the changes caused by each deprivation, suggesting that etiology matters. Understanding the lasting consequences of early blindness on neural function is essential for treatment of devastating early visual disorders.