Experience dependence of alpha rhythms and neural dynamics in mouse visual cortex

The role of experience in the development and maintenance of emergent network properties such as cortical oscillations and states is poorly understood. To define how early-life experience affects cortical dynamics in the visual cortex of adult, head-fixed mice, we examined the effects of two forms of blindness initiated before eye-opening and continuing through recording in adulthood: (1) bilateral loss of retinal input (enucleation) and (2) degradation of visual input (eyelid-suture). Neither form of deprivation fundamentally altered the state-dependent regulation of firing-rates or local field potentials. However, each form of deprivation did cause a unique set of changes in network behavior. Laminar analysis revealed two different generative mechanisms for low-frequency synchronization, one prevalent during movement, the other during quiet-wakefulness. The former was absent in enucleated mice, suggesting a mouse homolog of human alpha oscillations. In addition, neurons in enucleated animals were less correlated and fired more regularly, but showed no change in mean firing-rate. Chronic lid-suture decreased firing rates during quiet-wakefulness, but not during movement, with no effect on neural correlations or regularity. Sutured animals showed a broadband increase in dEEG power and an increased occurrence, but reduced central frequency, of narrowband gamma oscillations. The complementary--rather than additive--effects of lid-suture and enucleation suggest that the development of these emergent network properties does not require vision but is plastic to modified input. Our results suggest a complex interaction of internal set-points and experience determines the expression of mature cortical activity, with low-frequency synchronization being particularly susceptible to early deprivation. Significance statement The developmental rules that guide how cortex balances internal homeostatic set points with external inputs to establish the emergent network level dynamics critical to its function are unclear. Using multiple methods of early deprivation, we show that the development of dynamics in mouse visual cortex is not dependent on the type of input. Rather, specific neural rhythms, firing-rate set points, and neural correlations are differentially modified by experience. Our deprivations identify one specific rhythm as a likely homolog to human alpha and suggest a mechanism for its loss in blindness. Our results advance our understanding of the regulatory mechanism leading to normal cortical processing, which is altered in blindness and multiple neural disorders.