Quast KB, Reh RK, Caiati MD, Kopell N, McCarthy MM, Hensch TK
Proc Natl Acad Sci U S A. 2023 Jan 10;120(2):e2123182120. doi: 10.1073/pnas.2123182120
Significance
Critical periods are developmental windows of rapid plasticity and remodeling of brain networks, whose trajectories are not yet fully understood. Here, we identify transient γ-oscillations induced by sensory imbalance in the mouse visual cortex as a signature of rapid TC plasticity, only when these windows are open. Using computational modeling, we explain the origin of these transient γ-rhythms and their role in rewiring TC networks to initiate the precritical to critical period transition. These findings offer a robust noninvasive biomarker of open critical period state with which to probe derailed trajectories of brain development.
Abstract
Early-life experience enduringly sculpts thalamocortical (TC) axons and sensory processing. Here, we identify the very first synaptic targets that initiate critical period plasticity, heralded by altered cortical oscillations. Monocular deprivation (MD) acutely induced a transient (<3 h) peak in EEG γ-power (~40 Hz) specifically within the visual cortex, but only when the critical period was open (juvenile mice or adults after dark-rearing, Lynx1-deletion, or diazepam-rescued GAD65-deficiency). Rapid TC input loss onto parvalbumin-expressing (PV) inhibitory interneurons (but not onto nearby pyramidal cells) was observed within hours of MD in a TC slice preserving the visual pathway – again once critical periods opened. Computational TC modeling of the emergent γ-rhythm in response to MD delineated a cortical interneuronal gamma (ING) rhythm in networks of PV-cells bearing gap junctions at the start of the critical period. The ING rhythm effectively dissociated thalamic input from cortical spiking, leading to rapid loss of previously strong TC-to-PV connections through standard spike-timing-dependent plasticity rules. As a consequence, previously silent TC-to-PV connections could strengthen on a slower timescale, capturing the gradually increasing γ-frequency and eventual fade-out over time. Thus, ING enables cortical dynamics to transition from being dominated by the strongest TC input to one that senses the statistics of population TC input after MD. Taken together, our findings reveal the initial synaptic events underlying critical period plasticity and suggest that the fleeting ING accompanying a brief sensory perturbation may serve as a robust readout of TC network state with which to probe developmental trajectories.