Functional states shape the spatiotemporal representation of local and cortex-wide neural activity in mouse sensory cortex

Abstract

The spatiotemporal representation of neural activity during rest and upon sensory stimulation in cortical areas is highly dynamic, and may be predominantly governed by cortical state. On the mesoscale level, intrinsic neuronal activity ranges from a persistent state, generally associated with a sustained depolarization of neurons, to a bimodal, slow-wave like state with bursts of neuronal activation, alternating with silent periods. These different activity states are prevalent under certain types of sedatives, or are associated with specific behavioral or vigilance conditions. Neurophysiological experiments assessing circuit activity, usually assume a constant underlying state, yet reports of variability of neuronal responses under seemingly constant conditions are common in the field. Even when a certain type of neural activity or cortical state can stably be maintained over time, the associated response properties are highly relevant for explaining experimental outcomes. Here we describe the spatiotemporal characteristics of ongoing activity and sensory evoked responses under two predominant functional states in the sensory cortices of mice: persistent activity (PA) and slow wave activity (SWA). Using electrophysiological recordings, and local and wide-field calcium recordings, we examine whether spontaneous and sensory evoked neuronal activity propagate throughout the cortex in a state dependent manner. We find that PA and SWA differ in their spatiotemporal characteristics which determine the cortical network's response to a sensory stimulus. During PA state, sensory stimulation elicits gamma-based short-latency responses which precisely follow each stimulation pulse and are prone to adaptation upon higher stimulation frequencies. Sensory responses during SWA are more variable, dependent on refractory periods following spontaneous slow waves. While spontaneous slow waves propagated in anterior-posterior direction in a majority of observations, the direction of propagation of stimulus-elicited wave depends on the sensory modality. These findings suggest that cortical state explains variance and should be considered when investigating multi-scale correlates of functional neurocircuit activity.