Slow waves form expanding, memory-rich mesostates steered by local excitability in
fading anesthesia

Summary

Antonio Pazienti¹, Andrea Galluzzi¹, Miguel Dasilva^2,¥, Maria V. Sanchez-Vives^2,3, Maurizio Mattia^1,*

In the arousal process from sleep and anesthesia, the brain restores its integrative and complex activity from the synchronized state of slow wave activity (SWA) characteristic of NREM sleep. The mechanisms and dynamics of the cortical network underpinning this state transition remain however to be elucidated. Here we investigated the progressive shaping of SWA propagating through the cortex on the way to wakefulness. Using micro-electrocorticographical recordings in the mouse, we pharmacologically increased levels of slow-wave frequency and complexity from deep unconsciousness toward wakefulness, and probed several single neuronal assemblies throughout the whole cortex. We found a form of memory in the SWA at deep anesthesia, with a tight alternation of posterior-anterior-posterior modes of slow-wave propagation. When approaching wakefulness, metastable patterns of spiking cortical activity propagated in many more directions, reflecting an increased complexity in the network dynamics. We unveil a temporal component of the dynamics of the waves’ mesostates, predicted by simulations of a model network of spiking neurons and confirmed in our experimental data. Local excitability suffices to explain the transition from sleep to wakefulness without requiring modifications of the network connectivity. These results shed new light on the functional re-organization of the cortical network in the awakening brain.