Non-equilibrium critical dynamics of bursts in θ and δ rhythms as fundamental characteristic of sleep and wake micro-architecture

Abstract

Origin and functions of intermittent transitions among sleep stages, including short awakenings and arousals, constitute a challenge to the current homeostatic framework for sleep regulation, focusing on factors modulating sleep over large time scales. Here we propose that the complex micro-architecture characterizing the sleep-wake cycle results from an underlying non-equilibrium critical dynamics, bridging collective behaviors across spatio-temporal scales. We investigate θ and δ wave dynamics in control rats and in rats with lesions of sleep-promoting neurons in the parafacial zone. We demonstrate that intermittent bursts in θ and δ rhythms exhibit a complex temporal organization, with long-range power-law correlations and a robust duality of power law (θ-bursts, active phase) and exponential-like (δ-bursts, quiescent phase) duration distributions, typical features of non-equilibrium systems self-organizing at criticality. Crucially, such temporal organization relates to anti-correlated coupling between θ- and δ-bursts, and is independent of the dominant physiologic state and lesions, a solid indication of a basic principle in sleep dynamics. Sleep exhibits intermittent transitions among sleep stages and short awakenings, with continuous fluctuations within stages that trigger micro-states and brief arousals. Despite the established association between dominant brain rhythms and physiologic states, the nature and dynamics of sleep-wake and sleep-stage transitions remain not understood. Homeostatic models of sleep regulation at ultradian and circadian scales do not address empirical observations of spontaneous transitions in sleep micro-architecture, and do not account for the emergent complex structure of sleep stages and arousals, and the related dynamics of bursts in cortical rhythms. Empirical observations of intrinsic bursts in cortical activity, and corresponding intermittent transitions in sleep micro-architecture, raise the hypothesis that non-equilibrium critical dynamics underlie sleep regulation at short time scales. We analyze θ and δ cortical rhythms in control rats and rats with lesions in the parafacial zone, which plays a significant role in the regulation of slow-wave sleep. The results demonstrate that critical dynamics underlie cortical activation during sleep and wake, and lay the foundation for a new paradigm, considering sleep micro-architecture as result of a non-equilibrium process and self-organization among neuronal assemblies to maintain a critical state, in contrast to the homeostasis paradigm of sleep regulation at large time scales.