Fading Signatures of Critical Brain Dynamics during Sustained Wakefulness in Humans

Abstract

Sleep encompasses approximately a third of our lifetime, yet its purpose and biological function are not well understood. Without sleep optimal brain functioning such as responsiveness to stimuli, information processing, or learning may be impaired. Such observations suggest that sleep plays a crucial role in organizing or reorganizing neuronal networks of the brain toward states where information processing is optimized.Increasing evidence suggests that cortical neuronal networks operate near a critical state characterized by balanced activity patterns, which supports optimal information processing. However, it remains unknown whether critical dynamics is affected in the course of wake and sleep, which would also impact information processing. Here, we show that signatures of criticality are progressively disturbed during wake and restored by sleep. We demonstrate that the precise power-laws governing the cascading activity of neuronal avalanches and the distribution of phase-lock intervals in human electroencephalographic recordings are increasingly disarranged during sustained wakefulness. These changes are accompanied by a decrease in variability of synchronization. Interpreted in the context of a critical branching process, these seemingly different findings indicate a decline of balanced activity and progressive distance from criticality toward states characterized by an imbalance toward excitation where larger events prevail dynamics. Conversely, sleep restores the critical state resulting in recovered power-law characteristics in activity and variability of synchronization. These findings support the intriguing hypothesis that sleep may be important to reorganize cortical network dynamics to a critical state thereby assuring optimal computational capabilities for the following time awake.

Intrinsic excitability measures track antiepileptic drug action and uncover increasing/decreasing excitability over the wake/sleep cycle

“…To further investigate the relationship between R and vigilance we therefore extended our analysis to a dataset of eight healthy subjects where vigilance had been rigorously monitored and controlled. There, scalp EEG had been recorded every 3 h over a period of 40 h of sustained wakefulness (14,27). During this period of wakefulness we observed an increase of R that was significantly correlated to the time awake (Fig.…”

“…For example, a relative reduction of inhibition during time awake would similarly lead to an increase in the E/I balance. On a neuronal network level such structural wake-dependent alterations have been discussed to drive networks to states suboptimal for information processing (14). Despite the possibility that increasing synchrony R indicates an increase in excitability during wake, it is also conceivable that mechanisms other than increasing excitability are underlying the observed changes in R. For example, one could speculate that the elevated likelihood of neurons to go "offline" together, as observed in sleep-deprived rats (37), could manifest itself in increased synchronization levels measured from larger-scale data such as EEG.…”

“…A perturbational approach to study excitability in human cortex found increased responses after a period of sustained wakefulness that were rebalanced after sleep (12,13). Such findings suggest that excitability could increase during wake, which might result in suboptimal information processing in cortical networks (14,15) and point to a pivotal role of sleep in rebalancing the level of excitability. However, a continuous measurement of excitability during the wake/sleep cycle supporting this hypothesis is hard to obtain with current measures.…”

“…Recent insights into cortical activity from computational modeling (19,20), experiments in cultures in vitro (21), rodents (22,23), and also human magnetoencephalography and EEG (14,24) have pointed to the ability of global synchronization measures to characterize physiological cortical dynamics. It was shown that phase synchronization of ongoing cortical activity exhibits moderate mean over a broad range of frequency bands under normal conditions.…”

Voltage Imaging of Waking Mouse Cortex Reveals Emergence of Critical Neuronal Dynamics

“…The spatiotemporal extent of a cascade was defined via a thresholding method similar to previous studies of cascade-like neuronal activity in local field potentials (LFPs), EEG, and functional MRI (fMRI; Beggs and Plenz, 2003;Petermann et al, 2009;Tagliazucchi et al, 2012;Meisel et al, 2013). We used the voltage imaging time course at each pixel to identify times at which local activity crossed above a threshold from below (Fig.…”