Neuronal Avalanches Differ from Wakefulness to Deep Sleep – Evidence from Intracranial Depth Recordings in Humans

Abstract

Neuronal activity differs between wakefulness and sleep states. In contrast, an attractor state, called self-organized critical (SOC), was proposed to govern brain dynamics because it allows for optimal information coding. But is the human brain SOC for each vigilance state despite the variations in neuronal dynamics? We characterized neuronal avalanches – spatiotemporal waves of enhanced activity - from dense intracranial depth recordings in humans. We showed that avalanche distributions closely follow a power law – the hallmark feature of SOC - for each vigilance state. However, avalanches clearly differ with vigilance states: slow wave sleep (SWS) shows large avalanches, wakefulness intermediate, and rapid eye movement (REM) sleep small ones. Our SOC model, together with the data, suggested first that the differences are mediated by global but tiny changes in synaptic strength, and second, that the changes with vigilance states reflect small deviations from criticality to the subcritical regime, implying that the human brain does not operate at criticality proper but close to SOC. Independent of criticality, the analysis confirms that SWS shows increased correlations between cortical areas, and reveals that REM sleep shows more fragmented cortical dynamics.

Author Summary

Brain activity shows complex dynamics, even in the absence of external stimulation. In fact, most brain activity is generated internally. Therefore, it is crucial to understand the generation principles of internal activity. One hypothesis is that complex brain dynamics emerges from simple local interactions if the network is in a specific state, called “self-organized critical” (SOC). SOC indeed can account for dynamics in slices of brain tissue. However, we lack evidence that human brain dynamics is SOC. In addition, we wondered whether SOC can account for brain activity from wakefulness to deep sleep, despite clear changes in brain dynamics with vigilances states. To answer these questions, we analyzed intracranial depth recordings in humans. We found evidence that the human brain indeed operates close to criticality from wakefulness to deep sleep. However, we found deviations from criticality with vigilance states. These deviations, together with our modelling results, indicated that the human brain is close to SOC, but in a subcritical regime. In the subcritical regime complex dynamics still emerges from purely local interactions, but are more stable than the SOC state. In fact, operation the subcritical regime allows for a safety margin to supercriticality, which was linked to epilepsy.