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.
Highlights
Distinct patterns of neuronal dynamics are observed across vigilance states as the brain transitions from wakefulness to sleep [1]
Does the brain always operate in the self-organized critical (SOC) state, despite wide variations in the neuronal dynamics across vigilance states, or does the brain – in the framework of critical dynamics – undergo a state transition away from the critical to subcritical or supercritical states [5,6,7,8,9]? The critical state may be optimal for information processing and storage; during sleep the brain might not be in a state of optimal processing capacities, since sleep dynamics might be optimized to save energy, to restore tissue, for synaptic homeostasis, for thermoregulation, or for plasticity, learning and memory [10,11,12,13,14]
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)
Summary
Distinct patterns of neuronal dynamics are observed across vigilance states as the brain transitions from wakefulness to sleep [1]. Does the brain always operate in the SOC state, despite wide variations in the neuronal dynamics across vigilance states, or does the brain – in the framework of critical dynamics – undergo a state transition away from the critical to subcritical or supercritical states [5,6,7,8,9]? Evidence for phase transitions has been found in vitro and in silicio [5,6,7,8,9,15,16,17]. We have no evidence yet for phase transitions to sub- or supercriticality in vivo
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