Neuronal avalanches differ from wakefulness to deep sleep--evidence from intracranial depth recordings in humans

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...

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Bibliographic Details
Published in:PLoS computational biology 2013-03, Vol.9 (3), p.e1002985-e1002985
Main Authors: Priesemann, Viola, Valderrama, Mario, Wibral, Michael, Le Van Quyen, Michel
Format: Article
Language:English
Subjects:
Adult
Avalanches
Biology
Brain
Brain - physiology
Computational Biology
Electrodes, Implanted
Electroencephalography - methods
Female
Humans
Male
Middle Aged
Models, Neurological
Neural circuitry
Neural networks
Neurons - physiology
Neurophysiology
Physics
Physiological aspects
Sleep
Sleep Stages - physiology
Sleep-wake cycle
Wakefulness - physiology
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Summary: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.
ISSN:1553-7358
1553-734X
1553-7358
DOI:10.1371/journal.pcbi.1002985