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

PLoS Comput Biol. 2013;9(3):e1002985. doi: 10.1371/journal.pcbi.1002985. Epub 2013 Mar 21.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Brain / physiology*
  • Computational Biology
  • Electrodes, Implanted
  • Electroencephalography / methods*
  • Female
  • Humans
  • Male
  • Middle Aged
  • Models, Neurological*
  • Neurons / physiology*
  • Sleep Stages / physiology*
  • Wakefulness / physiology*

Grants and funding

VP received support from the Max Planck Society. VP and MW received support from LOEWE Grant Neuronale Koordination Forschungsschwerpunkt Frankfurt (NeFF). MV and MLVQ received support from the European Union-FP7 Project EPILEPSIAE (Evolving Platform for Improving Living Expectation of Subjects Suffering from IctAl Events, Grant No 211713). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.