Spontaneous cortical activity is transiently poised close to criticality

PLoS Comput Biol. 2017 May 24;13(5):e1005543. doi: 10.1371/journal.pcbi.1005543. eCollection 2017 May.


Brain activity displays a large repertoire of dynamics across the sleep-wake cycle and even during anesthesia. It was suggested that criticality could serve as a unifying principle underlying the diversity of dynamics. This view has been supported by the observation of spontaneous bursts of cortical activity with scale-invariant sizes and durations, known as neuronal avalanches, in recordings of mesoscopic cortical signals. However, the existence of neuronal avalanches in spiking activity has been equivocal with studies reporting both its presence and absence. Here, we show that signs of criticality in spiking activity can change between synchronized and desynchronized cortical states. We analyzed the spontaneous activity in the primary visual cortex of the anesthetized cat and the awake monkey, and found that neuronal avalanches and thermodynamic indicators of criticality strongly depend on collective synchrony among neurons, LFP fluctuations, and behavioral state. We found that synchronized states are associated to criticality, large dynamical repertoire and prolonged epochs of eye closure, while desynchronized states are associated to sub-criticality, reduced dynamical repertoire, and eyes open conditions. Our results show that criticality in cortical dynamics is not stationary, but fluctuates during anesthesia and between different vigilance states.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / physiology*
  • Animals
  • Cats
  • Cerebral Cortex / physiology*
  • Computational Biology
  • Haplorhini
  • Models, Neurological*
  • Neurons / physiology
  • Wakefulness / physiology*

Grants and funding

GH, CM and YF were supported by the CNRS, the Agence Nationale de la Recherche (ANR: V1-Complex) https://www.cnrs.fr. GH and GB were financed by the initial training network program FACETS-ITN (PITN-GA-2009- 237955) http://facets.kip.uni-heidelberg.de/ITN/. APA was supported by SEMAINE ERA-Net NEURON Project and by a Juan de la Cierva fellowship (IJCI-2014-21066) from the Spanish Ministry of Economy and Competitiveness. CM, GD and YF received funding from the EC grants BrainScales (FP7-2010- IST-FETPI 269921) and the flagship Human Brain Project (n.604102) https://www.humanbrainproject.eu/. The Utah array recordings were made possible through a loan by S.Grün (Research Center Jülich, INM6, Germany) and were part of a collaborative work with S. Grün and A. Riehle (INT, Marseille). AK received funding from the German Federal Ministry of Education and Research (BMBF 01GQ0420 to BCCN Freiburg and 01GQ0830 to BFNT Freiburg/Tübingen) https://www.bmbf.de/en/. GD is supported by the ERC Advanced Grant: DYSTRUCTURE (n. 295129), by the Spanish Research Project PSI2016-75688-P and by the the European Union’s Horizon 2020 research and innovation programme under grant agreement n. 720270 (HBP SGA1). GD obtained support from the ERC Advanced Grant DYSTRUCTURE (n. 295129) gustavodecolab.com/dystructure/ and the Spanish Research Project PSI2013-42091- P. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.