Original Research ARTICLE

Front. Syst. Neurosci., 24 June 2014 | doi: 10.3389/fnsys.2014.00108

Spike avalanches in vivo suggest a driven, slightly subcritical brain state

  • 1Department of Non-linear Dynamics, Max Planck Institute for Dynamics and Self-Organization, Göttingen, Germany
  • 2Bernstein Center for Computational Neuroscience, Göttingen, Germany
  • 3Frankfurt Institute for Advanced Studies, Frankfurt, Germany
  • 4Department of Neurophysiology, Max Planck Institute for Brain Research, Frankfurt, Germany
  • 5Magnetoencephalography Unit, Brain Imaging Center, Johann Wolfgang Goethe University, Frankfurt, Germany
  • 6Ernst Strüngmann Institute for Neuroscience in Cooperation with Max Planck Society, Frankfurt, Germany
  • 7Department of Biomedical Engineering, University of Los Andes, Bogotá, Colombia
  • 8Neural Information Processing Group, Department of Software Engineering and Theoretical Computer Science, TU Berlin, Berlin, Germany
  • 9Bernstein Center for Computational Neuroscience, Berlin, Germany
  • 10Centre de Recherche de l’Institut du Cerveau et de la Moelle épinière, Hôpital de la Pitié-Salpêtrière, INSERM UMRS 975—CNRS UMR 7225-UPMC, Paris, France
  • 11Department of Psychology, Faculty of Humanities and Social Sciences, University of Zagreb, Zagreb, Croatia
  • 12Physiology of Cognitive Processes, Max Planck Institute for Biological Cybernetics, Tübingen, Germany

In self-organized critical (SOC) systems avalanche size distributions follow power-laws. Power-laws have also been observed for neural activity, and so it has been proposed that SOC underlies brain organization as well. Surprisingly, for spiking activity in vivo, evidence for SOC is still lacking. Therefore, we analyzed highly parallel spike recordings from awake rats and monkeys, anaesthetized cats, and also local field potentials from humans. We compared these to spiking activity from two established critical models: the Bak-Tang-Wiesenfeld model, and a stochastic branching model. We found fundamental differences between the neural and the model activity. These differences could be overcome for both models through a combination of three modifications: (1) subsampling, (2) increasing the input to the model (this way eliminating the separation of time scales, which is fundamental to SOC and its avalanche definition), and (3) making the model slightly sub-critical. The match between the neural activity and the modified models held not only for the classical avalanche size distributions and estimated branching parameters, but also for two novel measures (mean avalanche size, and frequency of single spikes), and for the dependence of all these measures on the temporal bin size. Our results suggest that neural activity in vivo shows a mélange of avalanches, and not temporally separated ones, and that their global activity propagation can be approximated by the principle that one spike on average triggers a little less than one spike in the next step. This implies that neural activity does not reflect a SOC state but a slightly sub-critical regime without a separation of time scales. Potential advantages of this regime may be faster information processing, and a safety margin from super-criticality, which has been linked to epilepsy.

Keywords: self-organized criticality, human intracranial recordings, spike train analysis, highly parallel recordings, spiking neural networks, multiunit activity, cortex, monkeys

Citation: Priesemann V, Wibral M, Valderrama M, Pröpper R, Le Van Quyen M, Geisel T, Triesch J, Nikolić D and Munk MHJ (2014) Spike avalanches in vivo suggest a driven, slightly subcritical brain state. Front. Syst. Neurosci. 8:108. doi: 10.3389/fnsys.2014.00108

Received: 08 February 2014; Accepted: 21 May 2014;
Published online: 24 June 2014.

Edited by:

Valentina Pasquale, Fondazione Istituto Italiano di Tecnologia, Italy

Reviewed by:

John M. Beggs, Indiana University, USA
Mauro Copelli, Federal University of Pernambuco, Brazil
Silvia Scarpetta, University of Salerno, Italy
Miguel Angel Muñoz, Universidad de Granada, Spain

Copyright © 2014 Priesemann, Wibral, Valderrama, Pröpper, Le Van Quyen, Geisel, Triesch, Nikolić and Munk. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Viola Priesemann, Max Planck Institute for Dynamics and Self-Organization, Am Fassberg 17, 37077 Göttingen, Germany e-mail: v.priesemann@gmx.de

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