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

  • 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, anesthetized 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.

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Author:Viola PriesemannORCiDGND, Michael WibralORCiDGND, Mario Valderrama, Robert Pröpper, Michel Le Van Quyen, Theo Geisel, Jochen TrieschORCiD, Danko NikolićORCiDGND, Matthias Hans Joachim MunkORCiDGND
URN:urn:nbn:de:hebis:30:3-515253
DOI:https://doi.org/10.3389/fnsys.2014.00108
ISSN:1662-5137
Pubmed Id:https://pubmed.ncbi.nlm.nih.gov/25009473
Parent Title (English):Frontiers in systems neuroscience
Publisher:Frontiers Research Foundation
Place of publication:Lausanne
Contributor(s):Valentina Pasquale
Document Type:Article
Language:English
Year of Completion:2014
Date of first Publication:2014/06/24
Publishing Institution:Universitätsbibliothek Johann Christian Senckenberg
Release Date:2019/10/23
Tag:cortex; highly parallel recordings; human intracranial recordings; monkeys; multiunit activity; self-organized criticality; spike train analysis; spiking neural networks
Volume:8
Issue:Art. 108
Page Number:17
First Page:1
Last Page:17
Note:
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.
HeBIS-PPN:455356920
Institutes:Physik / Physik
Medizin / Medizin
Wissenschaftliche Zentren und koordinierte Programme / Frankfurt Institute for Advanced Studies (FIAS)
Angeschlossene und kooperierende Institutionen / MPI für Hirnforschung
Dewey Decimal Classification:6 Technik, Medizin, angewandte Wissenschaften / 61 Medizin und Gesundheit / 610 Medizin und Gesundheit
Sammlungen:Universitätspublikationen
Licence (German):License LogoCreative Commons - Namensnennung 3.0