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. T...

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Main Authors: Viola ePriesemann, Michael eWibral, Mario eValderrama, Robert ePröpper, Michel eLe Van Quyen, Theo eGeisel, Jochen eTriesch, Danko eNikolić, Matthias Hans Joachim Munk
Format: Article
Language:English
Published: Frontiers Media S.A. 2014-06-01
Series:Frontiers in Systems Neuroscience
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fnsys.2014.00108/full
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author Viola ePriesemann
Viola ePriesemann
Viola ePriesemann
Viola ePriesemann
Michael eWibral
Mario eValderrama
Robert ePröpper
Robert ePröpper
Michel eLe Van Quyen
Theo eGeisel
Theo eGeisel
Jochen eTriesch
Danko eNikolić
Danko eNikolić
Danko eNikolić
Danko eNikolić
Matthias Hans Joachim Munk
author_facet Viola ePriesemann
Viola ePriesemann
Viola ePriesemann
Viola ePriesemann
Michael eWibral
Mario eValderrama
Robert ePröpper
Robert ePröpper
Michel eLe Van Quyen
Theo eGeisel
Theo eGeisel
Jochen eTriesch
Danko eNikolić
Danko eNikolić
Danko eNikolić
Danko eNikolić
Matthias Hans Joachim Munk
author_sort Viola ePriesemann
collection DOAJ
description 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.
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spelling doaj.art-6060c2a6614b4ab9aa361a094a2c97992022-12-21T23:01:35ZengFrontiers Media S.A.Frontiers in Systems Neuroscience1662-51372014-06-01810.3389/fnsys.2014.0010877070Spike avalanches in vivo suggest a driven, slightly subcritical brain stateViola ePriesemann0Viola ePriesemann1Viola ePriesemann2Viola ePriesemann3Michael eWibral4Mario eValderrama5Robert ePröpper6Robert ePröpper7Michel eLe Van Quyen8Theo eGeisel9Theo eGeisel10Jochen eTriesch11Danko eNikolić12Danko eNikolić13Danko eNikolić14Danko eNikolić15Matthias Hans Joachim Munk16Max Planck Institute for Dynamics and Self-OrganizationFrankfurt Institute for Advanced StudiesMax Planck Institute for Brain ResearchBernstein Center for Computational Neuroscience GöttingenGoethe UniversityUniversity of Los AndesTU BerlinBernstein Center for Computational Neuroscience BerlinHôpital de la Pitié-SalpêtrièreMax Planck Institute for Dynamics and Self-OrganizationBernstein Center for Computational Neuroscience GöttingenFrankfurt Institute for Advanced StudiesFrankfurt Institute for Advanced StudiesMax Planck Institute for Brain ResearchUniversity of ZagrebErnst Strüngmann Institute (ESI)Max Planck Institute for Biological CyberneticsIn 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.http://journal.frontiersin.org/Journal/10.3389/fnsys.2014.00108/fullCatsHumansPhase TransitionPopulation DynamicsRatslocal field potential
spellingShingle Viola ePriesemann
Viola ePriesemann
Viola ePriesemann
Viola ePriesemann
Michael eWibral
Mario eValderrama
Robert ePröpper
Robert ePröpper
Michel eLe Van Quyen
Theo eGeisel
Theo eGeisel
Jochen eTriesch
Danko eNikolić
Danko eNikolić
Danko eNikolić
Danko eNikolić
Matthias Hans Joachim Munk
Spike avalanches in vivo suggest a driven, slightly subcritical brain state
Frontiers in Systems Neuroscience
Cats
Humans
Phase Transition
Population Dynamics
Rats
local field potential
title Spike avalanches in vivo suggest a driven, slightly subcritical brain state
title_full Spike avalanches in vivo suggest a driven, slightly subcritical brain state
title_fullStr Spike avalanches in vivo suggest a driven, slightly subcritical brain state
title_full_unstemmed Spike avalanches in vivo suggest a driven, slightly subcritical brain state
title_short Spike avalanches in vivo suggest a driven, slightly subcritical brain state
title_sort spike avalanches in vivo suggest a driven slightly subcritical brain state
topic Cats
Humans
Phase Transition
Population Dynamics
Rats
local field potential
url http://journal.frontiersin.org/Journal/10.3389/fnsys.2014.00108/full
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