Self-regulated critical brain dynamics originate from high frequency-band activity in the MEG.

Brain function requires the flexible coordination of billions of neurons across multiple scales. This could be achieved by scale-free, critical dynamics balanced at the edge of order and disorder. Criticality has been demonstrated in several, often reduced neurophysiological model systems. In the in...

Full description

Bibliographic Details
Main Authors: Stefan Dürschmid, Christoph Reichert, Nike Walter, Hermann Hinrichs, Hans-Jochen Heinze, Frank W Ohl, Giulio Tononi, Matthias Deliano
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2020-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0233589
_version_ 1819199515391950848
author Stefan Dürschmid
Christoph Reichert
Nike Walter
Hermann Hinrichs
Hans-Jochen Heinze
Frank W Ohl
Giulio Tononi
Matthias Deliano
author_facet Stefan Dürschmid
Christoph Reichert
Nike Walter
Hermann Hinrichs
Hans-Jochen Heinze
Frank W Ohl
Giulio Tononi
Matthias Deliano
author_sort Stefan Dürschmid
collection DOAJ
description Brain function requires the flexible coordination of billions of neurons across multiple scales. This could be achieved by scale-free, critical dynamics balanced at the edge of order and disorder. Criticality has been demonstrated in several, often reduced neurophysiological model systems. In the intact human brain criticality has yet been only verified for the resting state. A more direct link between the concept of criticality and oscillatory brain physiology, which is strongly related to cognition, is yet missing. In the present study we therefore carried out a frequency-specific analysis of criticality in the MEG, recorded while subjects were in a defined cognitive state through mindfulness meditation. In a two-step approach we assessed whether the macroscopic neural avalanche dynamics is scale-free by evaluating the goodness of a power-law fits of cascade size and duration distributions of MEG deflections in different frequency bands. In a second step we determined the closeness of the power-law exponents to a critical value of -1.5. Power-law fitting was evaluated by permutation testing, fitting of alternative distributions, and cascade shape analysis. Criticality was verified by defined relationships of exponents of cascade size and duration distributions. Behavioral relevance of criticality was tested by correlation of indices of criticality with individual scores of the Mindful Attention Awareness Scale. We found that relevant scale-free near-critical dynamics originated only from broad-band high-frequency (> 100 Hz) MEG activity, which has been associated with action potential firing, and therefore links criticality on the macroscopic level of MEG to critical spike avalanches on a microscopic level. Whereas a scale-free dynamics was found under mindfulness meditation and rest, avalanche dynamics shifted towards a critical point during meditation by reduction of neural noise. Together with our finding that during mindfulness meditation avalanches show differences in topography relative to rest, our results show that self-regulated attention as required during meditation can serve as a control parameter of criticality in scale-free brain dynamics.
first_indexed 2024-12-23T03:17:34Z
format Article
id doaj.art-a71b2e08e2e147e4a1b04c751a7e8e55
institution Directory Open Access Journal
issn 1932-6203
language English
last_indexed 2024-12-23T03:17:34Z
publishDate 2020-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS ONE
spelling doaj.art-a71b2e08e2e147e4a1b04c751a7e8e552022-12-21T18:02:03ZengPublic Library of Science (PLoS)PLoS ONE1932-62032020-01-01156e023358910.1371/journal.pone.0233589Self-regulated critical brain dynamics originate from high frequency-band activity in the MEG.Stefan DürschmidChristoph ReichertNike WalterHermann HinrichsHans-Jochen HeinzeFrank W OhlGiulio TononiMatthias DelianoBrain function requires the flexible coordination of billions of neurons across multiple scales. This could be achieved by scale-free, critical dynamics balanced at the edge of order and disorder. Criticality has been demonstrated in several, often reduced neurophysiological model systems. In the intact human brain criticality has yet been only verified for the resting state. A more direct link between the concept of criticality and oscillatory brain physiology, which is strongly related to cognition, is yet missing. In the present study we therefore carried out a frequency-specific analysis of criticality in the MEG, recorded while subjects were in a defined cognitive state through mindfulness meditation. In a two-step approach we assessed whether the macroscopic neural avalanche dynamics is scale-free by evaluating the goodness of a power-law fits of cascade size and duration distributions of MEG deflections in different frequency bands. In a second step we determined the closeness of the power-law exponents to a critical value of -1.5. Power-law fitting was evaluated by permutation testing, fitting of alternative distributions, and cascade shape analysis. Criticality was verified by defined relationships of exponents of cascade size and duration distributions. Behavioral relevance of criticality was tested by correlation of indices of criticality with individual scores of the Mindful Attention Awareness Scale. We found that relevant scale-free near-critical dynamics originated only from broad-band high-frequency (> 100 Hz) MEG activity, which has been associated with action potential firing, and therefore links criticality on the macroscopic level of MEG to critical spike avalanches on a microscopic level. Whereas a scale-free dynamics was found under mindfulness meditation and rest, avalanche dynamics shifted towards a critical point during meditation by reduction of neural noise. Together with our finding that during mindfulness meditation avalanches show differences in topography relative to rest, our results show that self-regulated attention as required during meditation can serve as a control parameter of criticality in scale-free brain dynamics.https://doi.org/10.1371/journal.pone.0233589
spellingShingle Stefan Dürschmid
Christoph Reichert
Nike Walter
Hermann Hinrichs
Hans-Jochen Heinze
Frank W Ohl
Giulio Tononi
Matthias Deliano
Self-regulated critical brain dynamics originate from high frequency-band activity in the MEG.
PLoS ONE
title Self-regulated critical brain dynamics originate from high frequency-band activity in the MEG.
title_full Self-regulated critical brain dynamics originate from high frequency-band activity in the MEG.
title_fullStr Self-regulated critical brain dynamics originate from high frequency-band activity in the MEG.
title_full_unstemmed Self-regulated critical brain dynamics originate from high frequency-band activity in the MEG.
title_short Self-regulated critical brain dynamics originate from high frequency-band activity in the MEG.
title_sort self regulated critical brain dynamics originate from high frequency band activity in the meg
url https://doi.org/10.1371/journal.pone.0233589
work_keys_str_mv AT stefandurschmid selfregulatedcriticalbraindynamicsoriginatefromhighfrequencybandactivityinthemeg
AT christophreichert selfregulatedcriticalbraindynamicsoriginatefromhighfrequencybandactivityinthemeg
AT nikewalter selfregulatedcriticalbraindynamicsoriginatefromhighfrequencybandactivityinthemeg
AT hermannhinrichs selfregulatedcriticalbraindynamicsoriginatefromhighfrequencybandactivityinthemeg
AT hansjochenheinze selfregulatedcriticalbraindynamicsoriginatefromhighfrequencybandactivityinthemeg
AT frankwohl selfregulatedcriticalbraindynamicsoriginatefromhighfrequencybandactivityinthemeg
AT giuliotononi selfregulatedcriticalbraindynamicsoriginatefromhighfrequencybandactivityinthemeg
AT matthiasdeliano selfregulatedcriticalbraindynamicsoriginatefromhighfrequencybandactivityinthemeg