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Assessing criticality in pre-seizure single-neuron activity of human epileptic cortex

Epileptic seizures are characterized by abnormal and excessive neural activity, where cortical network dynamics seem to become unstable. However, most of the time, during seizure-free periods, cortex of epilepsy patients shows perfectly stable dynamics. This raises the question of how recurring inst...

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Autores principales: Hagemann, Annika, Wilting, Jens, Samimizad, Bita, Mormann, Florian, Priesemann, Viola
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7971851/
https://www.ncbi.nlm.nih.gov/pubmed/33684101
http://dx.doi.org/10.1371/journal.pcbi.1008773
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author Hagemann, Annika
Wilting, Jens
Samimizad, Bita
Mormann, Florian
Priesemann, Viola
author_facet Hagemann, Annika
Wilting, Jens
Samimizad, Bita
Mormann, Florian
Priesemann, Viola
author_sort Hagemann, Annika
collection PubMed
description Epileptic seizures are characterized by abnormal and excessive neural activity, where cortical network dynamics seem to become unstable. However, most of the time, during seizure-free periods, cortex of epilepsy patients shows perfectly stable dynamics. This raises the question of how recurring instability can arise in the light of this stable default state. In this work, we examine two potential scenarios of seizure generation: (i) epileptic cortical areas might generally operate closer to instability, which would make epilepsy patients generally more susceptible to seizures, or (ii) epileptic cortical areas might drift systematically towards instability before seizure onset. We analyzed single-unit spike recordings from both the epileptogenic (focal) and the nonfocal cortical hemispheres of 20 epilepsy patients. We quantified the distance to instability in the framework of criticality, using a novel estimator, which enables an unbiased inference from a small set of recorded neurons. Surprisingly, we found no evidence for either scenario: Neither did focal areas generally operate closer to instability, nor were seizures preceded by a drift towards instability. In fact, our results from both pre-seizure and seizure-free intervals suggest that despite epilepsy, human cortex operates in the stable, slightly subcritical regime, just like cortex of other healthy mammalians.
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spelling pubmed-79718512021-03-31 Assessing criticality in pre-seizure single-neuron activity of human epileptic cortex Hagemann, Annika Wilting, Jens Samimizad, Bita Mormann, Florian Priesemann, Viola PLoS Comput Biol Research Article Epileptic seizures are characterized by abnormal and excessive neural activity, where cortical network dynamics seem to become unstable. However, most of the time, during seizure-free periods, cortex of epilepsy patients shows perfectly stable dynamics. This raises the question of how recurring instability can arise in the light of this stable default state. In this work, we examine two potential scenarios of seizure generation: (i) epileptic cortical areas might generally operate closer to instability, which would make epilepsy patients generally more susceptible to seizures, or (ii) epileptic cortical areas might drift systematically towards instability before seizure onset. We analyzed single-unit spike recordings from both the epileptogenic (focal) and the nonfocal cortical hemispheres of 20 epilepsy patients. We quantified the distance to instability in the framework of criticality, using a novel estimator, which enables an unbiased inference from a small set of recorded neurons. Surprisingly, we found no evidence for either scenario: Neither did focal areas generally operate closer to instability, nor were seizures preceded by a drift towards instability. In fact, our results from both pre-seizure and seizure-free intervals suggest that despite epilepsy, human cortex operates in the stable, slightly subcritical regime, just like cortex of other healthy mammalians. Public Library of Science 2021-03-08 /pmc/articles/PMC7971851/ /pubmed/33684101 http://dx.doi.org/10.1371/journal.pcbi.1008773 Text en © 2021 Hagemann et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Hagemann, Annika
Wilting, Jens
Samimizad, Bita
Mormann, Florian
Priesemann, Viola
Assessing criticality in pre-seizure single-neuron activity of human epileptic cortex
title Assessing criticality in pre-seizure single-neuron activity of human epileptic cortex
title_full Assessing criticality in pre-seizure single-neuron activity of human epileptic cortex
title_fullStr Assessing criticality in pre-seizure single-neuron activity of human epileptic cortex
title_full_unstemmed Assessing criticality in pre-seizure single-neuron activity of human epileptic cortex
title_short Assessing criticality in pre-seizure single-neuron activity of human epileptic cortex
title_sort assessing criticality in pre-seizure single-neuron activity of human epileptic cortex
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7971851/
https://www.ncbi.nlm.nih.gov/pubmed/33684101
http://dx.doi.org/10.1371/journal.pcbi.1008773
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