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Time-evolving controllability of effective connectivity networks during seizure progression

Over one third of the estimated 3 million people with epilepsy in the United States are medication resistant. Responsive neurostimulation from chronically implanted electrodes provides a promising treatment alternative to resective surgery. However, determining optimal personalized stimulation param...

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Autores principales: Scheid, Brittany H., Ashourvan, Arian, Stiso, Jennifer, Davis, Kathryn A., Mikhail, Fadi, Pasqualetti, Fabio, Litt, Brian, Bassett, Danielle S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7865160/
https://www.ncbi.nlm.nih.gov/pubmed/33495341
http://dx.doi.org/10.1073/pnas.2006436118
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author Scheid, Brittany H.
Ashourvan, Arian
Stiso, Jennifer
Davis, Kathryn A.
Mikhail, Fadi
Pasqualetti, Fabio
Litt, Brian
Bassett, Danielle S.
author_facet Scheid, Brittany H.
Ashourvan, Arian
Stiso, Jennifer
Davis, Kathryn A.
Mikhail, Fadi
Pasqualetti, Fabio
Litt, Brian
Bassett, Danielle S.
author_sort Scheid, Brittany H.
collection PubMed
description Over one third of the estimated 3 million people with epilepsy in the United States are medication resistant. Responsive neurostimulation from chronically implanted electrodes provides a promising treatment alternative to resective surgery. However, determining optimal personalized stimulation parameters, including when and where to intervene to guarantee a positive patient outcome, is a major open challenge. Network neuroscience and control theory offer useful tools that may guide improvements in parameter selection for control of anomalous neural activity. Here we use a method to characterize dynamic controllability across consecutive effective connectivity (EC) networks based on regularized partial correlations between implanted electrodes during the onset, propagation, and termination regimes of 34 seizures. We estimate regularized partial correlation adjacency matrices from 1-s time windows of intracranial electrocorticography recordings using the Graphical Least Absolute Shrinkage and Selection Operator (GLASSO). Average and modal controllability metrics calculated from each resulting EC network track the time-varying controllability of the brain on an evolving landscape of conditionally dependent network interactions. We show that average controllability increases throughout a seizure and is negatively correlated with modal controllability throughout. Our results support the hypothesis that the energy required to drive the brain to a seizure-free state from an ictal state is smallest during seizure onset, yet we find that applying control energy at electrodes in the seizure onset zone may not always be energetically favorable. Our work suggests that a low-complexity model of time-evolving controllability may offer insights for developing and improving control strategies targeting seizure suppression.
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spelling pubmed-78651602021-02-17 Time-evolving controllability of effective connectivity networks during seizure progression Scheid, Brittany H. Ashourvan, Arian Stiso, Jennifer Davis, Kathryn A. Mikhail, Fadi Pasqualetti, Fabio Litt, Brian Bassett, Danielle S. Proc Natl Acad Sci U S A Biological Sciences Over one third of the estimated 3 million people with epilepsy in the United States are medication resistant. Responsive neurostimulation from chronically implanted electrodes provides a promising treatment alternative to resective surgery. However, determining optimal personalized stimulation parameters, including when and where to intervene to guarantee a positive patient outcome, is a major open challenge. Network neuroscience and control theory offer useful tools that may guide improvements in parameter selection for control of anomalous neural activity. Here we use a method to characterize dynamic controllability across consecutive effective connectivity (EC) networks based on regularized partial correlations between implanted electrodes during the onset, propagation, and termination regimes of 34 seizures. We estimate regularized partial correlation adjacency matrices from 1-s time windows of intracranial electrocorticography recordings using the Graphical Least Absolute Shrinkage and Selection Operator (GLASSO). Average and modal controllability metrics calculated from each resulting EC network track the time-varying controllability of the brain on an evolving landscape of conditionally dependent network interactions. We show that average controllability increases throughout a seizure and is negatively correlated with modal controllability throughout. Our results support the hypothesis that the energy required to drive the brain to a seizure-free state from an ictal state is smallest during seizure onset, yet we find that applying control energy at electrodes in the seizure onset zone may not always be energetically favorable. Our work suggests that a low-complexity model of time-evolving controllability may offer insights for developing and improving control strategies targeting seizure suppression. National Academy of Sciences 2021-02-02 2021-01-25 /pmc/articles/PMC7865160/ /pubmed/33495341 http://dx.doi.org/10.1073/pnas.2006436118 Text en Copyright © 2021 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Scheid, Brittany H.
Ashourvan, Arian
Stiso, Jennifer
Davis, Kathryn A.
Mikhail, Fadi
Pasqualetti, Fabio
Litt, Brian
Bassett, Danielle S.
Time-evolving controllability of effective connectivity networks during seizure progression
title Time-evolving controllability of effective connectivity networks during seizure progression
title_full Time-evolving controllability of effective connectivity networks during seizure progression
title_fullStr Time-evolving controllability of effective connectivity networks during seizure progression
title_full_unstemmed Time-evolving controllability of effective connectivity networks during seizure progression
title_short Time-evolving controllability of effective connectivity networks during seizure progression
title_sort time-evolving controllability of effective connectivity networks during seizure progression
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7865160/
https://www.ncbi.nlm.nih.gov/pubmed/33495341
http://dx.doi.org/10.1073/pnas.2006436118
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