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Active probing to highlight approaching transitions to ictal states in coupled neural mass models

The extraction of electrophysiological features that reliably forecast the occurrence of seizures is one of the most challenging goals in epilepsy research. Among possible approaches to tackle this problem is the use of active probing paradigms in which responses to stimuli are used to detect underl...

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Autores principales: Carvalho, Vinícius Rezende, Moraes, Márcio Flávio Dutra, Cash, Sydney S., Mendes, Eduardo Mazoni Andrade Marçal
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7861539/
https://www.ncbi.nlm.nih.gov/pubmed/33493165
http://dx.doi.org/10.1371/journal.pcbi.1008377
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author Carvalho, Vinícius Rezende
Moraes, Márcio Flávio Dutra
Cash, Sydney S.
Mendes, Eduardo Mazoni Andrade Marçal
author_facet Carvalho, Vinícius Rezende
Moraes, Márcio Flávio Dutra
Cash, Sydney S.
Mendes, Eduardo Mazoni Andrade Marçal
author_sort Carvalho, Vinícius Rezende
collection PubMed
description The extraction of electrophysiological features that reliably forecast the occurrence of seizures is one of the most challenging goals in epilepsy research. Among possible approaches to tackle this problem is the use of active probing paradigms in which responses to stimuli are used to detect underlying system changes leading up to seizures. This work evaluates the theoretical and mechanistic underpinnings of this strategy using two coupled populations of the well-studied Wendling neural mass model. Different model settings are evaluated, shifting parameters (excitability, slow inhibition, or inter-population coupling gains) from normal towards ictal states while probing stimuli are applied every 2 seconds to the input of either one or both populations. The correlation between the extracted features and the ictogenic parameter shifting indicates if the impending transition to the ictal state may be identified in advance. Results show that not only can the response to the probing stimuli forecast seizures but this is true regardless of the altered ictogenic parameter. That is, similar feature changes are highlighted by probing stimuli responses in advance of the seizure including: increased response variance and lag-1 autocorrelation, decreased skewness, and increased mutual information between the outputs of both model subsets. These changes were mostly restricted to the stimulated population, showing a local effect of this perturbational approach. The transition latencies from normal activity to sustained discharges of spikes were not affected, suggesting that stimuli had no pro-ictal effects. However, stimuli were found to elicit interictal-like spikes just before the transition to the ictal state. Furthermore, the observed feature changes highlighted by probing the neuronal populations may reflect the phenomenon of critical slowing down, where increased recovery times from perturbations may signal the loss of a systems’ resilience and are common hallmarks of an impending critical transition. These results provide more evidence that active probing approaches highlight information about underlying system changes involved in ictogenesis and may be able to play a role in assisting seizure forecasting methods which can be incorporated into early-warning systems that ultimately enable closing the loop for targeted seizure-controlling interventions.
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spelling pubmed-78615392021-02-12 Active probing to highlight approaching transitions to ictal states in coupled neural mass models Carvalho, Vinícius Rezende Moraes, Márcio Flávio Dutra Cash, Sydney S. Mendes, Eduardo Mazoni Andrade Marçal PLoS Comput Biol Research Article The extraction of electrophysiological features that reliably forecast the occurrence of seizures is one of the most challenging goals in epilepsy research. Among possible approaches to tackle this problem is the use of active probing paradigms in which responses to stimuli are used to detect underlying system changes leading up to seizures. This work evaluates the theoretical and mechanistic underpinnings of this strategy using two coupled populations of the well-studied Wendling neural mass model. Different model settings are evaluated, shifting parameters (excitability, slow inhibition, or inter-population coupling gains) from normal towards ictal states while probing stimuli are applied every 2 seconds to the input of either one or both populations. The correlation between the extracted features and the ictogenic parameter shifting indicates if the impending transition to the ictal state may be identified in advance. Results show that not only can the response to the probing stimuli forecast seizures but this is true regardless of the altered ictogenic parameter. That is, similar feature changes are highlighted by probing stimuli responses in advance of the seizure including: increased response variance and lag-1 autocorrelation, decreased skewness, and increased mutual information between the outputs of both model subsets. These changes were mostly restricted to the stimulated population, showing a local effect of this perturbational approach. The transition latencies from normal activity to sustained discharges of spikes were not affected, suggesting that stimuli had no pro-ictal effects. However, stimuli were found to elicit interictal-like spikes just before the transition to the ictal state. Furthermore, the observed feature changes highlighted by probing the neuronal populations may reflect the phenomenon of critical slowing down, where increased recovery times from perturbations may signal the loss of a systems’ resilience and are common hallmarks of an impending critical transition. These results provide more evidence that active probing approaches highlight information about underlying system changes involved in ictogenesis and may be able to play a role in assisting seizure forecasting methods which can be incorporated into early-warning systems that ultimately enable closing the loop for targeted seizure-controlling interventions. Public Library of Science 2021-01-25 /pmc/articles/PMC7861539/ /pubmed/33493165 http://dx.doi.org/10.1371/journal.pcbi.1008377 Text en © 2021 Carvalho 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
Carvalho, Vinícius Rezende
Moraes, Márcio Flávio Dutra
Cash, Sydney S.
Mendes, Eduardo Mazoni Andrade Marçal
Active probing to highlight approaching transitions to ictal states in coupled neural mass models
title Active probing to highlight approaching transitions to ictal states in coupled neural mass models
title_full Active probing to highlight approaching transitions to ictal states in coupled neural mass models
title_fullStr Active probing to highlight approaching transitions to ictal states in coupled neural mass models
title_full_unstemmed Active probing to highlight approaching transitions to ictal states in coupled neural mass models
title_short Active probing to highlight approaching transitions to ictal states in coupled neural mass models
title_sort active probing to highlight approaching transitions to ictal states in coupled neural mass models
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7861539/
https://www.ncbi.nlm.nih.gov/pubmed/33493165
http://dx.doi.org/10.1371/journal.pcbi.1008377
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