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Neural diffusivity and pre-emptive epileptic seizure intervention

The propagation of epileptic seizure activity in the brain is a widespread pathophysiology that, in principle, should yield to intervention techniques guided by mathematical models of neuronal ensemble dynamics. During a seizure, neural activity will deviate from its current dynamical regime to one...

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Autores principales: Fagerholm, Erik D., Tangwiriyasakul, Chayanin, Friston, Karl J., Violante, Inês R., Williams, Steven, Carmichael, David W., Perani, Suejen, Turkheimer, Federico E., Moran, Rosalyn J., Leech, Robert, Richardson, Mark P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7732083/
https://www.ncbi.nlm.nih.gov/pubmed/33259483
http://dx.doi.org/10.1371/journal.pcbi.1008448
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author Fagerholm, Erik D.
Tangwiriyasakul, Chayanin
Friston, Karl J.
Violante, Inês R.
Williams, Steven
Carmichael, David W.
Perani, Suejen
Turkheimer, Federico E.
Moran, Rosalyn J.
Leech, Robert
Richardson, Mark P.
author_facet Fagerholm, Erik D.
Tangwiriyasakul, Chayanin
Friston, Karl J.
Violante, Inês R.
Williams, Steven
Carmichael, David W.
Perani, Suejen
Turkheimer, Federico E.
Moran, Rosalyn J.
Leech, Robert
Richardson, Mark P.
author_sort Fagerholm, Erik D.
collection PubMed
description The propagation of epileptic seizure activity in the brain is a widespread pathophysiology that, in principle, should yield to intervention techniques guided by mathematical models of neuronal ensemble dynamics. During a seizure, neural activity will deviate from its current dynamical regime to one in which there are significant signal fluctuations. In silico treatments of neural activity are an important tool for the understanding of how the healthy brain can maintain stability, as well as of how pathology can lead to seizures. The hope is that, contained within the mathematical foundations of such treatments, there lie potential strategies for mitigating instabilities, e.g. via external stimulation. Here, we demonstrate that the dynamic causal modelling neuronal state equation generalises to a Fokker-Planck formalism if one extends the framework to model the ways in which activity propagates along the structural connections of neural systems. Using the Jacobian of this generalised state equation, we show that an initially unstable system can be rendered stable via a reduction in diffusivity–i.e., by lowering the rate at which neuronal fluctuations disperse to neighbouring regions. We show, for neural systems prone to epileptic seizures, that such a reduction in diffusivity can be achieved via external stimulation. Specifically, we show that this stimulation should be applied in such a way as to temporarily mirror the activity profile of a pathological region in its functionally connected areas. This counter-intuitive method is intended to be used pre-emptively–i.e., in order to mitigate the effects of the seizure, or ideally even prevent it from occurring in the first place. We offer proof of principle using simulations based on functional neuroimaging data collected from patients with idiopathic generalised epilepsy, in which we successfully suppress pathological activity in a distinct sub-network prior to seizure onset. Our hope is that this technique can form the basis for future real-time monitoring and intervention devices that are capable of treating epilepsy in a non-invasive manner.
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spelling pubmed-77320832020-12-17 Neural diffusivity and pre-emptive epileptic seizure intervention Fagerholm, Erik D. Tangwiriyasakul, Chayanin Friston, Karl J. Violante, Inês R. Williams, Steven Carmichael, David W. Perani, Suejen Turkheimer, Federico E. Moran, Rosalyn J. Leech, Robert Richardson, Mark P. PLoS Comput Biol Research Article The propagation of epileptic seizure activity in the brain is a widespread pathophysiology that, in principle, should yield to intervention techniques guided by mathematical models of neuronal ensemble dynamics. During a seizure, neural activity will deviate from its current dynamical regime to one in which there are significant signal fluctuations. In silico treatments of neural activity are an important tool for the understanding of how the healthy brain can maintain stability, as well as of how pathology can lead to seizures. The hope is that, contained within the mathematical foundations of such treatments, there lie potential strategies for mitigating instabilities, e.g. via external stimulation. Here, we demonstrate that the dynamic causal modelling neuronal state equation generalises to a Fokker-Planck formalism if one extends the framework to model the ways in which activity propagates along the structural connections of neural systems. Using the Jacobian of this generalised state equation, we show that an initially unstable system can be rendered stable via a reduction in diffusivity–i.e., by lowering the rate at which neuronal fluctuations disperse to neighbouring regions. We show, for neural systems prone to epileptic seizures, that such a reduction in diffusivity can be achieved via external stimulation. Specifically, we show that this stimulation should be applied in such a way as to temporarily mirror the activity profile of a pathological region in its functionally connected areas. This counter-intuitive method is intended to be used pre-emptively–i.e., in order to mitigate the effects of the seizure, or ideally even prevent it from occurring in the first place. We offer proof of principle using simulations based on functional neuroimaging data collected from patients with idiopathic generalised epilepsy, in which we successfully suppress pathological activity in a distinct sub-network prior to seizure onset. Our hope is that this technique can form the basis for future real-time monitoring and intervention devices that are capable of treating epilepsy in a non-invasive manner. Public Library of Science 2020-12-01 /pmc/articles/PMC7732083/ /pubmed/33259483 http://dx.doi.org/10.1371/journal.pcbi.1008448 Text en © 2020 Fagerholm 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
Fagerholm, Erik D.
Tangwiriyasakul, Chayanin
Friston, Karl J.
Violante, Inês R.
Williams, Steven
Carmichael, David W.
Perani, Suejen
Turkheimer, Federico E.
Moran, Rosalyn J.
Leech, Robert
Richardson, Mark P.
Neural diffusivity and pre-emptive epileptic seizure intervention
title Neural diffusivity and pre-emptive epileptic seizure intervention
title_full Neural diffusivity and pre-emptive epileptic seizure intervention
title_fullStr Neural diffusivity and pre-emptive epileptic seizure intervention
title_full_unstemmed Neural diffusivity and pre-emptive epileptic seizure intervention
title_short Neural diffusivity and pre-emptive epileptic seizure intervention
title_sort neural diffusivity and pre-emptive epileptic seizure intervention
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7732083/
https://www.ncbi.nlm.nih.gov/pubmed/33259483
http://dx.doi.org/10.1371/journal.pcbi.1008448
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