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Putative cause of seizure-induced cognitive alterations: The oscillatory reconfiguration of seizure network

INTRODUCTION: The dynamic reconfiguration of network oscillations is connected with cognitive processes. Changes in how neural networks and signaling pathways work are crucial to how epilepsy and related conditions develop. Specifically, there is evidence that prolonged or recurrent seizures may ind...

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Autores principales: Fan, Denggui, Qi, Lixue, Yang, Zecheng, Luan, Guoming, Wang, Qingyun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9893114/
https://www.ncbi.nlm.nih.gov/pubmed/36743804
http://dx.doi.org/10.3389/fnins.2023.1126875
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author Fan, Denggui
Qi, Lixue
Yang, Zecheng
Luan, Guoming
Wang, Qingyun
author_facet Fan, Denggui
Qi, Lixue
Yang, Zecheng
Luan, Guoming
Wang, Qingyun
author_sort Fan, Denggui
collection PubMed
description INTRODUCTION: The dynamic reconfiguration of network oscillations is connected with cognitive processes. Changes in how neural networks and signaling pathways work are crucial to how epilepsy and related conditions develop. Specifically, there is evidence that prolonged or recurrent seizures may induce or exacerbate cognitive impairment. However, it still needs to be determined how the seizure brain configures its functional structure to shape the battle of strong local oscillations vs. slow global oscillations in the network to impair cognitive function. METHODS: In this paper, we aim to deduce the network mechanisms underlying seizure-induced cognitive impairment by comparing the evolution of strong local oscillations with slow global oscillations and their link to the resting state of healthy controls. Here, we construct a dynamically efficient network of pathological seizures by calculating the synchrony and directionality of information flow between nine patients’ SEEG signals. Then, using a pattern-based method, we found hierarchical modules in the brain’s functional network and measured the functional balance between the network’s local strong and slow global oscillations. RESULTS AND DISCUSSION: According to the findings, a tremendous rise in strong local oscillations during seizures and an increase in slow global oscillations after seizures corresponded to the initiation and recovery of cognitive impairment. Specifically, during the interictal period, local strong and slow global oscillations are in metastable balance, which is the same as a normal cognitive process and can be switched easily. During the pre-ictal period, the two show a bimodal pattern of separate peaks that cannot be easily switched, and some flexibility is lost. During the seizure period, a single-peak pattern with negative peaks is showcased, and the network eventually transitions to a very intense strong local oscillation state. These results shed light on the mechanism behind network oscillations in epilepsy-induced cognitive impairment. On the other hand, the differential (similarity) of oscillatory reorganization between the local (non) epileptogenic network and the global network may be an emergency protective mechanism of the brain, preventing the spread of pathological information flow to more healthy brain regions.
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spelling pubmed-98931142023-02-03 Putative cause of seizure-induced cognitive alterations: The oscillatory reconfiguration of seizure network Fan, Denggui Qi, Lixue Yang, Zecheng Luan, Guoming Wang, Qingyun Front Neurosci Neuroscience INTRODUCTION: The dynamic reconfiguration of network oscillations is connected with cognitive processes. Changes in how neural networks and signaling pathways work are crucial to how epilepsy and related conditions develop. Specifically, there is evidence that prolonged or recurrent seizures may induce or exacerbate cognitive impairment. However, it still needs to be determined how the seizure brain configures its functional structure to shape the battle of strong local oscillations vs. slow global oscillations in the network to impair cognitive function. METHODS: In this paper, we aim to deduce the network mechanisms underlying seizure-induced cognitive impairment by comparing the evolution of strong local oscillations with slow global oscillations and their link to the resting state of healthy controls. Here, we construct a dynamically efficient network of pathological seizures by calculating the synchrony and directionality of information flow between nine patients’ SEEG signals. Then, using a pattern-based method, we found hierarchical modules in the brain’s functional network and measured the functional balance between the network’s local strong and slow global oscillations. RESULTS AND DISCUSSION: According to the findings, a tremendous rise in strong local oscillations during seizures and an increase in slow global oscillations after seizures corresponded to the initiation and recovery of cognitive impairment. Specifically, during the interictal period, local strong and slow global oscillations are in metastable balance, which is the same as a normal cognitive process and can be switched easily. During the pre-ictal period, the two show a bimodal pattern of separate peaks that cannot be easily switched, and some flexibility is lost. During the seizure period, a single-peak pattern with negative peaks is showcased, and the network eventually transitions to a very intense strong local oscillation state. These results shed light on the mechanism behind network oscillations in epilepsy-induced cognitive impairment. On the other hand, the differential (similarity) of oscillatory reorganization between the local (non) epileptogenic network and the global network may be an emergency protective mechanism of the brain, preventing the spread of pathological information flow to more healthy brain regions. Frontiers Media S.A. 2023-01-19 /pmc/articles/PMC9893114/ /pubmed/36743804 http://dx.doi.org/10.3389/fnins.2023.1126875 Text en Copyright © 2023 Fan, Qi, Yang, Luan and Wang. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Fan, Denggui
Qi, Lixue
Yang, Zecheng
Luan, Guoming
Wang, Qingyun
Putative cause of seizure-induced cognitive alterations: The oscillatory reconfiguration of seizure network
title Putative cause of seizure-induced cognitive alterations: The oscillatory reconfiguration of seizure network
title_full Putative cause of seizure-induced cognitive alterations: The oscillatory reconfiguration of seizure network
title_fullStr Putative cause of seizure-induced cognitive alterations: The oscillatory reconfiguration of seizure network
title_full_unstemmed Putative cause of seizure-induced cognitive alterations: The oscillatory reconfiguration of seizure network
title_short Putative cause of seizure-induced cognitive alterations: The oscillatory reconfiguration of seizure network
title_sort putative cause of seizure-induced cognitive alterations: the oscillatory reconfiguration of seizure network
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9893114/
https://www.ncbi.nlm.nih.gov/pubmed/36743804
http://dx.doi.org/10.3389/fnins.2023.1126875
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