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Large‐scale network dynamics underlying the first few hundred milliseconds after stimulus presentation: An investigation of visual recognition memory using iEEG

Recognition memory is the ability to recognize previously encountered objects. Even this relatively simple, yet extremely fast, ability requires the coordinated activity of large‐scale brain networks. However, little is known about the sub‐second dynamics of these networks. The majority of current s...

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Autores principales: Kopal, Jakub, Hlinka, Jaroslav, Despouy, Elodie, Valton, Luc, Denuelle, Marie, Sol, Jean‐Christophe, Curot, Jonathan, Barbeau, Emmanuel J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley & Sons, Inc. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10619408/
https://www.ncbi.nlm.nih.gov/pubmed/37688546
http://dx.doi.org/10.1002/hbm.26477
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author Kopal, Jakub
Hlinka, Jaroslav
Despouy, Elodie
Valton, Luc
Denuelle, Marie
Sol, Jean‐Christophe
Curot, Jonathan
Barbeau, Emmanuel J.
author_facet Kopal, Jakub
Hlinka, Jaroslav
Despouy, Elodie
Valton, Luc
Denuelle, Marie
Sol, Jean‐Christophe
Curot, Jonathan
Barbeau, Emmanuel J.
author_sort Kopal, Jakub
collection PubMed
description Recognition memory is the ability to recognize previously encountered objects. Even this relatively simple, yet extremely fast, ability requires the coordinated activity of large‐scale brain networks. However, little is known about the sub‐second dynamics of these networks. The majority of current studies into large‐scale network dynamics is primarily based on imaging techniques suffering from either poor temporal or spatial resolution. We investigated the dynamics of large‐scale functional brain networks underlying recognition memory at the millisecond scale. Specifically, we analyzed dynamic effective connectivity from intracranial electroencephalography while epileptic subjects (n = 18) performed a fast visual recognition memory task. Our data‐driven investigation using Granger causality and the analysis of communities with the Louvain algorithm spotlighted a dynamic interplay of two large‐scale networks associated with successful recognition. The first network involved the right visual ventral stream and bilateral frontal regions. It was characterized by early, predominantly bottom‐up information flow peaking at 115 ms. It was followed by the involvement of another network with predominantly top‐down connectivity peaking at 220 ms, mainly in the left anterior hemisphere. The transition between these two networks was associated with changes in network topology, evolving from a more segregated to a more integrated state. These results highlight that distinct large‐scale brain networks involved in visual recognition memory unfold early and quickly, within the first 300 ms after stimulus onset. Our study extends the current understanding of the rapid network changes during rapid cognitive processes.
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spelling pubmed-106194082023-11-02 Large‐scale network dynamics underlying the first few hundred milliseconds after stimulus presentation: An investigation of visual recognition memory using iEEG Kopal, Jakub Hlinka, Jaroslav Despouy, Elodie Valton, Luc Denuelle, Marie Sol, Jean‐Christophe Curot, Jonathan Barbeau, Emmanuel J. Hum Brain Mapp Research Articles Recognition memory is the ability to recognize previously encountered objects. Even this relatively simple, yet extremely fast, ability requires the coordinated activity of large‐scale brain networks. However, little is known about the sub‐second dynamics of these networks. The majority of current studies into large‐scale network dynamics is primarily based on imaging techniques suffering from either poor temporal or spatial resolution. We investigated the dynamics of large‐scale functional brain networks underlying recognition memory at the millisecond scale. Specifically, we analyzed dynamic effective connectivity from intracranial electroencephalography while epileptic subjects (n = 18) performed a fast visual recognition memory task. Our data‐driven investigation using Granger causality and the analysis of communities with the Louvain algorithm spotlighted a dynamic interplay of two large‐scale networks associated with successful recognition. The first network involved the right visual ventral stream and bilateral frontal regions. It was characterized by early, predominantly bottom‐up information flow peaking at 115 ms. It was followed by the involvement of another network with predominantly top‐down connectivity peaking at 220 ms, mainly in the left anterior hemisphere. The transition between these two networks was associated with changes in network topology, evolving from a more segregated to a more integrated state. These results highlight that distinct large‐scale brain networks involved in visual recognition memory unfold early and quickly, within the first 300 ms after stimulus onset. Our study extends the current understanding of the rapid network changes during rapid cognitive processes. John Wiley & Sons, Inc. 2023-09-09 /pmc/articles/PMC10619408/ /pubmed/37688546 http://dx.doi.org/10.1002/hbm.26477 Text en © 2023 The Authors. Human Brain Mapping published by Wiley Periodicals LLC. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ (https://creativecommons.org/licenses/by-nc-nd/4.0/) License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.
spellingShingle Research Articles
Kopal, Jakub
Hlinka, Jaroslav
Despouy, Elodie
Valton, Luc
Denuelle, Marie
Sol, Jean‐Christophe
Curot, Jonathan
Barbeau, Emmanuel J.
Large‐scale network dynamics underlying the first few hundred milliseconds after stimulus presentation: An investigation of visual recognition memory using iEEG
title Large‐scale network dynamics underlying the first few hundred milliseconds after stimulus presentation: An investigation of visual recognition memory using iEEG
title_full Large‐scale network dynamics underlying the first few hundred milliseconds after stimulus presentation: An investigation of visual recognition memory using iEEG
title_fullStr Large‐scale network dynamics underlying the first few hundred milliseconds after stimulus presentation: An investigation of visual recognition memory using iEEG
title_full_unstemmed Large‐scale network dynamics underlying the first few hundred milliseconds after stimulus presentation: An investigation of visual recognition memory using iEEG
title_short Large‐scale network dynamics underlying the first few hundred milliseconds after stimulus presentation: An investigation of visual recognition memory using iEEG
title_sort large‐scale network dynamics underlying the first few hundred milliseconds after stimulus presentation: an investigation of visual recognition memory using ieeg
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10619408/
https://www.ncbi.nlm.nih.gov/pubmed/37688546
http://dx.doi.org/10.1002/hbm.26477
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