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Episodic memory network connectivity in temporal lobe epilepsy

OBJECTIVE: Temporal lobe epilepsy (TLE) affects brain networks and is associated with impairment of episodic memory. Temporal and extratemporal reorganization of memory functions is described in functional magnetic resonance imaging (fMRI) studies. Functional reorganizations have been shown at the l...

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Autores principales: Fleury, Marine, Buck, Sarah, Binding, Lawrence P., Caciagli, Lorenzo, Vos, Sjoerd B., Winston, Gavin P., Thompson, Pamela J., Koepp, Matthias J., Duncan, John S., Sidhu, Meneka K.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9804196/
https://www.ncbi.nlm.nih.gov/pubmed/35848050
http://dx.doi.org/10.1111/epi.17370
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author Fleury, Marine
Buck, Sarah
Binding, Lawrence P.
Caciagli, Lorenzo
Vos, Sjoerd B.
Winston, Gavin P.
Thompson, Pamela J.
Koepp, Matthias J.
Duncan, John S.
Sidhu, Meneka K.
author_facet Fleury, Marine
Buck, Sarah
Binding, Lawrence P.
Caciagli, Lorenzo
Vos, Sjoerd B.
Winston, Gavin P.
Thompson, Pamela J.
Koepp, Matthias J.
Duncan, John S.
Sidhu, Meneka K.
author_sort Fleury, Marine
collection PubMed
description OBJECTIVE: Temporal lobe epilepsy (TLE) affects brain networks and is associated with impairment of episodic memory. Temporal and extratemporal reorganization of memory functions is described in functional magnetic resonance imaging (fMRI) studies. Functional reorganizations have been shown at the local activation level, but network‐level alterations have been underinvestigated. We aim to investigate the functional anatomy of memory networks using memory fMRI and determine how this relates to memory function in TLE. METHODS: Ninety patients with unilateral TLE (43 left) and 29 controls performed a memory‐encoding fMRI paradigm of faces and words with subsequent out‐of‐scanner recognition test. Subsequent memory event‐related contrasts of words and faces remembered were generated. Psychophysiological interaction analysis investigated task‐associated changes in functional connectivity seeding from the mesial temporal lobes (MTLs). Correlations between changes in functional connectivity and clinical memory scores, epilepsy duration, age at epilepsy onset, and seizure frequency were investigated, and between connectivity supportive of better memory and disease burden. Connectivity differences between controls and TLE, and between TLE with and without hippocampal sclerosis, were explored using these confounds as regressors of no interest. RESULTS: Compared to controls, TLE patients showed widespread decreased connectivity between bilateral MTLs and frontal lobes, and increased local connectivity between the anterior MTLs bilaterally. Increased intrinsic connectivity within the bilateral MTLs correlated with better out‐of‐scanner memory performance in both left and right TLE. Longer epilepsy duration and higher seizure frequency were associated with decreased connectivity between bilateral MTLs and left/right orbitofrontal cortex (OFC) and insula, connections supportive of memory functions. TLE due to hippocampal sclerosis was associated with greater connectivity disruption within the MTL and extratemporally. SIGNIFICANCE: Connectivity analyses showed that TLE is associated with temporal and extratemporal memory network reorganization. Increased bilateral functional connectivity within the MTL and connectivity to OFC and insula are efficient, and are disrupted by greater disease burden.
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spelling pubmed-98041962023-01-03 Episodic memory network connectivity in temporal lobe epilepsy Fleury, Marine Buck, Sarah Binding, Lawrence P. Caciagli, Lorenzo Vos, Sjoerd B. Winston, Gavin P. Thompson, Pamela J. Koepp, Matthias J. Duncan, John S. Sidhu, Meneka K. Epilepsia Research Article OBJECTIVE: Temporal lobe epilepsy (TLE) affects brain networks and is associated with impairment of episodic memory. Temporal and extratemporal reorganization of memory functions is described in functional magnetic resonance imaging (fMRI) studies. Functional reorganizations have been shown at the local activation level, but network‐level alterations have been underinvestigated. We aim to investigate the functional anatomy of memory networks using memory fMRI and determine how this relates to memory function in TLE. METHODS: Ninety patients with unilateral TLE (43 left) and 29 controls performed a memory‐encoding fMRI paradigm of faces and words with subsequent out‐of‐scanner recognition test. Subsequent memory event‐related contrasts of words and faces remembered were generated. Psychophysiological interaction analysis investigated task‐associated changes in functional connectivity seeding from the mesial temporal lobes (MTLs). Correlations between changes in functional connectivity and clinical memory scores, epilepsy duration, age at epilepsy onset, and seizure frequency were investigated, and between connectivity supportive of better memory and disease burden. Connectivity differences between controls and TLE, and between TLE with and without hippocampal sclerosis, were explored using these confounds as regressors of no interest. RESULTS: Compared to controls, TLE patients showed widespread decreased connectivity between bilateral MTLs and frontal lobes, and increased local connectivity between the anterior MTLs bilaterally. Increased intrinsic connectivity within the bilateral MTLs correlated with better out‐of‐scanner memory performance in both left and right TLE. Longer epilepsy duration and higher seizure frequency were associated with decreased connectivity between bilateral MTLs and left/right orbitofrontal cortex (OFC) and insula, connections supportive of memory functions. TLE due to hippocampal sclerosis was associated with greater connectivity disruption within the MTL and extratemporally. SIGNIFICANCE: Connectivity analyses showed that TLE is associated with temporal and extratemporal memory network reorganization. Increased bilateral functional connectivity within the MTL and connectivity to OFC and insula are efficient, and are disrupted by greater disease burden. John Wiley and Sons Inc. 2022-08-02 2022-10 /pmc/articles/PMC9804196/ /pubmed/35848050 http://dx.doi.org/10.1111/epi.17370 Text en © 2022 The Authors. Epilepsia published by Wiley Periodicals LLC on behalf of International League Against Epilepsy. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Fleury, Marine
Buck, Sarah
Binding, Lawrence P.
Caciagli, Lorenzo
Vos, Sjoerd B.
Winston, Gavin P.
Thompson, Pamela J.
Koepp, Matthias J.
Duncan, John S.
Sidhu, Meneka K.
Episodic memory network connectivity in temporal lobe epilepsy
title Episodic memory network connectivity in temporal lobe epilepsy
title_full Episodic memory network connectivity in temporal lobe epilepsy
title_fullStr Episodic memory network connectivity in temporal lobe epilepsy
title_full_unstemmed Episodic memory network connectivity in temporal lobe epilepsy
title_short Episodic memory network connectivity in temporal lobe epilepsy
title_sort episodic memory network connectivity in temporal lobe epilepsy
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9804196/
https://www.ncbi.nlm.nih.gov/pubmed/35848050
http://dx.doi.org/10.1111/epi.17370
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