Bilingualism and Structural Network Organization in Temporal Lobe Epilepsy: Resilience in Neurologic Disease.

Humans Epilepsy, Temporal Lobe Multilingualism Magnetic Resonance Imaging / methods Temporal Lobe Connectome

Journal

Neurology
ISSN: 1526-632X
Titre abrégé: Neurology
Pays: United States
ID NLM: 0401060

Informations de publication

Date de publication:
02 05 2023
Historique:
received: 15 07 2022
accepted: 06 01 2023
pmc-release: 02 05 2024
medline: 3 5 2023
pubmed: 1 3 2023
entrez: 28 2 2023
Statut: ppublish

Résumé

There is growing evidence that bilingualism can induce neuroplasticity and modulate neural efficiency, resulting in greater resistance to neurologic disease. However, whether bilingualism is beneficial to neural health in the presence of epilepsy is unknown. We tested whether bilingual individuals with temporal lobe epilepsy (TLE) have improved whole-brain structural white matter network organization. Healthy controls and individuals with TLE recruited from 2 specialized epilepsy centers completed diffusion-weighted MRI and neuropsychological testing as part of an observational cohort study. Whole-brain connectomes were generated via diffusion tractography and analyzed using graph theory. Global analyses compared network integration (path length) and specialization (transitivity) in TLE vs controls and in a 2 (left vs right TLE) × 2 (bilingual vs monolingual) model. Local analyses compared mean local efficiency of predefined frontal-executive and language (i.e., perisylvian) subnetworks. Exploratory correlations examined associations between network organization and neuropsychological performance. A total of 29 bilingual and 88 monolingual individuals with TLE matched on several demographic and clinical variables and 81 age-matched healthy controls were included. Globally, a significant interaction between language status and side of seizure onset revealed higher network organization in bilinguals compared with monolinguals but only in left TLE (LTLE). Locally, bilinguals with LTLE showed higher efficiency in frontal-executive but not in perisylvian networks compared with LTLE monolinguals. Improved whole-brain network organization was associated with better executive function performance in bilingual but not monolingual LTLE. Higher white matter network organization in bilingual individuals with LTLE suggests a neuromodulatory effect of bilingualism on whole-brain connectivity in epilepsy, providing evidence for neural reserve. This may reflect attenuation of or compensation for epilepsy-related dysfunction of the left hemisphere, potentially driven by increased efficiency of frontal-executive networks that mediate dual-language control. This highlights a potential role of bilingualism as a protective factor in epilepsy, motivating further research across neurologic disorders to define mechanisms and develop interventions.

Sections du résumé

BACKGROUND AND OBJECTIVES
There is growing evidence that bilingualism can induce neuroplasticity and modulate neural efficiency, resulting in greater resistance to neurologic disease. However, whether bilingualism is beneficial to neural health in the presence of epilepsy is unknown. We tested whether bilingual individuals with temporal lobe epilepsy (TLE) have improved whole-brain structural white matter network organization.
METHODS
Healthy controls and individuals with TLE recruited from 2 specialized epilepsy centers completed diffusion-weighted MRI and neuropsychological testing as part of an observational cohort study. Whole-brain connectomes were generated via diffusion tractography and analyzed using graph theory. Global analyses compared network integration (path length) and specialization (transitivity) in TLE vs controls and in a 2 (left vs right TLE) × 2 (bilingual vs monolingual) model. Local analyses compared mean local efficiency of predefined frontal-executive and language (i.e., perisylvian) subnetworks. Exploratory correlations examined associations between network organization and neuropsychological performance.
RESULTS
A total of 29 bilingual and 88 monolingual individuals with TLE matched on several demographic and clinical variables and 81 age-matched healthy controls were included. Globally, a significant interaction between language status and side of seizure onset revealed higher network organization in bilinguals compared with monolinguals but only in left TLE (LTLE). Locally, bilinguals with LTLE showed higher efficiency in frontal-executive but not in perisylvian networks compared with LTLE monolinguals. Improved whole-brain network organization was associated with better executive function performance in bilingual but not monolingual LTLE.
DISCUSSION
Higher white matter network organization in bilingual individuals with LTLE suggests a neuromodulatory effect of bilingualism on whole-brain connectivity in epilepsy, providing evidence for neural reserve. This may reflect attenuation of or compensation for epilepsy-related dysfunction of the left hemisphere, potentially driven by increased efficiency of frontal-executive networks that mediate dual-language control. This highlights a potential role of bilingualism as a protective factor in epilepsy, motivating further research across neurologic disorders to define mechanisms and develop interventions.

Identifiants

DOI: 10.1212/WNL.0000000000207087 PMID: 36854619 PMC: PMC10159767
pubmed: 36854619
pii: WNL.0000000000207087
doi: 10.1212/WNL.0000000000207087
pmc: PMC10159767
doi:

Types de publication

Observational Study Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1887-e1899

Subventions

Organisme : NINDS NIH HHS
ID : K01 NS124831
Pays : United States
Organisme : NCATS NIH HHS
ID : UL1 TR001442
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS122827
Pays : United States
Organisme : NINDS NIH HHS
ID : F32 NS119285
Pays : United States
Organisme : NINDS NIH HHS
ID : F31 NS111883
Pays : United States
Organisme : NIDCD NIH HHS
ID : K01 DC016904
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS124585
Pays : United States

Commentaires et corrections

Type : CommentIn

Informations de copyright

© 2023 American Academy of Neurology.

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Auteurs

Alena Stasenko (A)

From the Center for Multimodal Imaging and Genetics (A. Stasenko, E.K., D.A., A. Schadler, A.R., C.R.M.), Department of Psychiatry (A. Stasenko, E.K., D.A., A. Schadler, C.R.M.), Department of Radiation Medicine & Applied Sciences (A.R., C.R.M.), and Department of Neurosciences (J.J.S.), University of California, San Diego; Department of Psychology (J.L.H.), San Diego State University, CA; and Department of Psychiatry and Biobehavioral Sciences (M.P.), David Geffen School of Medicine at UCLA, University of California, Los Angeles.
ORCID: 0000-0001-9446-9018

Erik Kaestner (E)

From the Center for Multimodal Imaging and Genetics (A. Stasenko, E.K., D.A., A. Schadler, A.R., C.R.M.), Department of Psychiatry (A. Stasenko, E.K., D.A., A. Schadler, C.R.M.), Department of Radiation Medicine & Applied Sciences (A.R., C.R.M.), and Department of Neurosciences (J.J.S.), University of California, San Diego; Department of Psychology (J.L.H.), San Diego State University, CA; and Department of Psychiatry and Biobehavioral Sciences (M.P.), David Geffen School of Medicine at UCLA, University of California, Los Angeles.
ORCID: 0000-0003-3252-5365

Donatello Arienzo (D)

From the Center for Multimodal Imaging and Genetics (A. Stasenko, E.K., D.A., A. Schadler, A.R., C.R.M.), Department of Psychiatry (A. Stasenko, E.K., D.A., A. Schadler, C.R.M.), Department of Radiation Medicine & Applied Sciences (A.R., C.R.M.), and Department of Neurosciences (J.J.S.), University of California, San Diego; Department of Psychology (J.L.H.), San Diego State University, CA; and Department of Psychiatry and Biobehavioral Sciences (M.P.), David Geffen School of Medicine at UCLA, University of California, Los Angeles.

Adam Schadler (A)

From the Center for Multimodal Imaging and Genetics (A. Stasenko, E.K., D.A., A. Schadler, A.R., C.R.M.), Department of Psychiatry (A. Stasenko, E.K., D.A., A. Schadler, C.R.M.), Department of Radiation Medicine & Applied Sciences (A.R., C.R.M.), and Department of Neurosciences (J.J.S.), University of California, San Diego; Department of Psychology (J.L.H.), San Diego State University, CA; and Department of Psychiatry and Biobehavioral Sciences (M.P.), David Geffen School of Medicine at UCLA, University of California, Los Angeles.

Anny Reyes (A)

From the Center for Multimodal Imaging and Genetics (A. Stasenko, E.K., D.A., A. Schadler, A.R., C.R.M.), Department of Psychiatry (A. Stasenko, E.K., D.A., A. Schadler, C.R.M.), Department of Radiation Medicine & Applied Sciences (A.R., C.R.M.), and Department of Neurosciences (J.J.S.), University of California, San Diego; Department of Psychology (J.L.H.), San Diego State University, CA; and Department of Psychiatry and Biobehavioral Sciences (M.P.), David Geffen School of Medicine at UCLA, University of California, Los Angeles.

Jerry J Shih (JJ)

From the Center for Multimodal Imaging and Genetics (A. Stasenko, E.K., D.A., A. Schadler, A.R., C.R.M.), Department of Psychiatry (A. Stasenko, E.K., D.A., A. Schadler, C.R.M.), Department of Radiation Medicine & Applied Sciences (A.R., C.R.M.), and Department of Neurosciences (J.J.S.), University of California, San Diego; Department of Psychology (J.L.H.), San Diego State University, CA; and Department of Psychiatry and Biobehavioral Sciences (M.P.), David Geffen School of Medicine at UCLA, University of California, Los Angeles.

Jonathan L Helm (JL)

From the Center for Multimodal Imaging and Genetics (A. Stasenko, E.K., D.A., A. Schadler, A.R., C.R.M.), Department of Psychiatry (A. Stasenko, E.K., D.A., A. Schadler, C.R.M.), Department of Radiation Medicine & Applied Sciences (A.R., C.R.M.), and Department of Neurosciences (J.J.S.), University of California, San Diego; Department of Psychology (J.L.H.), San Diego State University, CA; and Department of Psychiatry and Biobehavioral Sciences (M.P.), David Geffen School of Medicine at UCLA, University of California, Los Angeles.

Monika Połczyńska (M)

From the Center for Multimodal Imaging and Genetics (A. Stasenko, E.K., D.A., A. Schadler, A.R., C.R.M.), Department of Psychiatry (A. Stasenko, E.K., D.A., A. Schadler, C.R.M.), Department of Radiation Medicine & Applied Sciences (A.R., C.R.M.), and Department of Neurosciences (J.J.S.), University of California, San Diego; Department of Psychology (J.L.H.), San Diego State University, CA; and Department of Psychiatry and Biobehavioral Sciences (M.P.), David Geffen School of Medicine at UCLA, University of California, Los Angeles.

Carrie R McDonald (CR)

From the Center for Multimodal Imaging and Genetics (A. Stasenko, E.K., D.A., A. Schadler, A.R., C.R.M.), Department of Psychiatry (A. Stasenko, E.K., D.A., A. Schadler, C.R.M.), Department of Radiation Medicine & Applied Sciences (A.R., C.R.M.), and Department of Neurosciences (J.J.S.), University of California, San Diego; Department of Psychology (J.L.H.), San Diego State University, CA; and Department of Psychiatry and Biobehavioral Sciences (M.P.), David Geffen School of Medicine at UCLA, University of California, Los Angeles. camcdonald@ucsd.edu.

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Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Bilingualism and Structural Network...
questionsmedicales.fr › Maladies du système nerveux › Maladies du système nerveux central › Encéphalopathies › Épilepsie › Syndromes épileptiques › Épilepsie temporale › Bilingualism and Structural Network...
questionsmedicales.fr › Sciences de l'information › Langage › Arts du langage › Multilinguisme › Bilingualism and Structural Network...
questionsmedicales.fr › Diagnostic › Techniques et procédures diagnostiques › Imagerie diagnostique › Tomographie › Imagerie par résonance magnétique › Bilingualism and Structural Network...
questionsmedicales.fr › Système nerveux › Système nerveux central › Encéphale › Prosencéphale › Télencéphale › Cerveau › Cortex cérébral › Lobe temporal › Bilingualism and Structural Network...
questionsmedicales.fr › Techniques d'investigation › Neuroimagerie › Neuroimagerie fonctionnelle › Cartographie cérébrale › Connectome › Bilingualism and Structural Network...