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May 02, 2023; 100 (18) Research Article

Bilingualism and Structural Network Organization in Temporal Lobe Epilepsy

Resilience in Neurologic Disease

View ORCID ProfileAlena Stasenko, View ORCID ProfileErik Kaestner, Donatello Arienzo, Adam Schadler, Anny Reyes, Jerry J. Shih, Jonathan L. Helm, Monika Połczyńska, Carrie R. McDonald
First published February 28, 2023, DOI: https://doi.org/10.1212/WNL.0000000000207087
Alena Stasenko
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.
PhD
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  • ORCID record for Alena Stasenko
Erik Kaestner
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.
PhD
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Donatello Arienzo
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.
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Adam Schadler
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.
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Anny Reyes
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.
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Jerry J. Shih
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.
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Jonathan L. Helm
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.
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Monika Połczyńska
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.
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Carrie R. McDonald
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.
PhD
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Citation
Bilingualism and Structural Network Organization in Temporal Lobe Epilepsy
Resilience in Neurologic Disease
Alena Stasenko, Erik Kaestner, Donatello Arienzo, Adam Schadler, Anny Reyes, Jerry J. Shih, Jonathan L. Helm, Monika Połczyńska, Carrie R. McDonald
Neurology May 2023, 100 (18) e1887-e1899; DOI: 10.1212/WNL.0000000000207087

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Abstract

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.

Glossary

3D=
3 dimensional;
AD=
Alzheimer disease;
ANOVA=
analysis of variance;
B-LTLE=
bilingual LTLE;
B-RTLE=
bilingual RTLE;
dMRI=
diffusion-weighted MRI;
DRM=
dynamic restructuring model;
FOV=
field of view;
HC=
healthy control;
LTLE=
left TLE;
M-LTLE=
monolingual LTLE;
M-RTLE=
monolingual RTLE;
MTS=
mesial temporal sclerosis;
ROI=
region of interest;
RTLE=
right TLE;
TE=
echo time;
TI=
inversion time;
TLE=
temporal lobe epilepsy;
TR=
repetition time;
UC=
University of California;
UCSD=
UC San Diego;
UCSF=
UC San Francisco;
WASI=
Wechsler Abbreviated Scale of Intelligence

Footnotes

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Submitted and externally peer reviewed. The handling editor was Associate Editor Barbara Jobst, MD, PhD, FAAN.

  • Editorial, page 847

  • Received July 15, 2022.
  • Accepted in final form January 6, 2023.
  • © 2023 American Academy of Neurology
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