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April 23, 2019; 92 (17) Article

Cognitive phenotypes in temporal lobe epilepsy are associated with distinct patterns of white matter network abnormalities

Anny Reyes, Erik Kaestner, Naeim Bahrami, Akshara Balachandra, Manu Hegde, Brianna M. Paul, Bruce Hermann, Carrie R. McDonald
First published March 27, 2019, DOI: https://doi.org/10.1212/WNL.0000000000007370
Anny Reyes
From the San Diego State University/University of California San Diego Joint Doctoral Program in Clinical Psychology (A.R.); Center for Multimodal Imaging and Genetics (A.R., E.K., N.B., A.B., C.R.M.) and Department of Psychiatry (C.R.M.), University of California, San Diego; Department of Neurology (M.H., B.M.P.), University of California, San Francisco; UCSF Comprehensive Epilepsy Center (M.H., B.M.P.), San Francisco; Matthews Neuropsychology Section (B.H.), University of Wisconsin–Madison; and UCSD Comprehensive Epilepsy Center (C.R.M.), San Diego, CA.
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Erik Kaestner
From the San Diego State University/University of California San Diego Joint Doctoral Program in Clinical Psychology (A.R.); Center for Multimodal Imaging and Genetics (A.R., E.K., N.B., A.B., C.R.M.) and Department of Psychiatry (C.R.M.), University of California, San Diego; Department of Neurology (M.H., B.M.P.), University of California, San Francisco; UCSF Comprehensive Epilepsy Center (M.H., B.M.P.), San Francisco; Matthews Neuropsychology Section (B.H.), University of Wisconsin–Madison; and UCSD Comprehensive Epilepsy Center (C.R.M.), San Diego, CA.
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Naeim Bahrami
From the San Diego State University/University of California San Diego Joint Doctoral Program in Clinical Psychology (A.R.); Center for Multimodal Imaging and Genetics (A.R., E.K., N.B., A.B., C.R.M.) and Department of Psychiatry (C.R.M.), University of California, San Diego; Department of Neurology (M.H., B.M.P.), University of California, San Francisco; UCSF Comprehensive Epilepsy Center (M.H., B.M.P.), San Francisco; Matthews Neuropsychology Section (B.H.), University of Wisconsin–Madison; and UCSD Comprehensive Epilepsy Center (C.R.M.), San Diego, CA.
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Akshara Balachandra
From the San Diego State University/University of California San Diego Joint Doctoral Program in Clinical Psychology (A.R.); Center for Multimodal Imaging and Genetics (A.R., E.K., N.B., A.B., C.R.M.) and Department of Psychiatry (C.R.M.), University of California, San Diego; Department of Neurology (M.H., B.M.P.), University of California, San Francisco; UCSF Comprehensive Epilepsy Center (M.H., B.M.P.), San Francisco; Matthews Neuropsychology Section (B.H.), University of Wisconsin–Madison; and UCSD Comprehensive Epilepsy Center (C.R.M.), San Diego, CA.
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Manu Hegde
From the San Diego State University/University of California San Diego Joint Doctoral Program in Clinical Psychology (A.R.); Center for Multimodal Imaging and Genetics (A.R., E.K., N.B., A.B., C.R.M.) and Department of Psychiatry (C.R.M.), University of California, San Diego; Department of Neurology (M.H., B.M.P.), University of California, San Francisco; UCSF Comprehensive Epilepsy Center (M.H., B.M.P.), San Francisco; Matthews Neuropsychology Section (B.H.), University of Wisconsin–Madison; and UCSD Comprehensive Epilepsy Center (C.R.M.), San Diego, CA.
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Brianna M. Paul
From the San Diego State University/University of California San Diego Joint Doctoral Program in Clinical Psychology (A.R.); Center for Multimodal Imaging and Genetics (A.R., E.K., N.B., A.B., C.R.M.) and Department of Psychiatry (C.R.M.), University of California, San Diego; Department of Neurology (M.H., B.M.P.), University of California, San Francisco; UCSF Comprehensive Epilepsy Center (M.H., B.M.P.), San Francisco; Matthews Neuropsychology Section (B.H.), University of Wisconsin–Madison; and UCSD Comprehensive Epilepsy Center (C.R.M.), San Diego, CA.
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Bruce Hermann
From the San Diego State University/University of California San Diego Joint Doctoral Program in Clinical Psychology (A.R.); Center for Multimodal Imaging and Genetics (A.R., E.K., N.B., A.B., C.R.M.) and Department of Psychiatry (C.R.M.), University of California, San Diego; Department of Neurology (M.H., B.M.P.), University of California, San Francisco; UCSF Comprehensive Epilepsy Center (M.H., B.M.P.), San Francisco; Matthews Neuropsychology Section (B.H.), University of Wisconsin–Madison; and UCSD Comprehensive Epilepsy Center (C.R.M.), San Diego, CA.
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Carrie R. McDonald
From the San Diego State University/University of California San Diego Joint Doctoral Program in Clinical Psychology (A.R.); Center for Multimodal Imaging and Genetics (A.R., E.K., N.B., A.B., C.R.M.) and Department of Psychiatry (C.R.M.), University of California, San Diego; Department of Neurology (M.H., B.M.P.), University of California, San Francisco; UCSF Comprehensive Epilepsy Center (M.H., B.M.P.), San Francisco; Matthews Neuropsychology Section (B.H.), University of Wisconsin–Madison; and UCSD Comprehensive Epilepsy Center (C.R.M.), San Diego, CA.
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Cognitive phenotypes in temporal lobe epilepsy are associated with distinct patterns of white matter network abnormalities
Anny Reyes, Erik Kaestner, Naeim Bahrami, Akshara Balachandra, Manu Hegde, Brianna M. Paul, Bruce Hermann, Carrie R. McDonald
Neurology Apr 2019, 92 (17) e1957-e1968; DOI: 10.1212/WNL.0000000000007370

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Abstract

Objective To identify distinct cognitive phenotypes in temporal lobe epilepsy (TLE) and evaluate patterns of white matter (WM) network alterations associated with each phenotype.

Methods Seventy patients with TLE were characterized into 4 distinct cognitive phenotypes based on patterns of impairment in language and verbal memory measures (language and memory impaired, memory impaired only, language impaired only, no impairment). Diffusion tensor imaging was obtained in all patients and in 46 healthy controls (HC). Fractional anisotropy (FA) and mean diffusivity (MD) of the WM directly beneath neocortex (i.e., superficial WM [SWM]) and of deep WM tracts associated with memory and language were calculated for each phenotype. Regional and network-based SWM analyses were performed across phenotypes.

Results The language and memory impaired group and the memory impaired group showed distinct patterns of microstructural abnormalities in SWM relative to HC. In addition, the language and memory impaired group showed widespread alterations in WM tracts and altered global SWM network topology. Patients with isolated language impairment exhibited poor network structure within perisylvian cortex, despite relatively intact global SWM network structure, whereas patients with no impairment appeared similar to HC across all measures.

Conclusions These findings demonstrate a differential pattern of WM microstructural abnormalities across distinct cognitive phenotypes in TLE that can be appreciated at both the regional and network levels. These findings not only help to unravel the underlying neurobiology associated with cognitive impairment in TLE, but they could also aid in establishing cognitive taxonomies or in the prediction of cognitive course in TLE.

Glossary

AD=
Alzheimer disease;
AED=
antiepileptic drug;
ANOVA=
analysis of variance;
ARC=
arcuate fasciculus;
DTI=
diffusion tensor imaging;
FA=
fractional anisotropy;
FDR=
false discovery rate;
FOV=
field of view;
HC=
healthy control;
ILF=
inferior longitudinal fasciculus;
MD=
mean diffusivity;
MTS=
mesial temporal sclerosis;
ROI=
region of interest;
STG=
superior temporal gyrus;
SWM=
superficial white matter;
TE=
echo time;
TLE=
temporal lobe epilepsy;
TR=
repetition time;
UNC=
uncinate fasciculus;
WM=
white matter

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.

  • Received September 28, 2018.
  • Accepted in final form December 31, 2018.
  • © 2019 American Academy of Neurology
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