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November 05, 2013; 81 (19) Article

Presurgical connectome and postsurgical seizure control in temporal lobe epilepsy

Leonardo Bonilha, Joseph A. Helpern, Rup Sainju, Travis Nesland, Jonathan C. Edwards, Steven S. Glazier, Ali Tabesh
First published October 9, 2013, DOI: https://doi.org/10.1212/01.wnl.0000435306.95271.5f
Leonardo Bonilha
From the Comprehensive Epilepsy Center, Department of Neurosciences (L.B., R.S., T.N., J.C.E.), Department of Radiology and Radiological Science (J.A.H., A.T.), and Center for Biomedical Imaging (L.B., J.A.H., A.T.), Medical University of South Carolina, Charleston; and Department of Neurosurgery (S.S.G.), Straub Clinic & Hospital, Honolulu, HI.
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Joseph A. Helpern
From the Comprehensive Epilepsy Center, Department of Neurosciences (L.B., R.S., T.N., J.C.E.), Department of Radiology and Radiological Science (J.A.H., A.T.), and Center for Biomedical Imaging (L.B., J.A.H., A.T.), Medical University of South Carolina, Charleston; and Department of Neurosurgery (S.S.G.), Straub Clinic & Hospital, Honolulu, HI.
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Rup Sainju
From the Comprehensive Epilepsy Center, Department of Neurosciences (L.B., R.S., T.N., J.C.E.), Department of Radiology and Radiological Science (J.A.H., A.T.), and Center for Biomedical Imaging (L.B., J.A.H., A.T.), Medical University of South Carolina, Charleston; and Department of Neurosurgery (S.S.G.), Straub Clinic & Hospital, Honolulu, HI.
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Travis Nesland
From the Comprehensive Epilepsy Center, Department of Neurosciences (L.B., R.S., T.N., J.C.E.), Department of Radiology and Radiological Science (J.A.H., A.T.), and Center for Biomedical Imaging (L.B., J.A.H., A.T.), Medical University of South Carolina, Charleston; and Department of Neurosurgery (S.S.G.), Straub Clinic & Hospital, Honolulu, HI.
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Jonathan C. Edwards
From the Comprehensive Epilepsy Center, Department of Neurosciences (L.B., R.S., T.N., J.C.E.), Department of Radiology and Radiological Science (J.A.H., A.T.), and Center for Biomedical Imaging (L.B., J.A.H., A.T.), Medical University of South Carolina, Charleston; and Department of Neurosurgery (S.S.G.), Straub Clinic & Hospital, Honolulu, HI.
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Steven S. Glazier
From the Comprehensive Epilepsy Center, Department of Neurosciences (L.B., R.S., T.N., J.C.E.), Department of Radiology and Radiological Science (J.A.H., A.T.), and Center for Biomedical Imaging (L.B., J.A.H., A.T.), Medical University of South Carolina, Charleston; and Department of Neurosurgery (S.S.G.), Straub Clinic & Hospital, Honolulu, HI.
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Ali Tabesh
From the Comprehensive Epilepsy Center, Department of Neurosciences (L.B., R.S., T.N., J.C.E.), Department of Radiology and Radiological Science (J.A.H., A.T.), and Center for Biomedical Imaging (L.B., J.A.H., A.T.), Medical University of South Carolina, Charleston; and Department of Neurosurgery (S.S.G.), Straub Clinic & Hospital, Honolulu, HI.
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Citation
Presurgical connectome and postsurgical seizure control in temporal lobe epilepsy
Leonardo Bonilha, Joseph A. Helpern, Rup Sainju, Travis Nesland, Jonathan C. Edwards, Steven S. Glazier, Ali Tabesh
Neurology Nov 2013, 81 (19) 1704-1710; DOI: 10.1212/01.wnl.0000435306.95271.5f

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Abstract

Objectives: The objective of this study was to evaluate whether patients with surgically refractory medial temporal lobe epilepsy (MTLE) exhibit a distinct pattern of structural network organization involving the temporal lobes and extratemporal regions.

Methods: We retrospectively studied 18 healthy controls and 20 patients with medication refractory unilateral MTLE who underwent anterior temporal lobectomy for treatment of seizures. Patients were classified as seizure-free or not seizure-free at least 1 year after surgery. The presurgical brain connectome was calculated through probabilistic connectivity from MRI–diffusion tensor imaging from 83 anatomically defined regions of interest encompassing the whole brain. The connectivity patterns were analyzed regarding group differences in regional connectivity and network graph properties.

Results: Compared with controls, patients exhibited a decrease in connectivity involving ipsilateral thalamocortical regions, with a pathologic increase in ipsilateral medial temporal lobe, insular, and frontal connectivity. Among patients, those not seizure-free exhibited a higher connectivity between structures in 1) the ipsilateral medial and lateral temporal lobe, 2) the ipsilateral medial temporal and parietal lobe, and 3) the contralateral temporal pole and parietal lobe. Patients not seizure-free also exhibited lower small-worldness in the subnetwork within the ipsilateral temporal lobe, with higher subnetwork integration at the expense of segregation.

Conclusions: MTLE is associated with network rearrangement within, but not restricted to, the temporal lobe ipsilateral to the onset of seizures. Networks involving key components of the medial temporal lobe and structures traditionally not removed during surgery may be associated with seizure control after surgical treatment of MTLE.

GLOSSARY

DWI=
diffusion-weighted image;
FDT=
FMRIB's Diffusion Toolbox;
MTLE=
medial temporal lobe epilepsy;
MUSC=
Medical University of South Carolina;
ROI=
region of interest

Footnotes

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

  • Supplemental data at www.neurology.org

  • Received March 11, 2013.
  • Accepted in final form August 13, 2013.
  • © 2013 American Academy of Neurology
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