Presurgical thalamic “hubness” predicts surgical outcome in temporal lobe epilepsy
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Abstract
Objective: To characterize the presurgical brain functional architecture presented in patients with temporal lobe epilepsy (TLE) using graph theoretical measures of resting-state fMRI data and to test its association with surgical outcome.
Methods: Fifty-six unilateral patients with TLE, who subsequently underwent anterior temporal lobectomy and were classified as obtaining a seizure-free (Engel class I, n = 35) vs not seizure-free (Engel classes II–IV, n = 21) outcome at 1 year after surgery, and 28 matched healthy controls were enrolled. On the basis of their presurgical resting-state functional connectivity, network properties, including nodal hubness (importance of a node to the network; degree, betweenness, and eigenvector centralities) and integration (global efficiency), were estimated and compared across our experimental groups. Cross-validations with support vector machine (SVM) were used to examine whether selective nodal hubness exceeded standard clinical characteristics in outcome prediction.
Results: Compared to the seizure-free patients and healthy controls, the not seizure-free patients displayed a specific increase in nodal hubness (degree and eigenvector centralities) involving both the ipsilateral and contralateral thalami, contributed by an increase in the number of connections to regions distributed mostly in the contralateral hemisphere. Simulating removal of thalamus reduced network integration more dramatically in not seizure-free patients. Lastly, SVM models built on these thalamic hubness measures produced 76% prediction accuracy, while models built with standard clinical variables yielded only 58% accuracy (both were cross-validated).
Conclusions: A thalamic network associated with seizure recurrence may already be established presurgically. Thalamic hubness can serve as a potential biomarker of surgical outcome, outperforming the clinical characteristics commonly used in epilepsy surgery centers.
GLOSSARY
- ATL=
- anterior temporal lobectomy;
- BC=
- betweenness centrality;
- DC=
- degree centrality;
- DSM-IV=
- Diagnostic and Statistical Manual of Mental Disorders, 4th edition;
- EC=
- eigenvector centrality;
- Eglobal=
- global efficiency;
- FDR=
- false discovery rate;
- HC=
- healthy control;
- MST=
- minimum spanning tree;
- NSF=
- not seizure-free;
- rsFC=
- resting-state functional connectivity;
- rsfMRI=
- resting-state fMRI;
- SANTE=
- Stimulation of the Anterior Nucleus of Thalamus for Epilepsy;
- SF=
- seizure-free;
- SVM=
- support vector machine;
- TLE=
- temporal lobe epilepsy
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 Neurology.org
Editorial, page 2246
- Received October 26, 2016.
- Accepted in final form March 14, 2017.
- © 2017 American Academy of Neurology
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