Language network reorganization before and after temporal lobe epilepsy surgery

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  • 1 Departments of Biomedical Imaging and Image-guided Therapy,
  • 2 Neurology, and
  • 3 Pediatrics and Adolescent Medicine, Medical University of Vienna;
  • 4 General Hospital Hietzing with Neurological Center Rosenhuegel, Vienna; and
  • 5 Institute of Neurology and
  • 6 Department of Neurosurgery, Medical University of Vienna, Austria
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OBJECTIVE

Epilepsy surgery is the recommended treatment option for patients with drug-resistant temporal lobe epilepsy (TLE). This method offers a good chance of seizure freedom but carries a considerable risk of postoperative language impairment. The extremely variable neurocognitive profiles in surgical epilepsy patients cannot be fully explained by extent of resection, fiber integrity, or current task-based functional MRI (fMRI). In this study, the authors aimed to investigate pathology- and surgery-triggered language organization in TLE by using fMRI activation and network analysis as well as considering structural and neuropsychological measures.

METHODS

Twenty-eight patients with unilateral TLE (16 right, 12 left) underwent T1-weighted imaging, diffusion tensor imaging, and task-based language fMRI pre- and postoperatively (n = 15 anterior temporal lobectomy, n = 11 selective amygdalohippocampectomy, n = 2 focal resection). Twenty-two healthy subjects served as the control cohort. Functional connectivity, activation maps, and laterality indices for language dominance were analyzed from fMRI data. Postoperative fractional anisotropy values of 7 major tracts were calculated. Naming, semantic, and phonematic verbal fluency scores before and after surgery were correlated with imaging parameters.

RESULTS

fMRI network analysis revealed widespread, bihemispheric alterations in language architecture that were not captured by activation analysis. These network changes were found preoperatively and proceeded after surgery with characteristic patterns in the left and right TLEs. Ipsilesional fronto-temporal connectivity decreased in both left and right TLE. In left TLE specifically, preoperative atypical language dominance predicted better postoperative verbal fluency and naming function. In right TLE, left frontal language dominance correlated with good semantic verbal fluency before and after surgery, and left fronto-temporal language laterality predicted good naming outcome. Ongoing seizures after surgery (Engel classes ID–IV) were associated with naming deterioration irrespective of seizure side. Functional findings were not explained by the extent of resection or integrity of major white matter tracts.

CONCLUSIONS

Functional connectivity analysis contributes unique insight into bihemispheric remodeling processes of language networks after epilepsy surgery, with characteristic findings in left and right TLE. Presurgical contralateral language recruitment is associated with better postsurgical language outcome in left and right TLE.

ABBREVIATIONS ATL = anterior temporal lobectomy; DTI = diffusion tensor imaging; FA = fractional anisotropy; FC = functional connectivity; fMRI = functional MRI; IFG = inferior frontal gyrus; LI = laterality index; p uncorr = uncorrected p value; ROI = region of interest; SAH = selective amygdalohippocampectomy; TLE = temporal lobe epilepsy; T1WI = T1-weighted imaging.

Supplementary Materials

    • Supplementary Methods and Tables (PDF 565 KB)

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Contributor Notes

Correspondence Gregor Kasprian: Medical University of Vienna, Austria. gregor.kasprian@meduniwien.ac.at.

INCLUDE WHEN CITING Published online July 3, 2020; DOI: 10.3171/2020.4.JNS193401.

Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

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