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Contribution of White Matter Fiber Bundle Damage to Language Change After Surgery for Temporal Lobe Epilepsy

Binding, Lawrence Peter; Dasgupta, Debayan; Taylor, Peter Neal; Thompson, Pamela Jane; O'Keeffe, Aidan G; de Tisi, Jane; McEvoy, Andrew William; ... Vos, Sjoerd B; + view all (2023) Contribution of White Matter Fiber Bundle Damage to Language Change After Surgery for Temporal Lobe Epilepsy. Neurology , 100 (15) e1621-e1633. 10.1212/WNL.0000000000206862. Green open access

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Abstract

BACKGROUND AND OBJECTIVES: In medically refractory temporal lobe epilepsy (TLE), 30-50% of patients experience substantial language decline following resection in the language dominant hemisphere. Here, we investigate the contribution of white matter fiber bundle damage to language change at 3- and 12-months after surgery. METHODS: We studied 127 patients who underwent TLE surgery from 2010-2019. Neuropsychological testing included picture naming, semantic, and phonemic verbal fluency, performed pre-operatively, 3- and 12-months post-operatively. Outcome was assessed using reliable change index (RCI; clinically significant decline) and change across timepoints (post- minus pre-operative scores).Functional MRI was used to determine language lateralization. The arcuate (AF), inferior fronto-occipital (IFOF), inferior longitudinal, middle longitudinal (MLF), and uncinate fasciculi were mapped using diffusion MRI probabilistic tractography. Resection masks, drawn comparing co-registered pre- and post-operative T1 MRI scans, were used as exclusion regions on pre-operative tractography to estimate the percentage of pre-operative tracts transected in surgery. Chi-squared assessments evaluated the occurrence of RCI-determined language decline. Independent samples T-tests and MM-estimator robust regressions were used to assess the impact of clinical factors and fiber transection on RCI and change outcomes, respectively. RESULTS: Language dominant and non-dominant resections were treated separately for picture naming, as post-operative outcomes were significantly different between these groups. In language dominant hemisphere resections, greater surgical damage to the AF and IFOF was related to RCI-decline at 3 months. Damage to the inferior frontal sub-fasciculus of the IFOF was related to change at 3 months. In language non-dominant hemisphere resections, increased MLF resection was associated with RCI-decline at 3 months, and damage to the anterior sub-fasciculus was related to change at 3 months.Language dominant and non-dominant resections were treated as one cohort for semantic and phonemic fluency, as there were no significant differences in post-operative decline between these groups. Post-operative seizure freedom was associated with an absence of significant language decline 12 months after surgery for semantic fluency. DISCUSSION: We demonstrate a relationship between fiber transection and naming decline after temporal lobe resection. Individualized surgical planning to spare white matter fiber bundles could help to preserve language function after surgery.

Type: Article
Title: Contribution of White Matter Fiber Bundle Damage to Language Change After Surgery for Temporal Lobe Epilepsy
Location: United States
Open access status: An open access version is available from UCL Discovery
DOI: 10.1212/WNL.0000000000206862
Publisher version: https://doi.org/10.1212/WNL.0000000000206862
Language: English
Additional information: This is an open access article distributed under the terms of the Creative Commons Attribution License 4.0 (CC BY), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
UCL classification: UCL
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences
UCL > Provost and Vice Provost Offices > UCL BEAMS
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences
UCL > Provost and Vice Provost Offices > UCL BEAMS > Faculty of Engineering Science
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences > UCL Queen Square Institute of Neurology
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences > UCL Queen Square Institute of Neurology > Clinical and Experimental Epilepsy
UCL > Provost and Vice Provost Offices > UCL BEAMS > Faculty of Engineering Science > Dept of Computer Science
UCL > Provost and Vice Provost Offices > UCL BEAMS > Faculty of Engineering Science > Dept of Med Phys and Biomedical Eng
URI: https://discovery.ucl.ac.uk/id/eprint/10164651
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