Decoupling of functional and structural language networks in temporal lobe epilepsy

Karin Trimmel*, Sjoerd B. Vos, Lorenzo Caciagli, Fenglai Xiao, Louis A. van Graan, Gavin P. Winston, Matthias J. Koepp, Pamela J. Thompson, John S. Duncan

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

Abstract

Objective: To identify functional and structural alterations in language networks of people with temporal lobe epilepsy (TLE), who frequently present with naming and word-finding difficulties. Methods: Fifty-five patients with unilateral TLE (29 left) and 16 controls were studied with auditory and picture naming functional magnetic resonance imaging (fMRI) tasks. Activation maxima in the left posterobasal temporal lobe were used as seed regions for whole-brain functional connectivity analyses (psychophysiological interaction). White matter language pathways were investigated using diffusion tensor imaging and neurite orientation dispersion and density imaging metrics extracted along fiber bundles starting from fMRI-guided seeds. Regression analyses were performed to investigate the correlation of functional connectivity with diffusion MRI metrics. Results: In the whole group of patients and controls, weaker functional connectivity from the left posterobasal temporal lobe (1) to the bilateral anterior temporal lobe, precentral gyrus, and lingual gyrus during auditory naming and (2) to the bilateral occipital cortex and right fusiform gyrus during picture naming was associated with decreased neurite orientation dispersion and higher free water fraction of white matter tracts. Compared to controls, TLE patients exhibited fewer structural connections and an impaired coupling of functional and structural metrics. Significance: TLE is associated with an impairment and decoupling of functional and structural language networks. White matter damage, as evidenced by diffusion abnormalities, may contribute to impaired functional connectivity and language dysfunction in TLE.

Original languageEnglish
JournalEpilepsia
DOIs
Publication statusAccepted/In press - 2021
Externally publishedYes

Bibliographical note

Funding Information:
We thank Monika Czech for helping with patient recruitment; the radiographers at the Epilepsy Society, Jane Burdett and Andrea Hill; and all our participants and our colleagues for their enthusiastic cooperation. This study was supported by the National Institute for Health Research University College London Hospitals Biomedical Research Centre. We are grateful to the Wolfson Foundation and the Epilepsy Society for supporting the Epilepsy Society MRI scanner; and the European Academy of Neurology and Austrian Society of Neurology, which each supported KT with a 1‐year fellowship. L.C. acknowledges support from a PhD scholarship by Brain Research UK (award 14181). G.P.W. was funded by the Medical Research Council (G0802012, MR/M00841X/1). This work was supported by Epilepsy Research UK (grant number P1904).

Publisher Copyright:
© 2021 The Authors. Epilepsia published by Wiley Periodicals LLC on behalf of International League Against Epilepsy

Keywords

  • DTI
  • NODDI
  • diffusion MRI
  • functional connectivity
  • language network
  • naming function
  • temporal lobe epilepsy

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