Thalamic arousal network disturbances in temporal lobe epilepsy and improvement after surgery

J Neurol Neurosurg Psychiatry. 2019 Oct;90(10):1109-1116. doi: 10.1136/jnnp-2019-320748. Epub 2019 May 23.

Abstract

Objective: The effects of temporal lobe epilepsy (TLE) on subcortical arousal structures remain incompletely understood. Here, we evaluate thalamic arousal network functional connectivity in TLE and examine changes after epilepsy surgery.

Methods: We examined 26 adult patients with TLE and 26 matched control participants and used resting-state functional MRI (fMRI) to measure functional connectivity between the thalamus (entire thalamus and 19 bilateral thalamic nuclei) and both neocortex and brainstem ascending reticular activating system (ARAS) nuclei. Postoperative imaging was completed for 19 patients >1 year after surgery and compared with preoperative baseline.

Results: Before surgery, patients with TLE demonstrated abnormal thalamo-occipital functional connectivity, losing the normal negative fMRI correlation between the intralaminar central lateral (CL) nucleus and medial occipital lobe seen in controls (p < 0.001, paired t-test). Patients also had abnormal connectivity between ARAS and CL, lower ipsilateral intrathalamic connectivity, and smaller ipsilateral thalamic volume compared with controls (p < 0.05 for each, paired t-tests). Abnormal brainstem-thalamic connectivity was associated with impaired visuospatial attention (ρ = -0.50, p = 0.02, Spearman's rho) while lower intrathalamic connectivity and volume were related to higher frequency of consciousness-sparing seizures (p < 0.02, Spearman's rho). After epilepsy surgery, patients with improved seizures showed partial recovery of thalamo-occipital and brainstem-thalamic connectivity, with values more closely resembling controls (p < 0.01 for each, analysis of variance).

Conclusions: Overall, patients with TLE demonstrate impaired connectivity in thalamic arousal networks that may be involved in visuospatial attention, but these disturbances may partially recover after successful epilepsy surgery. Thalamic arousal network dysfunction may contribute to morbidity in TLE.

Keywords: epilepsy surgery; functional connectivity; functional neuroimaging; partial seizures; temporal lobe epilepsy.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Arousal / physiology*
  • Brain Stem / diagnostic imaging*
  • Brain Stem / physiopathology
  • Case-Control Studies
  • Epilepsy, Temporal Lobe / diagnostic imaging*
  • Epilepsy, Temporal Lobe / physiopathology
  • Epilepsy, Temporal Lobe / surgery
  • Female
  • Functional Neuroimaging
  • Humans
  • Magnetic Resonance Imaging
  • Male
  • Middle Aged
  • Neocortex / diagnostic imaging*
  • Neocortex / physiopathology
  • Neural Pathways / diagnostic imaging
  • Neural Pathways / physiopathology
  • Neurosurgical Procedures
  • Thalamic Nuclei / diagnostic imaging*
  • Thalamic Nuclei / physiopathology
  • Thalamus / diagnostic imaging
  • Thalamus / physiopathology