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Research paper
Thalamic arousal network disturbances in temporal lobe epilepsy and improvement after surgery
  1. Hernán F J González1,2,
  2. Srijata Chakravorti3,
  3. Sarah E Goodale1,2,
  4. Kanupriya Gupta2,4,
  5. Daniel O Claassen5,
  6. Benoit Dawant2,6,
  7. Victoria L Morgan1,2,7,
  8. Dario J Englot1,2,4
  1. 1 Department of Biomedical Engineering, Vanderbilt University, Nashville, Tennessee, USA
  2. 2 Vanderbilt University Institute of Imaging Science, Department of Radiology and Radiological Sciences, Vanderbilt University Medical Center, Nashville, Tennessee, USA
  3. 3 Department of Electrical Engineering and Computer Science, Vanderbilt University, Nashville, Tennessee, USA
  4. 4 Department of Neurological Surgery, Vanderbilt University Medical Center, Nashville, Tennessee, USA
  5. 5 Department of Neurology, Vanderbilt University Medical Center, Nashville, Tennessee, USA
  6. 6 Department of Biomedical Engineering, Vanderbilt University, Nashville, Tennessee, USA
  7. 7 Department of Radiology and Radiological Sciences, Vanderbilt University Medical Center, Nashville, Tennessee, USA
  1. Correspondence to Hernán F J González, Biomedical Engineering, Vanderbilt University, Nashville, Tennessee 37212, USA; hfjgonzalez{at}gmail.com

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.

  • temporal lobe epilepsy
  • epilepsy surgery
  • functional neuroimaging
  • partial seizures
  • functional connectivity

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Footnotes

  • Contributors Data were primarily collected by HFJG, SEG, KG, VLM and DJE. Data analysis was conducted by HFJG, SC, BMD, VLM and DJE. HFJG produced the first draft of the manuscript. All authors read, provided input and approved the final manuscript.

  • Funding Supported by NIH R00 NS097618 (DJE), R01 NS095291 (BMD), R01 NS0757270 (VLM), R01 NS110130 (VLM), T32 EB021937 (HFJG), T32 GM07347 (HFJG), F31 NS106735 (HFJG), and the Vanderbilt Institute for Surgery and Engineering (VISE).

  • Competing interests None declared.

  • Patient consent for publication Not required.

  • Ethics approval Vanderbilt University Institutional Review Board (IRB# 170560).

  • Provenance and peer review Not commissioned; externally peer reviewed.

  • Data availability statement Data are available upon reasonable request.

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