Brainstem Functional Connectivity Disturbances in Epilepsy may Recover After Successful Surgery

Hernán F J González; Sarah E Goodale; Monica L Jacobs; Kevin F Haas; Bennett A Landman; Victoria L Morgan; Dario J Englot

doi:10.1093/neuros/nyz128

Brainstem Functional Connectivity Disturbances in Epilepsy may Recover After Successful Surgery

Neurosurgery. 2020 Mar 1;86(3):417-428. doi: 10.1093/neuros/nyz128.

Authors

Hernán F J González^{1

2}, Sarah E Goodale^{1

2

3}, Monica L Jacobs^{4

5}, Kevin F Haas⁵, Bennett A Landman^{2

6

7

8}, Victoria L Morgan^{1

2

3

5

6

8}, Dario J Englot^{1

2

3

8}

Affiliations

¹ Department of Biomedical Engineering, Vanderbilt University, Nashville, Tennessee.
² Vanderbilt University Institute of Imaging Science, Vanderbilt University Medical center, Nashville, Tennessee.
³ Department of Neurological Surgery, Vanderbilt University Medical Center, Nashville, Tennessee.
⁴ Department of Psychiatry and Behavioral Sciences, Vanderbilt University Medical Center, Nashville, Tennessee.
⁵ Department of Neurology, Vanderbilt University Medical Center, Nashville, Tennessee.
⁶ Department of Electrical Engineering, Vanderbilt University, Nashville, Tennessee.
⁷ Department of Computer Science, Vanderbilt University, Nashville, Tennessee.
⁸ Department of Radiology and Radiological Sciences, Vanderbilt University Medical Center, Nashville, Tennessee.

Abstract

Background: Focal seizures in temporal lobe epilepsy (TLE) are associated with widespread brain network perturbations and neurocognitive problems.

Objective: To determine whether brainstem connectivity disturbances improve with successful epilepsy surgery, as recent work has demonstrated decreased brainstem connectivity in TLE that is related to disease severity and neurocognitive profile.

Methods: We evaluated 15 adult TLE patients before and after (>1 yr; mean, 3.4 yr) surgery, and 15 matched control subjects using magnetic resonance imaging to measure functional and structural connectivity of ascending reticular activating system (ARAS) structures, including cuneiform/subcuneiform nuclei (CSC), pedunculopontine nucleus (PPN), and ventral tegmental area (VTA).

Results: TLE patients who achieved long-term postoperative seizure freedom (10 of 15) demonstrated increases in functional connectivity between ARAS structures and fronto-parietal-insular neocortex compared to preoperative baseline (P = .01, Kruskal-Wallis), with postoperative connectivity patterns resembling controls' connectivity. No functional connectivity changes were detected in 5 patients with persistent seizures after surgery (P = .9, Kruskal-Wallis). Among seizure-free postoperative patients, larger increases in CSC, PPN, and VTA functional connectivity were observed in individuals with more frequent seizures before surgery (P < .05 for each, Spearman's rho). Larger postoperative increases in PPN functional connectivity were seen in patients with lower baseline verbal IQ (P = .03, Spearman's rho) or verbal memory (P = .04, Mann-Whitney U). No changes in ARAS structural connectivity were detected after successful surgery.

Conclusion: ARAS functional connectivity disturbances are present in TLE but may recover after successful epilepsy surgery. Larger increases in postoperative connectivity may be seen in individuals with more severe disease at baseline.

Keywords: Brainstem; Epilepsy surgery; Functional connectivity; Postoperative; Temporal lobe epilepsy.

Publication types

Research Support, N.I.H., Extramural

MeSH terms

Adult
Brain Stem / diagnostic imaging*
Epilepsy, Temporal Lobe / diagnostic imaging
Epilepsy, Temporal Lobe / surgery*
Female
Humans
Magnetic Resonance Imaging / methods
Male
Middle Aged
Nerve Net / diagnostic imaging
Nerve Net / surgery*
Postoperative Period
Recovery of Function / physiology*

Abstract

Publication types

MeSH terms

Grants and funding