Progressive remodeling of structural networks following surgery for operculo-insular epilepsy

Sami Obaid; Guido I Guberman; Etienne St-Onge; Emma Campbell; Manon Edde; Layton Lamsam; Alain Bouthillier; Alexander G Weil; Alessandro Daducci; François Rheault; Dang K Nguyen; Maxime Descoteaux

doi:10.3389/fneur.2024.1400601

Progressive remodeling of structural networks following surgery for operculo-insular epilepsy

Front Neurol. 2024 Jul 31:15:1400601. doi: 10.3389/fneur.2024.1400601. eCollection 2024.

Authors

Sami Obaid^{1

2

3

4}, Guido I Guberman⁵, Etienne St-Onge⁶, Emma Campbell⁷, Manon Edde⁴, Layton Lamsam⁸, Alain Bouthillier³, Alexander G Weil^{1

9}, Alessandro Daducci¹⁰, François Rheault¹¹, Dang K Nguyen^{1

2

12}, Maxime Descoteaux⁴

Affiliations

¹ Department of Neurosciences, University of Montreal, Montreal, QC, Canada.
² University of Montreal Hospital Research Center (CRCHUM), Montreal, QC, Canada.
³ Division of Neurosurgery, Department of Surgery, University of Montreal Hospital Center (CHUM), Montreal, QC, Canada.
⁴ Sherbrooke Connectivity Imaging Lab (SCIL), Sherbrooke University, Sherbrooke, QC, Canada.
⁵ Department of Neurology and Neurosurgery, Faculty of Medicine, McGill University, Montreal, QC, Canada.
⁶ Department of Computer Science and Engineering, Université du Québec en Outaouais, Montreal, QC, Canada.
⁷ Department of Psychology, University of Montreal, Montreal, QC, Canada.
⁸ Department of Neurosurgery, Yale School of Medicine, Yale University, New Haven, CT, United States.
⁹ Division of Pediatric Neurosurgery, Department of Surgery, Sainte Justine Hospital, University of Montreal, Montreal, QC, Canada.
¹⁰ Department of Computer Science, University of Verona, Verona, Italy.
¹¹ Medical Imaging and Neuroimaging (MINi) Lab, Sherbrooke University, Sherbrooke, QC, Canada.
¹² Division of Neurology, University of Montreal Hospital Center (CHUM), Montreal, QC, Canada.

Abstract

Introduction: Operculo-insular epilepsy (OIE) is a rare condition amenable to surgery in well-selected cases. Despite the high rate of neurological complications associated with OIE surgery, most postoperative deficits recover fully and rapidly. We provide insights into this peculiar pattern of functional recovery by investigating the longitudinal reorganization of structural networks after surgery for OIE in 10 patients.

Methods: Structural T1 and diffusion-weighted MRIs were performed before surgery (t₀) and at 6 months (t₁) and 12 months (t₂) postoperatively. These images were processed with an original, comprehensive structural connectivity pipeline. Using our method, we performed comparisons between the t₀ and t₁ timepoints and between the t₁ and t₂ timepoints to characterize the progressive structural remodeling.

Results: We found a widespread pattern of postoperative changes primarily in the surgical hemisphere, most of which consisted of reductions in connectivity strength (CS) and regional graph theoretic measures (rGTM) that reflect local connectivity. We also observed increases in CS and rGTMs predominantly in regions located near the resection cavity and in the contralateral healthy hemisphere. Finally, most structural changes arose in the first six months following surgery (i.e., between t₀ and t₁).

Discussion: To our knowledge, this study provides the first description of postoperative structural connectivity changes following surgery for OIE. The ipsilateral reductions in connectivity unveiled by our analysis may result from the reversal of seizure-related structural alterations following postoperative seizure control. Moreover, the strengthening of connections in peri-resection areas and in the contralateral hemisphere may be compatible with compensatory structural plasticity, a process that could contribute to the recovery of functions seen following operculo-insular resections for focal epilepsy.

Keywords: connectome; epilepsy; epilepsy surgery; insula; plasticity; tractography.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This research was funded by the Quebec Bio-Imaging Network (5886), the Canadian Institute of Health Research (MOP-BSC343410-97930-DLGNH), the Natural Sciences and Engineering Research Council of Canada (RGPIN-2016-05216N) and the Université de Sherbrooke Institutional Chair in Neuroinformatics. The main author was awarded the Savoy Foundation studentship, the Quebec Bio-Imaging Network postdoctoral scholarship and various Fonds de Recherche du Québec -Santé scholarships (277581 and 313244) and grants (325293). These funding sources had no involvement in the study design, in the collection, analysis and interpretation of data, in the writing of the report or in the decision to submit the article for publication.