Structure-function coupling increases during interictal spikes in temporal lobe epilepsy: A graph signal processing study

I Rigoni; J Rué Queralt; K Glomb; M G Preti; N Roehri; S Tourbier; L Spinelli; M Seeck; D Van De Ville; P Hagmann; S Vulliémoz

doi:10.1016/j.clinph.2023.05.012

Structure-function coupling increases during interictal spikes in temporal lobe epilepsy: A graph signal processing study

Clin Neurophysiol. 2023 Sep:153:1-10. doi: 10.1016/j.clinph.2023.05.012. Epub 2023 Jun 15.

Authors

I Rigoni¹, J Rué Queralt², K Glomb³, M G Preti⁴, N Roehri⁵, S Tourbier², L Spinelli⁵, M Seeck⁵, D Van De Ville⁶, P Hagmann², S Vulliémoz⁵

Affiliations

¹ EEG and Epilepsy Unit, University Hospital and Faculty of Medicine of Geneva, University of Geneva, Switzerland. Electronic address: isotta.rigoni@unige.ch.
² Department of Radiology, Lausanne University Hospital and University of Lausanne (CHUV-UNIL), Switzerland.
³ Brain Simulation Section, Berlin Institute of Health/Charite, 10098 Berlin, Germany.
⁴ Neuro-X Institute, School of Engineering, Ecole polytechnique fédérale de Lausanne, Geneva, Switzerland; Department of Radiology and Medical Informatics, Faculty of Medicine, University of Geneva, Geneva, Switzerland; CIBM Center for Biomedical Imaging, Switzerland.
⁵ EEG and Epilepsy Unit, University Hospital and Faculty of Medicine of Geneva, University of Geneva, Switzerland.
⁶ Neuro-X Institute, School of Engineering, Ecole polytechnique fédérale de Lausanne, Geneva, Switzerland; Department of Radiology and Medical Informatics, Faculty of Medicine, University of Geneva, Geneva, Switzerland.

PMID: 37364402
DOI: 10.1016/j.clinph.2023.05.012

Abstract

Objective: Structure-function coupling remains largely unknown in brain disorders. We studied this coupling during interictal epileptic discharges (IEDs), using graph signal processing in temporal lobe epilepsy (TLE).

Methods: We decomposed IEDs of 17 patients on spatial maps, i.e. network harmonics, extracted from a structural connectome. Harmonics were split in smooth maps (long-range interactions reflecting integration) and coarse maps (short-range interactions reflecting segregation) and were used to reconstruct the part of the signal coupled (Xc) and decoupled (Xd) from the structure, respectively. We analysed how Xc and Xd embed the IED energy over time, at global and regional level.

Results: For Xc, the energy was smaller than for Xd before the IED onset (p < .001), but became larger around the first IED peak (p < .05, cluster 2, C2). Locally, the ipsilateral mesial regions were significantly coupled to the structure over the whole epoch. The ipsilateral hippocampus increased its coupling during C2 (p < .01).

Conclusions: At whole-brain level, segregation gives way to integrative processes during the IED. Locally, brain regions commonly involved in the TLE epileptogenic network increase their reliance on long-range couplings during IED (C2).

Significance: In TLE, integration mechanisms prevail during the IED and are localized in the ipsilateral mesial temporal regions.

Keywords: EEG; Graph signal processing; Structure–function coupling; Temporal lobe epilepsy.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Brain
Electroencephalography
Epilepsy*
Epilepsy, Temporal Lobe*
Humans
Magnetic Resonance Imaging
Temporal Lobe