Data-driven method to infer the seizure propagation patterns in an epileptic brain from intracranial electroencephalography

PLoS Comput Biol. 2021 Feb 17;17(2):e1008689. doi: 10.1371/journal.pcbi.1008689. eCollection 2021 Feb.

Abstract

Surgical interventions in epileptic patients aimed at the removal of the epileptogenic zone have success rates at only 60-70%. This failure can be partly attributed to the insufficient spatial sampling by the implanted intracranial electrodes during the clinical evaluation, leading to an incomplete picture of spatio-temporal seizure organization in the regions that are not directly observed. Utilizing the partial observations of the seizure spreading through the brain network, complemented by the assumption that the epileptic seizures spread along the structural connections, we infer if and when are the unobserved regions recruited in the seizure. To this end we introduce a data-driven model of seizure recruitment and propagation across a weighted network, which we invert using the Bayesian inference framework. Using a leave-one-out cross-validation scheme on a cohort of 45 patients we demonstrate that the method can improve the predictions of the states of the unobserved regions compared to an empirical estimate that does not use the structural information, yet it is on the same level as the estimate that takes the structure into account. Furthermore, a comparison with the performed surgical resection and the surgery outcome indicates a link between the inferred excitable regions and the actual epileptogenic zone. The results emphasize the importance of the structural connectome in the large-scale spatio-temporal organization of epileptic seizures and introduce a novel way to integrate the patient-specific connectome and intracranial seizure recordings in a whole-brain computational model of seizure spread.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bayes Theorem
  • Brain / diagnostic imaging*
  • Brain Mapping / methods
  • Computer Simulation
  • Electrocorticography / methods*
  • Electrodes
  • Electrodes, Implanted
  • Humans
  • Magnetic Resonance Imaging
  • Models, Neurological
  • Models, Statistical
  • Nerve Net
  • Predictive Value of Tests
  • Reproducibility of Results
  • Seizures / physiopathology*
  • Seizures / surgery
  • Treatment Outcome

Grants and funding

This work was funded by the French National Research Agency (ANR) as part of the second “Investissements d’Avenir” program, ANR-17-RHUS-0004, EPINOV (https://anr.fr) to VJ, FB, and MG, by European Union’s Horizon 2020 Framework Programme for Research and Innovation under the Specific Grant Agreement No. 785907 and 945539, Human Brain Project SGA2 and SGA3 (https://ec.europa.eu/programmes/horizon2020) to VJ, by European Union’s Horizon 2020 Framework Programme for Research and Innovation under the Specific Grant Agreement and No. 826421, VirtualBrainCloud (https://ec.europa.eu/programmes/horizon2020) to VJ, and by SATT Sud-Est, 827-SA-16-UAM (https://www.sattse.com) to VJ, FB, and MG. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.