Controlling seizure propagation in large-scale brain networks

PLoS Comput Biol. 2019 Feb 25;15(2):e1006805. doi: 10.1371/journal.pcbi.1006805. eCollection 2019 Feb.

Abstract

Information transmission in the human brain is a fundamentally dynamic network process. In partial epilepsy, this process is perturbed and highly synchronous seizures originate in a local network, the so-called epileptogenic zone (EZ), before recruiting other close or distant brain regions. We studied patient-specific brain network models of 15 drug-resistant epilepsy patients with implanted stereotactic electroencephalography (SEEG) electrodes. Each personalized brain model was derived from structural data of magnetic resonance imaging (MRI) and diffusion tensor weighted imaging (DTI), comprising 88 nodes equipped with region specific neural mass models capable of demonstrating a range of epileptiform discharges. Each patient's virtual brain was further personalized through the integration of the clinically hypothesized EZ. Subsequent simulations and connectivity modulations were performed and uncovered a finite repertoire of seizure propagation patterns. Across patients, we found that (i) patient-specific network connectivity is predictive for the subsequent seizure propagation pattern; (ii) seizure propagation is characterized by a systematic sequence of brain states; (iii) propagation can be controlled by an optimal intervention on the connectivity matrix; (iv) the degree of invasiveness can be significantly reduced via the proposed seizure control as compared to traditional resective surgery. To stop seizures, neurosurgeons typically resect the EZ completely. We showed that stability analysis of the network dynamics, employing structural and dynamical information, estimates reliably the spatiotemporal properties of seizure propagation. This suggests novel less invasive paradigms of surgical interventions to treat and manage partial epilepsy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Brain / physiology*
  • Brain Mapping
  • Computer Simulation
  • Electrodes, Implanted
  • Electroencephalography
  • Epilepsies, Partial / physiopathology
  • Female
  • Humans
  • Imaging, Three-Dimensional
  • Magnetic Resonance Imaging
  • Male
  • Middle Aged
  • Nerve Net / physiology*
  • Seizures / physiopathology*
  • Signal Processing, Computer-Assisted

Grants and funding

This work was partially supported by The Short Term Mobility Program founded by the Italian National Research Council (protocol number 0057676, date 31/08/2015). This work was further supported by the FHU EPINEXT [A*MIDEX project (ANR-11-IDEX-0001-02) funded by the ‘Investissements d’Avenir’ French Government] and the European Union’s Horizon 2020 research and innovation programme under grant agreement No. 720270. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.