Degenerate time-dependent network dynamics anticipate seizures in human epileptic brain

Adrià Tauste Campo; Alessandro Principe; Miguel Ley; Rodrigo Rocamora; Gustavo Deco

doi:10.1371/journal.pbio.2002580

Degenerate time-dependent network dynamics anticipate seizures in human epileptic brain

PLoS Biol. 2018 Apr 5;16(4):e2002580. doi: 10.1371/journal.pbio.2002580. eCollection 2018 Apr.

Authors

Adrià Tauste Campo^{1

2}, Alessandro Principe^{2

3}, Miguel Ley², Rodrigo Rocamora^{2

3}, Gustavo Deco^{1

4}

Affiliations

¹ Center for Brain and Cognition, Department of Information and Communication Technologies, Universitat Pompeu Fabra, Barcelona, Spain.
² Epilepsy Unit, Department of Neurology, Hospital del Mar-Hospital del Mar Medical Research Institute (IMIM), Barcelona, Spain.
³ Faculty of Health and Life Sciences, Universitat Pompeu Fabra, Barcelona, Spain.
⁴ Institució Catalana de Recerca i Estudis Avançats (ICREA), Barcelona, Spain.

Abstract

Epileptic seizures are known to follow specific changes in brain dynamics. While some algorithms can nowadays robustly detect these changes, a clear understanding of the mechanism by which these alterations occur and generate seizures is still lacking. Here, we provide crossvalidated evidence that such changes are initiated by an alteration of physiological network state dynamics. Specifically, our analysis of long intracranial electroencephalography (iEEG) recordings from a group of 10 patients identifies a critical phase of a few hours in which time-dependent network states become less variable ("degenerate"), and this phase is followed by a global functional connectivity reduction before seizure onset. This critical phase is characterized by an abnormal occurrence of highly correlated network instances and is shown to be particularly associated with the activity of the resected regions in patients with validated postsurgical outcome. Our approach characterizes preseizure network dynamics as a cascade of 2 sequential events providing new insights into seizure prediction and control.

Publication types

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

MeSH terms

Adult
Algorithms
Brain / diagnostic imaging
Brain / pathology
Brain / physiopathology*
Brain / surgery
Connectome
Electrocorticography
Female
Follow-Up Studies
Humans
Male
Middle Aged
Nerve Net / diagnostic imaging
Nerve Net / pathology
Nerve Net / physiopathology*
Nerve Net / surgery
Prognosis
Seizures / diagnostic imaging
Seizures / pathology
Seizures / physiopathology*
Seizures / surgery
Time Factors

Grants and funding

European Community’s Seventh Framework Programme (FP7/2007-2013) https://ec.europa.eu/research/mariecurieactions/ (grant number PEOPLE- 2012-IEF-329837). ATC was supported by this source of funding. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. European Research Council https://erc.europa.eu/ (grant number ERC-2011-ADG-295129). GD was supported by this source of funding. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Ministerio de Economía y Competitividad (grant number PSI2016-75688-P). ATC and GD were supported by this source of funding. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Horizon 2020 FET Flagship Human Brain Project http://ec.europa.eu/programmes/horizon2020/en/h2020-section/fet-flagships (grant number 720270 HBP SGA1). GD was supported by this source of funding. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.