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A Systems-Level Approach to Human Epileptic Seizures

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Abstract

Epileptic seizures are due to the pathological collective activity of large cellular assemblies. A better understanding of this collective activity is integral to the development of novel diagnostic and therapeutic procedures. In contrast to reductionist analyses, which focus solely on small-scale characteristics of ictogenesis, here we follow a systems-level approach, which combines both small-scale and larger-scale analyses. Peri-ictal dynamics of epileptic networks are assessed by studying correlation within and between different spatial scales of intracranial electroencephalographic recordings (iEEG) of a heterogeneous group of patients suffering from pharmaco-resistant epilepsy. Epileptiform activity as recorded by a single iEEG electrode is determined objectively by the signal derivative and then subjected to a multivariate analysis of correlation between all iEEG channels. We find that during seizure, synchrony increases on the smallest and largest spatial scales probed by iEEG. In addition, a dynamic reorganization of spatial correlation is observed on intermediate scales, which persists after seizure termination. It is proposed that this reorganization may indicate a balancing mechanism that decreases high local correlation. Our findings are consistent with the hypothesis that during epileptic seizures hypercorrelated and therefore functionally segregated brain areas are re-integrated into more collective brain dynamics. In addition, except for a special sub-group, a highly significant association is found between the location of ictal iEEG activity and the location of areas of relative decrease of localised EEG correlation. The latter could serve as a clinically important quantitative marker of the seizure onset zone (SOZ).

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Abbreviations

CC:

equal-time cross-correlation

EEG:

electroencephalogram

FLE:

frontal lobe epilepsy

Fo:

foramen ovale

iEEG:

intracranial electroencephalogram

MRI:

magnetic resonance imaging

PLE:

parietal lobe epilepsy

TCS:

total correlation strength

TLE:

temporal lobe epilepsy

SCC:

slope cross-correlation

SOZ:

seizure onset zone

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Acknowledgments

C.R. and K.S. thank Markus Müller for fruitful discussions. This work was supported by Deutsche Forschungsgemeinschaft, Germany (grant RU 1401/2-1) and Schweizerischer Nationalfonds, Switzerland (projects 320030-122010 and 33CM30-124089). M.G. acknowledges financial support from the EPSRC and BBSRC (UK).

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Rummel, C., Goodfellow, M., Gast, H. et al. A Systems-Level Approach to Human Epileptic Seizures. Neuroinform 11, 159–173 (2013). https://doi.org/10.1007/s12021-012-9161-2

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