Domino-like transient dynamics at seizure onset in epilepsy
Open Access
- 28 September 2020
- journal article
- research article
- Published by Public Library of Science (PLoS) in PLOS Computational Biology
- Vol. 16 (9) , e1008206
Abstract
The International League Against Epilepsy (ILAE) groups seizures into “focal”, “generalized” and “unknown” based on whether the seizure onset is confined to a brain region in one hemisphere, arises in several brain region simultaneously, or is not known, respectively. This separation fails to account for the rich diversity of clinically and experimentally observed spatiotemporal patterns of seizure onset and even less so for the properties of the brain networks generating them. We consider three different patterns of domino-like seizure onset in Idiopathic Generalized Epilepsy (IGE) and present a novel approach to classification of seizures. To understand how these patterns are generated on networks requires understanding of the relationship between intrinsic node dynamics and coupling between nodes in the presence of noise, which currently is unknown. We investigate this interplay here in the framework of domino-like recruitment across a network. In particular, we use a phenomenological model of seizure onset with heterogeneous coupling and node properties, and show that in combination they generate a range of domino-like onset patterns observed in the IGE seizures. We further explore the individual contribution of heterogeneous node dynamics and coupling by interpreting in-vitro experimental data in which the speed of onset can be chemically modulated. This work contributes to a better understanding of possible drivers for the spatiotemporal patterns observed at seizure onset and may ultimately contribute to a more personalized approach to classification of seizure types in clinical practice. Epilepsy is a serious neurological condition encompassing a variety of syndromes that affect around 65 million people worldwide. Seizure type in epilepsy is characterized by onset pattern and brain network involved into three categories that do not fully capture the complexity of observed onset patterns. Ambiguity of seizure onset observed in the clinic could result in significant diagnostic delay and inappropriate treatment for an individual. We show how a variety of recruitment patterns across a network arise as the result of interplay between heterogeneous node dynamics and heterogeneous coupling among nodes. Our results demonstrate the important role of brain network dynamics in driving spatiotemporal patterns of seizure onset and provide a dynamic mechanism that could inform novel classifications of seizure types in clinical practice.Keywords
Funding Information
- Medical Research Council (MR/S019499/1)
- Engineering and Physical Sciences Research Council (EP/N014391/1)
- Royal Society (IE170112)
- National Natural Science Foundation of China-Yunnan Joint Fund (11701201)
This publication has 54 references indexed in Scilit:
- Epileptic Neuronal Networks: Methods of Identification and Clinical RelevanceFrontiers in Neurology, 2013
- Epilepsy: Ever-changing states of cortical excitabilityNeuroscience, 2012
- Seizure generation: The role of nodes and networksEpilepsia, 2012
- A phenomenological model of seizure initiation suggests network structure may explain seizure frequency in idiopathic generalised epilepsyThe Journal of Mathematical Neuroscience, 2012
- The importance of modeling epileptic seizure dynamics as spatio-temporal patternsFrontiers in Physiology, 2012
- Derivation and analysis of an ordinary differential equation mean-field model for studying clinically recorded epilepsy dynamicsPhysical Review E, 2009
- Spatial analysis of intracerebral electroencephalographic signals in the time and frequency domain: identification of epileptogenic networks in partial epilepsyPhilosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, 2008
- Biostatistical AnalysisEcology, 1996
- The hyperexcitable neuron: Microelectrode studies of the chronic epileptic focus in the intact, awake monkeyExperimental Neurology, 1967
- On a Test of Whether one of Two Random Variables is Stochastically Larger than the OtherThe Annals of Mathematical Statistics, 1947