Alejandro Nieto Ramos, Balu Krishnan, Andreas V Alexopoulos, William Bingaman, Imad Najm, Juan C Bulacio, Demitre Serletis
{"title":"Epileptic network identification: insights from dynamic mode decomposition of sEEG data.","authors":"Alejandro Nieto Ramos, Balu Krishnan, Andreas V Alexopoulos, William Bingaman, Imad Najm, Juan C Bulacio, Demitre Serletis","doi":"10.1088/1741-2552/ad705f","DOIUrl":null,"url":null,"abstract":"<p><p><i>Objective.</i>For medically-refractory epilepsy patients, stereoelectroencephalography (sEEG) is a surgical method using intracranial electrode recordings to identify brain networks participating in early seizure organization and propagation (i.e. the epileptogenic zone, EZ). If identified, surgical EZ treatment via resection, ablation or neuromodulation can lead to seizure-freedom. To date, quantification of sEEG data, including its visualization and interpretation, remains a clinical and computational challenge. Given elusiveness of physical laws or governing equations modelling complex brain dynamics, data science offers unique insight into identifying unknown patterns within high-dimensional sEEG data. We apply here an unsupervised data-driven algorithm, dynamic mode decomposition (DMD), to sEEG recordings from five focal epilepsy patients (three with temporal lobe, and two with cingulate epilepsy), who underwent subsequent resective or ablative surgery and became seizure free.<i>Approach.</i>DMD obtains a linear approximation of nonlinear data dynamics, generating coherent structures ('modes') defining important signal features, used to extract frequencies, growth rates and spatial structures. DMD was adapted to produce dynamic modal maps (DMMs) across frequency sub-bands, capturing onset and evolution of epileptiform dynamics in sEEG data. Additionally, we developed a static estimate of EZ-localized electrode contacts, termed the higher-frequency mode-based norm index (MNI). DMM and MNI maps for representative patient seizures were validated against clinical sEEG results and seizure-free outcomes following surgery.<i>Main results.</i>DMD was most informative at higher frequencies, i.e. gamma (including high-gamma) and beta range, successfully identifying EZ contacts. Combined interpretation of DMM/MNI plots best identified spatiotemporal evolution of mode-specific network changes, with strong concordance to sEEG results and outcomes across all five patients. The method identified network attenuation in other contacts not implicated in the EZ.<i>Significance.</i>This is the first application of DMD to sEEG data analysis, supporting integration of neuroengineering, mathematical and machine learning methods into traditional workflows for sEEG review and epilepsy surgical decision-making.</p>","PeriodicalId":94096,"journal":{"name":"Journal of neural engineering","volume":null,"pages":null},"PeriodicalIF":0.0000,"publicationDate":"2024-08-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of neural engineering","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1088/1741-2552/ad705f","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"","JCRName":"","Score":null,"Total":0}
引用次数: 0
Abstract
Objective.For medically-refractory epilepsy patients, stereoelectroencephalography (sEEG) is a surgical method using intracranial electrode recordings to identify brain networks participating in early seizure organization and propagation (i.e. the epileptogenic zone, EZ). If identified, surgical EZ treatment via resection, ablation or neuromodulation can lead to seizure-freedom. To date, quantification of sEEG data, including its visualization and interpretation, remains a clinical and computational challenge. Given elusiveness of physical laws or governing equations modelling complex brain dynamics, data science offers unique insight into identifying unknown patterns within high-dimensional sEEG data. We apply here an unsupervised data-driven algorithm, dynamic mode decomposition (DMD), to sEEG recordings from five focal epilepsy patients (three with temporal lobe, and two with cingulate epilepsy), who underwent subsequent resective or ablative surgery and became seizure free.Approach.DMD obtains a linear approximation of nonlinear data dynamics, generating coherent structures ('modes') defining important signal features, used to extract frequencies, growth rates and spatial structures. DMD was adapted to produce dynamic modal maps (DMMs) across frequency sub-bands, capturing onset and evolution of epileptiform dynamics in sEEG data. Additionally, we developed a static estimate of EZ-localized electrode contacts, termed the higher-frequency mode-based norm index (MNI). DMM and MNI maps for representative patient seizures were validated against clinical sEEG results and seizure-free outcomes following surgery.Main results.DMD was most informative at higher frequencies, i.e. gamma (including high-gamma) and beta range, successfully identifying EZ contacts. Combined interpretation of DMM/MNI plots best identified spatiotemporal evolution of mode-specific network changes, with strong concordance to sEEG results and outcomes across all five patients. The method identified network attenuation in other contacts not implicated in the EZ.Significance.This is the first application of DMD to sEEG data analysis, supporting integration of neuroengineering, mathematical and machine learning methods into traditional workflows for sEEG review and epilepsy surgical decision-making.