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Expert-Level Intracranial Electroencephalogram Ictal Pattern Detection by a Deep Learning Neural Network

Background: Decision-making in epilepsy surgery is strongly connected to the interpretation of the intracranial EEG (iEEG). Although deep learning approaches have demonstrated efficiency in processing extracranial EEG, few studies have addressed iEEG seizure detection, in part due to the small numbe...

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Autores principales: Constantino, Alexander C., Sisterson, Nathaniel D., Zaher, Naoir, Urban, Alexandra, Richardson, R. Mark, Kokkinos, Vasileios
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8126697/
https://www.ncbi.nlm.nih.gov/pubmed/34012415
http://dx.doi.org/10.3389/fneur.2021.603868
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author Constantino, Alexander C.
Sisterson, Nathaniel D.
Zaher, Naoir
Urban, Alexandra
Richardson, R. Mark
Kokkinos, Vasileios
author_facet Constantino, Alexander C.
Sisterson, Nathaniel D.
Zaher, Naoir
Urban, Alexandra
Richardson, R. Mark
Kokkinos, Vasileios
author_sort Constantino, Alexander C.
collection PubMed
description Background: Decision-making in epilepsy surgery is strongly connected to the interpretation of the intracranial EEG (iEEG). Although deep learning approaches have demonstrated efficiency in processing extracranial EEG, few studies have addressed iEEG seizure detection, in part due to the small number of seizures per patient typically available from intracranial investigations. This study aims to evaluate the efficiency of deep learning methodology in detecting iEEG seizures using a large dataset of ictal patterns collected from epilepsy patients implanted with a responsive neurostimulation system (RNS). Methods: Five thousand two hundred and twenty-six ictal events were collected from 22 patients implanted with RNS. A convolutional neural network (CNN) architecture was created to provide personalized seizure annotations for each patient. Accuracy of seizure identification was tested in two scenarios: patients with seizures occurring following a period of chronic recording (scenario 1) and patients with seizures occurring immediately following implantation (scenario 2). The accuracy of the CNN in identifying RNS-recorded iEEG ictal patterns was evaluated against human neurophysiology expertise. Statistical performance was assessed via the area-under-precision-recall curve (AUPRC). Results: In scenario 1, the CNN achieved a maximum mean binary classification AUPRC of 0.84 ± 0.19 (95%CI, 0.72–0.93) and mean regression accuracy of 6.3 ± 1.0 s (95%CI, 4.3–8.5 s) at 30 seed samples. In scenario 2, maximum mean AUPRC was 0.80 ± 0.19 (95%CI, 0.68–0.91) and mean regression accuracy was 6.3 ± 0.9 s (95%CI, 4.8–8.3 s) at 20 seed samples. We obtained near-maximum accuracies at seed size of 10 in both scenarios. CNN classification failures can be explained by ictal electro-decrements, brief seizures, single-channel ictal patterns, highly concentrated interictal activity, changes in the sleep-wake cycle, and progressive modulation of electrographic ictal features. Conclusions: We developed a deep learning neural network that performs personalized detection of RNS-derived ictal patterns with expert-level accuracy. These results suggest the potential for automated techniques to significantly improve the management of closed-loop brain stimulation, including during the initial period of recording when the device is otherwise naïve to a given patient's seizures.
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spelling pubmed-81266972021-05-18 Expert-Level Intracranial Electroencephalogram Ictal Pattern Detection by a Deep Learning Neural Network Constantino, Alexander C. Sisterson, Nathaniel D. Zaher, Naoir Urban, Alexandra Richardson, R. Mark Kokkinos, Vasileios Front Neurol Neurology Background: Decision-making in epilepsy surgery is strongly connected to the interpretation of the intracranial EEG (iEEG). Although deep learning approaches have demonstrated efficiency in processing extracranial EEG, few studies have addressed iEEG seizure detection, in part due to the small number of seizures per patient typically available from intracranial investigations. This study aims to evaluate the efficiency of deep learning methodology in detecting iEEG seizures using a large dataset of ictal patterns collected from epilepsy patients implanted with a responsive neurostimulation system (RNS). Methods: Five thousand two hundred and twenty-six ictal events were collected from 22 patients implanted with RNS. A convolutional neural network (CNN) architecture was created to provide personalized seizure annotations for each patient. Accuracy of seizure identification was tested in two scenarios: patients with seizures occurring following a period of chronic recording (scenario 1) and patients with seizures occurring immediately following implantation (scenario 2). The accuracy of the CNN in identifying RNS-recorded iEEG ictal patterns was evaluated against human neurophysiology expertise. Statistical performance was assessed via the area-under-precision-recall curve (AUPRC). Results: In scenario 1, the CNN achieved a maximum mean binary classification AUPRC of 0.84 ± 0.19 (95%CI, 0.72–0.93) and mean regression accuracy of 6.3 ± 1.0 s (95%CI, 4.3–8.5 s) at 30 seed samples. In scenario 2, maximum mean AUPRC was 0.80 ± 0.19 (95%CI, 0.68–0.91) and mean regression accuracy was 6.3 ± 0.9 s (95%CI, 4.8–8.3 s) at 20 seed samples. We obtained near-maximum accuracies at seed size of 10 in both scenarios. CNN classification failures can be explained by ictal electro-decrements, brief seizures, single-channel ictal patterns, highly concentrated interictal activity, changes in the sleep-wake cycle, and progressive modulation of electrographic ictal features. Conclusions: We developed a deep learning neural network that performs personalized detection of RNS-derived ictal patterns with expert-level accuracy. These results suggest the potential for automated techniques to significantly improve the management of closed-loop brain stimulation, including during the initial period of recording when the device is otherwise naïve to a given patient's seizures. Frontiers Media S.A. 2021-05-03 /pmc/articles/PMC8126697/ /pubmed/34012415 http://dx.doi.org/10.3389/fneur.2021.603868 Text en Copyright © 2021 Constantino, Sisterson, Zaher, Urban, Richardson and Kokkinos. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neurology
Constantino, Alexander C.
Sisterson, Nathaniel D.
Zaher, Naoir
Urban, Alexandra
Richardson, R. Mark
Kokkinos, Vasileios
Expert-Level Intracranial Electroencephalogram Ictal Pattern Detection by a Deep Learning Neural Network
title Expert-Level Intracranial Electroencephalogram Ictal Pattern Detection by a Deep Learning Neural Network
title_full Expert-Level Intracranial Electroencephalogram Ictal Pattern Detection by a Deep Learning Neural Network
title_fullStr Expert-Level Intracranial Electroencephalogram Ictal Pattern Detection by a Deep Learning Neural Network
title_full_unstemmed Expert-Level Intracranial Electroencephalogram Ictal Pattern Detection by a Deep Learning Neural Network
title_short Expert-Level Intracranial Electroencephalogram Ictal Pattern Detection by a Deep Learning Neural Network
title_sort expert-level intracranial electroencephalogram ictal pattern detection by a deep learning neural network
topic Neurology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8126697/
https://www.ncbi.nlm.nih.gov/pubmed/34012415
http://dx.doi.org/10.3389/fneur.2021.603868
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