Cognitive Processing Impacts High Frequency Intracranial EEG Activity of Human Hippocampus in Patients With Pharmacoresistant Focal Epilepsy

The electrophysiological EEG features such as high frequency oscillations, spikes and functional connectivity are often used for delineation of epileptogenic tissue and study of the normal function of the brain. The epileptogenic activity is also known to be suppressed by cognitive processing. Howev...

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Main Authors: Jan Cimbalnik, Martin Pail, Petr Klimes, Vojtech Travnicek, Robert Roman, Adam Vajcner, Milan Brazdil
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-10-01
Series:Frontiers in Neurology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fneur.2020.578571/full
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author Jan Cimbalnik
Martin Pail
Petr Klimes
Petr Klimes
Vojtech Travnicek
Vojtech Travnicek
Robert Roman
Robert Roman
Adam Vajcner
Adam Vajcner
Milan Brazdil
Milan Brazdil
author_facet Jan Cimbalnik
Martin Pail
Petr Klimes
Petr Klimes
Vojtech Travnicek
Vojtech Travnicek
Robert Roman
Robert Roman
Adam Vajcner
Adam Vajcner
Milan Brazdil
Milan Brazdil
author_sort Jan Cimbalnik
collection DOAJ
description The electrophysiological EEG features such as high frequency oscillations, spikes and functional connectivity are often used for delineation of epileptogenic tissue and study of the normal function of the brain. The epileptogenic activity is also known to be suppressed by cognitive processing. However, differences between epileptic and healthy brain behavior during rest and task were not studied in detail. In this study we investigate the impact of cognitive processing on epileptogenic and non-epileptogenic hippocampus and the intracranial EEG features representing the underlying electrophysiological processes. We investigated intracranial EEG in 24 epileptic and 24 non-epileptic hippocampi in patients with intractable focal epilepsy during a resting state period and during performance of various cognitive tasks. We evaluated the behavior of features derived from high frequency oscillations, interictal epileptiform discharges and functional connectivity and their changes in relation to cognitive processing. Subsequently, we performed an analysis whether cognitive processing can contribute to classification of epileptic and non-epileptic hippocampus using a machine learning approach. The results show that cognitive processing suppresses epileptogenic activity in epileptic hippocampus while it causes a shift toward higher frequencies in non-epileptic hippocampus. Statistical analysis reveals significantly different electrophysiological reactions of epileptic and non-epileptic hippocampus during cognitive processing, which can be measured by high frequency oscillations, interictal epileptiform discharges and functional connectivity. The calculated features showed high classification potential for epileptic hippocampus (AUC = 0.93). In conclusion, the differences between epileptic and non-epileptic hippocampus during cognitive processing bring new insight in delineation between pathological and physiological processes. Analysis of computed iEEG features in rest and task condition can improve the functional mapping during pre-surgical evaluation and provide additional guidance for distinguishing between epileptic and non-epileptic structure which is absolutely crucial for achieving the best possible outcome with as little side effects as possible.
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spelling doaj.art-2d45d4bb12af4be691688813530204682022-12-21T18:00:42ZengFrontiers Media S.A.Frontiers in Neurology1664-22952020-10-011110.3389/fneur.2020.578571578571Cognitive Processing Impacts High Frequency Intracranial EEG Activity of Human Hippocampus in Patients With Pharmacoresistant Focal EpilepsyJan Cimbalnik0Martin Pail1Petr Klimes2Petr Klimes3Vojtech Travnicek4Vojtech Travnicek5Robert Roman6Robert Roman7Adam Vajcner8Adam Vajcner9Milan Brazdil10Milan Brazdil11International Clinical Research Center, St. Anne's University Hospital, Brno, CzechiaDepartment of Neurology, Faculty of Medicine, Brno Epilepsy Center, St. Anne's University Hospital, Masaryk University, Brno, CzechiaInternational Clinical Research Center, St. Anne's University Hospital, Brno, CzechiaInstitute of Scientific Instruments, The Czech Academy of Sciences, Brno, CzechiaInternational Clinical Research Center, St. Anne's University Hospital, Brno, CzechiaInstitute of Scientific Instruments, The Czech Academy of Sciences, Brno, CzechiaDepartment of Neurology, Faculty of Medicine, Brno Epilepsy Center, St. Anne's University Hospital, Masaryk University, Brno, CzechiaBehavioral and Social Neuroscience Research Group, CEITEC - Central European Institute of Technology, Masaryk University, Brno, CzechiaDepartment of Neurology, Faculty of Medicine, Brno Epilepsy Center, St. Anne's University Hospital, Masaryk University, Brno, CzechiaDepartment of Sports Medicine and Rehabilitation, Faculty of Medicine, St. Anne's University Hospital, Masaryk University, Brno, CzechiaDepartment of Neurology, Faculty of Medicine, Brno Epilepsy Center, St. Anne's University Hospital, Masaryk University, Brno, CzechiaBehavioral and Social Neuroscience Research Group, CEITEC - Central European Institute of Technology, Masaryk University, Brno, CzechiaThe electrophysiological EEG features such as high frequency oscillations, spikes and functional connectivity are often used for delineation of epileptogenic tissue and study of the normal function of the brain. The epileptogenic activity is also known to be suppressed by cognitive processing. However, differences between epileptic and healthy brain behavior during rest and task were not studied in detail. In this study we investigate the impact of cognitive processing on epileptogenic and non-epileptogenic hippocampus and the intracranial EEG features representing the underlying electrophysiological processes. We investigated intracranial EEG in 24 epileptic and 24 non-epileptic hippocampi in patients with intractable focal epilepsy during a resting state period and during performance of various cognitive tasks. We evaluated the behavior of features derived from high frequency oscillations, interictal epileptiform discharges and functional connectivity and their changes in relation to cognitive processing. Subsequently, we performed an analysis whether cognitive processing can contribute to classification of epileptic and non-epileptic hippocampus using a machine learning approach. The results show that cognitive processing suppresses epileptogenic activity in epileptic hippocampus while it causes a shift toward higher frequencies in non-epileptic hippocampus. Statistical analysis reveals significantly different electrophysiological reactions of epileptic and non-epileptic hippocampus during cognitive processing, which can be measured by high frequency oscillations, interictal epileptiform discharges and functional connectivity. The calculated features showed high classification potential for epileptic hippocampus (AUC = 0.93). In conclusion, the differences between epileptic and non-epileptic hippocampus during cognitive processing bring new insight in delineation between pathological and physiological processes. Analysis of computed iEEG features in rest and task condition can improve the functional mapping during pre-surgical evaluation and provide additional guidance for distinguishing between epileptic and non-epileptic structure which is absolutely crucial for achieving the best possible outcome with as little side effects as possible.https://www.frontiersin.org/articles/10.3389/fneur.2020.578571/fullpharmacoresistant epilepsyhigh frequency oscillation (HFO)interictal epileptiform dischargefunctional connectivityhippocampuscognitive processing
spellingShingle Jan Cimbalnik
Martin Pail
Petr Klimes
Petr Klimes
Vojtech Travnicek
Vojtech Travnicek
Robert Roman
Robert Roman
Adam Vajcner
Adam Vajcner
Milan Brazdil
Milan Brazdil
Cognitive Processing Impacts High Frequency Intracranial EEG Activity of Human Hippocampus in Patients With Pharmacoresistant Focal Epilepsy
Frontiers in Neurology
pharmacoresistant epilepsy
high frequency oscillation (HFO)
interictal epileptiform discharge
functional connectivity
hippocampus
cognitive processing
title Cognitive Processing Impacts High Frequency Intracranial EEG Activity of Human Hippocampus in Patients With Pharmacoresistant Focal Epilepsy
title_full Cognitive Processing Impacts High Frequency Intracranial EEG Activity of Human Hippocampus in Patients With Pharmacoresistant Focal Epilepsy
title_fullStr Cognitive Processing Impacts High Frequency Intracranial EEG Activity of Human Hippocampus in Patients With Pharmacoresistant Focal Epilepsy
title_full_unstemmed Cognitive Processing Impacts High Frequency Intracranial EEG Activity of Human Hippocampus in Patients With Pharmacoresistant Focal Epilepsy
title_short Cognitive Processing Impacts High Frequency Intracranial EEG Activity of Human Hippocampus in Patients With Pharmacoresistant Focal Epilepsy
title_sort cognitive processing impacts high frequency intracranial eeg activity of human hippocampus in patients with pharmacoresistant focal epilepsy
topic pharmacoresistant epilepsy
high frequency oscillation (HFO)
interictal epileptiform discharge
functional connectivity
hippocampus
cognitive processing
url https://www.frontiersin.org/articles/10.3389/fneur.2020.578571/full
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