Transfer Function Models for the Localization of Seizure Onset Zone From Cortico-Cortical Evoked Potentials

Surgical resection of the seizure onset zone (SOZ) could potentially lead to seizure-freedom in medically refractory epilepsy patients. However, localizing the SOZ can be a time consuming and tedious process involving visual inspection of intracranial electroencephalographic (iEEG) recordings captur...

Full description

Bibliographic Details
Main Authors: Golnoosh Kamali, Rachel June Smith, Mark Hays, Christopher Coogan, Nathan E. Crone, Joon Y. Kang, Sridevi V. Sarma
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-12-01
Series:Frontiers in Neurology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fneur.2020.579961/full
_version_ 1818433659244380160
author Golnoosh Kamali
Rachel June Smith
Mark Hays
Christopher Coogan
Nathan E. Crone
Joon Y. Kang
Sridevi V. Sarma
Sridevi V. Sarma
author_facet Golnoosh Kamali
Rachel June Smith
Mark Hays
Christopher Coogan
Nathan E. Crone
Joon Y. Kang
Sridevi V. Sarma
Sridevi V. Sarma
author_sort Golnoosh Kamali
collection DOAJ
description Surgical resection of the seizure onset zone (SOZ) could potentially lead to seizure-freedom in medically refractory epilepsy patients. However, localizing the SOZ can be a time consuming and tedious process involving visual inspection of intracranial electroencephalographic (iEEG) recordings captured during passive patient monitoring. Cortical stimulation is currently performed on patients undergoing invasive EEG monitoring for the main purpose of mapping functional brain networks such as language and motor networks. We hypothesized that evoked responses from single pulse electrical stimulation (SPES) can also be used to localize the SOZ as they may express the natural frequencies and connectivity of the iEEG network. To test our hypothesis, we constructed patient specific transfer function models from the evoked responses recorded from 22 epilepsy patients that underwent SPES evaluation and iEEG monitoring. We then computed the frequency and connectivity dependent “peak gain” of the system as measured by the H∞  norm from systems theory. We found that in cases for which clinicians had high confidence in localizing the SOZ, the highest peak gain transfer functions with the smallest “floor gain” (gain at which the dipped H∞   3dB below DC gain) corresponded to when the clinically annotated SOZ and early spread regions were stimulated. In more complex cases, there was a large spread of the peak-to-floor (PF) ratios when the clinically annotated SOZ was stimulated. Interestingly for patients who had successful surgeries, our ratio of gains, agreed with clinical localization, no matter the complexity of the case. For patients with failed surgeries, the PF ratio did not match clinical annotations. Our findings suggest that transfer function gains and their corresponding frequency responses computed from SPES evoked responses may improve SOZ localization and thus surgical outcomes.
first_indexed 2024-12-14T16:24:36Z
format Article
id doaj.art-2d4b019327f846dfb3ed8b89c66fb2ec
institution Directory Open Access Journal
issn 1664-2295
language English
last_indexed 2024-12-14T16:24:36Z
publishDate 2020-12-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Neurology
spelling doaj.art-2d4b019327f846dfb3ed8b89c66fb2ec2022-12-21T22:54:44ZengFrontiers Media S.A.Frontiers in Neurology1664-22952020-12-011110.3389/fneur.2020.579961579961Transfer Function Models for the Localization of Seizure Onset Zone From Cortico-Cortical Evoked PotentialsGolnoosh Kamali0Rachel June Smith1Mark Hays2Christopher Coogan3Nathan E. Crone4Joon Y. Kang5Sridevi V. Sarma6Sridevi V. Sarma7Neuromedical Control Systems Laboratory, Department of Electrical and Computer Engineering, Institute of Computational Medicine, Johns Hopkins University, Baltimore, MD, United StatesNeuromedical Control Systems Laboratory, Department of Biomedical Engineering, Institute of Computational Medicine, Johns Hopkins University, Baltimore, MD, United StatesCognitive Research, Online Neuroengineering and Electrophysiology Laboratory, Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD, United StatesCognitive Research, Online Neuroengineering and Electrophysiology Laboratory, Department of Neurology-Epilepsy, Johns Hopkins School of Medicine, Baltimore, MD, United StatesCognitive Research, Online Neuroengineering and Electrophysiology Laboratory, Department of Neurology-Epilepsy, Johns Hopkins School of Medicine, Baltimore, MD, United StatesDepartment of Neurology-Epilepsy, Johns Hopkins School of Medicine, Baltimore, MD, United StatesNeuromedical Control Systems Laboratory, Department of Electrical and Computer Engineering, Institute of Computational Medicine, Johns Hopkins University, Baltimore, MD, United StatesNeuromedical Control Systems Laboratory, Department of Biomedical Engineering, Institute of Computational Medicine, Johns Hopkins University, Baltimore, MD, United StatesSurgical resection of the seizure onset zone (SOZ) could potentially lead to seizure-freedom in medically refractory epilepsy patients. However, localizing the SOZ can be a time consuming and tedious process involving visual inspection of intracranial electroencephalographic (iEEG) recordings captured during passive patient monitoring. Cortical stimulation is currently performed on patients undergoing invasive EEG monitoring for the main purpose of mapping functional brain networks such as language and motor networks. We hypothesized that evoked responses from single pulse electrical stimulation (SPES) can also be used to localize the SOZ as they may express the natural frequencies and connectivity of the iEEG network. To test our hypothesis, we constructed patient specific transfer function models from the evoked responses recorded from 22 epilepsy patients that underwent SPES evaluation and iEEG monitoring. We then computed the frequency and connectivity dependent “peak gain” of the system as measured by the H∞  norm from systems theory. We found that in cases for which clinicians had high confidence in localizing the SOZ, the highest peak gain transfer functions with the smallest “floor gain” (gain at which the dipped H∞   3dB below DC gain) corresponded to when the clinically annotated SOZ and early spread regions were stimulated. In more complex cases, there was a large spread of the peak-to-floor (PF) ratios when the clinically annotated SOZ was stimulated. Interestingly for patients who had successful surgeries, our ratio of gains, agreed with clinical localization, no matter the complexity of the case. For patients with failed surgeries, the PF ratio did not match clinical annotations. Our findings suggest that transfer function gains and their corresponding frequency responses computed from SPES evoked responses may improve SOZ localization and thus surgical outcomes.https://www.frontiersin.org/articles/10.3389/fneur.2020.579961/fullepilepsyCCEPsstimulationSPESseizure
spellingShingle Golnoosh Kamali
Rachel June Smith
Mark Hays
Christopher Coogan
Nathan E. Crone
Joon Y. Kang
Sridevi V. Sarma
Sridevi V. Sarma
Transfer Function Models for the Localization of Seizure Onset Zone From Cortico-Cortical Evoked Potentials
Frontiers in Neurology
epilepsy
CCEPs
stimulation
SPES
seizure
title Transfer Function Models for the Localization of Seizure Onset Zone From Cortico-Cortical Evoked Potentials
title_full Transfer Function Models for the Localization of Seizure Onset Zone From Cortico-Cortical Evoked Potentials
title_fullStr Transfer Function Models for the Localization of Seizure Onset Zone From Cortico-Cortical Evoked Potentials
title_full_unstemmed Transfer Function Models for the Localization of Seizure Onset Zone From Cortico-Cortical Evoked Potentials
title_short Transfer Function Models for the Localization of Seizure Onset Zone From Cortico-Cortical Evoked Potentials
title_sort transfer function models for the localization of seizure onset zone from cortico cortical evoked potentials
topic epilepsy
CCEPs
stimulation
SPES
seizure
url https://www.frontiersin.org/articles/10.3389/fneur.2020.579961/full
work_keys_str_mv AT golnooshkamali transferfunctionmodelsforthelocalizationofseizureonsetzonefromcorticocorticalevokedpotentials
AT racheljunesmith transferfunctionmodelsforthelocalizationofseizureonsetzonefromcorticocorticalevokedpotentials
AT markhays transferfunctionmodelsforthelocalizationofseizureonsetzonefromcorticocorticalevokedpotentials
AT christophercoogan transferfunctionmodelsforthelocalizationofseizureonsetzonefromcorticocorticalevokedpotentials
AT nathanecrone transferfunctionmodelsforthelocalizationofseizureonsetzonefromcorticocorticalevokedpotentials
AT joonykang transferfunctionmodelsforthelocalizationofseizureonsetzonefromcorticocorticalevokedpotentials
AT sridevivsarma transferfunctionmodelsforthelocalizationofseizureonsetzonefromcorticocorticalevokedpotentials
AT sridevivsarma transferfunctionmodelsforthelocalizationofseizureonsetzonefromcorticocorticalevokedpotentials