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Distinction of Physiologic and Epileptic Ripples: An Electrical Stimulation Study

Ripple oscillations (80–250 Hz) are a promising biomarker of epileptic activity, but are also involved in memory consolidation, which impairs their value as a diagnostic tool. Distinguishing physiologic from epileptic ripples has been particularly challenging because usually, invasive recordings are...

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Autores principales: Schönberger, Jan, Knopf, Anja, Klotz, Kerstin Alexandra, Dümpelmann, Matthias, Schulze-Bonhage, Andreas, Jacobs, Julia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8146715/
https://www.ncbi.nlm.nih.gov/pubmed/33923317
http://dx.doi.org/10.3390/brainsci11050538
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author Schönberger, Jan
Knopf, Anja
Klotz, Kerstin Alexandra
Dümpelmann, Matthias
Schulze-Bonhage, Andreas
Jacobs, Julia
author_facet Schönberger, Jan
Knopf, Anja
Klotz, Kerstin Alexandra
Dümpelmann, Matthias
Schulze-Bonhage, Andreas
Jacobs, Julia
author_sort Schönberger, Jan
collection PubMed
description Ripple oscillations (80–250 Hz) are a promising biomarker of epileptic activity, but are also involved in memory consolidation, which impairs their value as a diagnostic tool. Distinguishing physiologic from epileptic ripples has been particularly challenging because usually, invasive recordings are only performed in patients with refractory epilepsy. Here, we identified ‘healthy’ brain areas based on electrical stimulation and hypothesized that these regions specifically generate ‘pure’ ripples not coupled to spikes. Intracranial electroencephalography (EEG) recorded with subdural grid electrodes was retrospectively analyzed in 19 patients with drug-resistant focal epilepsy. Interictal spikes and ripples were automatically detected in slow-wave sleep using the publicly available Delphos software. We found that rates of spikes, ripples and ripples coupled to spikes (‘spike–ripples’) were higher inside the seizure-onset zone (p < 0.001). A comparison of receiver operating characteristic curves revealed that spike–ripples slightly delineated the seizure-onset zone channels, but did this significantly better than spikes (p < 0.001). Ripples were more frequent in the eloquent neocortex than in the remaining non-seizure onset zone areas (p < 0.001). This was due to the higher rates of ‘pure’ ripples (p < 0.001; median rates 3.3/min vs. 1.4/min), whereas spike–ripple rates were not significantly different (p = 0.87). ‘Pure’ ripples identified ‘healthy’ channels significantly better than chance (p < 0.001). Our findings suggest that, in contrast to epileptic spike–ripples, ‘pure’ ripples are mainly physiological. They may be considered, in addition to electrical stimulation, to delineate eloquent cortex in pre-surgical patients. Since we applied open source software for detection, our approach may be generally suited to tackle a variety of research questions in epilepsy and cognitive science.
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spelling pubmed-81467152021-05-26 Distinction of Physiologic and Epileptic Ripples: An Electrical Stimulation Study Schönberger, Jan Knopf, Anja Klotz, Kerstin Alexandra Dümpelmann, Matthias Schulze-Bonhage, Andreas Jacobs, Julia Brain Sci Article Ripple oscillations (80–250 Hz) are a promising biomarker of epileptic activity, but are also involved in memory consolidation, which impairs their value as a diagnostic tool. Distinguishing physiologic from epileptic ripples has been particularly challenging because usually, invasive recordings are only performed in patients with refractory epilepsy. Here, we identified ‘healthy’ brain areas based on electrical stimulation and hypothesized that these regions specifically generate ‘pure’ ripples not coupled to spikes. Intracranial electroencephalography (EEG) recorded with subdural grid electrodes was retrospectively analyzed in 19 patients with drug-resistant focal epilepsy. Interictal spikes and ripples were automatically detected in slow-wave sleep using the publicly available Delphos software. We found that rates of spikes, ripples and ripples coupled to spikes (‘spike–ripples’) were higher inside the seizure-onset zone (p < 0.001). A comparison of receiver operating characteristic curves revealed that spike–ripples slightly delineated the seizure-onset zone channels, but did this significantly better than spikes (p < 0.001). Ripples were more frequent in the eloquent neocortex than in the remaining non-seizure onset zone areas (p < 0.001). This was due to the higher rates of ‘pure’ ripples (p < 0.001; median rates 3.3/min vs. 1.4/min), whereas spike–ripple rates were not significantly different (p = 0.87). ‘Pure’ ripples identified ‘healthy’ channels significantly better than chance (p < 0.001). Our findings suggest that, in contrast to epileptic spike–ripples, ‘pure’ ripples are mainly physiological. They may be considered, in addition to electrical stimulation, to delineate eloquent cortex in pre-surgical patients. Since we applied open source software for detection, our approach may be generally suited to tackle a variety of research questions in epilepsy and cognitive science. MDPI 2021-04-24 /pmc/articles/PMC8146715/ /pubmed/33923317 http://dx.doi.org/10.3390/brainsci11050538 Text en © 2021 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Schönberger, Jan
Knopf, Anja
Klotz, Kerstin Alexandra
Dümpelmann, Matthias
Schulze-Bonhage, Andreas
Jacobs, Julia
Distinction of Physiologic and Epileptic Ripples: An Electrical Stimulation Study
title Distinction of Physiologic and Epileptic Ripples: An Electrical Stimulation Study
title_full Distinction of Physiologic and Epileptic Ripples: An Electrical Stimulation Study
title_fullStr Distinction of Physiologic and Epileptic Ripples: An Electrical Stimulation Study
title_full_unstemmed Distinction of Physiologic and Epileptic Ripples: An Electrical Stimulation Study
title_short Distinction of Physiologic and Epileptic Ripples: An Electrical Stimulation Study
title_sort distinction of physiologic and epileptic ripples: an electrical stimulation study
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8146715/
https://www.ncbi.nlm.nih.gov/pubmed/33923317
http://dx.doi.org/10.3390/brainsci11050538
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