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Validating EEG source imaging using intracranial electrical stimulation

Electrical source imaging is used in presurgical epilepsy evaluation and in cognitive neurosciences to localize neuronal sources of brain potentials recorded on EEG. This study evaluates the spatial accuracy of electrical source imaging for known sources, using electrical stimulation potentials reco...

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Autores principales: Unnwongse, Kanjana, Rampp, Stefan, Wehner, Tim, Kowoll, Annika, Parpaley, Yaroslav, von Lehe, Marec, Lanfer, Benjamin, Rusiniak, Mateusz, Wolters, Carsten, Wellmer, Jörg
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9942548/
https://www.ncbi.nlm.nih.gov/pubmed/36824389
http://dx.doi.org/10.1093/braincomms/fcad023
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author Unnwongse, Kanjana
Rampp, Stefan
Wehner, Tim
Kowoll, Annika
Parpaley, Yaroslav
von Lehe, Marec
Lanfer, Benjamin
Rusiniak, Mateusz
Wolters, Carsten
Wellmer, Jörg
author_facet Unnwongse, Kanjana
Rampp, Stefan
Wehner, Tim
Kowoll, Annika
Parpaley, Yaroslav
von Lehe, Marec
Lanfer, Benjamin
Rusiniak, Mateusz
Wolters, Carsten
Wellmer, Jörg
author_sort Unnwongse, Kanjana
collection PubMed
description Electrical source imaging is used in presurgical epilepsy evaluation and in cognitive neurosciences to localize neuronal sources of brain potentials recorded on EEG. This study evaluates the spatial accuracy of electrical source imaging for known sources, using electrical stimulation potentials recorded on simultaneous stereo-EEG and 37-electrode scalp EEG, and identifies factors determining the localization error. In 11 patients undergoing simultaneous stereo-EEG and 37-electrode scalp EEG recordings, sequential series of 99–110 biphasic pulses (2 ms pulse width) were applied by bipolar electrical stimulation on adjacent contacts of implanted stereo-EEG electrodes. The scalp EEG correlates of stimulation potentials were recorded with a sampling rate of 30 kHz. Electrical source imaging of averaged stimulation potentials was calculated utilizing a dipole source model of peak stimulation potentials based on individual four-compartment finite element method head models with various skull conductivities (range from 0.0413 to 0.001 S/m). Fitted dipoles with a goodness of fit of ≥80% were included in the analysis. The localization error was calculated using the Euclidean distance between the estimated dipoles and the centre point of adjacent stimulating contacts. A total of 3619 stimulation locations, respectively, dipole localizations, were included in the evaluation. Mean localization errors ranged from 10.3 to 26 mm, depending on source depth and selected skull conductivity. The mean localization error increased with an increase in source depth (r(3617) = [0.19], P = 0.000) and decreased with an increase in skull conductivity (r(3617) = [−0.26], P = 0.000). High skull conductivities (0.0413–0.0118 S/m) yielded significantly lower localization errors for all source depths. For superficial sources (<20 mm from the inner skull), all skull conductivities yielded insignificantly different localization errors. However, for deeper sources, in particular >40 mm, high skull conductivities of 0.0413 and 0.0206 S/m yielded significantly lower localization errors. In relation to stimulation locations, the majority of estimated dipoles moved outward-forward-downward to inward-forward-downward with a decrease in source depth and an increase in skull conductivity. Multivariate analysis revealed that an increase in source depth, number of skull holes and white matter volume, while a decrease in skull conductivity independently led to higher localization error. This evaluation of electrical source imaging accuracy using artificial patterns with a high signal-to-noise ratio supports its application in presurgical epilepsy evaluation and cognitive neurosciences. In our artificial potential model, optimizing the selected skull conductivity minimized the localization error. Future studies should examine if this accounts for true neural signals.
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spelling pubmed-99425482023-02-22 Validating EEG source imaging using intracranial electrical stimulation Unnwongse, Kanjana Rampp, Stefan Wehner, Tim Kowoll, Annika Parpaley, Yaroslav von Lehe, Marec Lanfer, Benjamin Rusiniak, Mateusz Wolters, Carsten Wellmer, Jörg Brain Commun Original Article Electrical source imaging is used in presurgical epilepsy evaluation and in cognitive neurosciences to localize neuronal sources of brain potentials recorded on EEG. This study evaluates the spatial accuracy of electrical source imaging for known sources, using electrical stimulation potentials recorded on simultaneous stereo-EEG and 37-electrode scalp EEG, and identifies factors determining the localization error. In 11 patients undergoing simultaneous stereo-EEG and 37-electrode scalp EEG recordings, sequential series of 99–110 biphasic pulses (2 ms pulse width) were applied by bipolar electrical stimulation on adjacent contacts of implanted stereo-EEG electrodes. The scalp EEG correlates of stimulation potentials were recorded with a sampling rate of 30 kHz. Electrical source imaging of averaged stimulation potentials was calculated utilizing a dipole source model of peak stimulation potentials based on individual four-compartment finite element method head models with various skull conductivities (range from 0.0413 to 0.001 S/m). Fitted dipoles with a goodness of fit of ≥80% were included in the analysis. The localization error was calculated using the Euclidean distance between the estimated dipoles and the centre point of adjacent stimulating contacts. A total of 3619 stimulation locations, respectively, dipole localizations, were included in the evaluation. Mean localization errors ranged from 10.3 to 26 mm, depending on source depth and selected skull conductivity. The mean localization error increased with an increase in source depth (r(3617) = [0.19], P = 0.000) and decreased with an increase in skull conductivity (r(3617) = [−0.26], P = 0.000). High skull conductivities (0.0413–0.0118 S/m) yielded significantly lower localization errors for all source depths. For superficial sources (<20 mm from the inner skull), all skull conductivities yielded insignificantly different localization errors. However, for deeper sources, in particular >40 mm, high skull conductivities of 0.0413 and 0.0206 S/m yielded significantly lower localization errors. In relation to stimulation locations, the majority of estimated dipoles moved outward-forward-downward to inward-forward-downward with a decrease in source depth and an increase in skull conductivity. Multivariate analysis revealed that an increase in source depth, number of skull holes and white matter volume, while a decrease in skull conductivity independently led to higher localization error. This evaluation of electrical source imaging accuracy using artificial patterns with a high signal-to-noise ratio supports its application in presurgical epilepsy evaluation and cognitive neurosciences. In our artificial potential model, optimizing the selected skull conductivity minimized the localization error. Future studies should examine if this accounts for true neural signals. Oxford University Press 2023-02-07 /pmc/articles/PMC9942548/ /pubmed/36824389 http://dx.doi.org/10.1093/braincomms/fcad023 Text en © The Author(s) 2023. Published by Oxford University Press on behalf of the Guarantors of Brain. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Article
Unnwongse, Kanjana
Rampp, Stefan
Wehner, Tim
Kowoll, Annika
Parpaley, Yaroslav
von Lehe, Marec
Lanfer, Benjamin
Rusiniak, Mateusz
Wolters, Carsten
Wellmer, Jörg
Validating EEG source imaging using intracranial electrical stimulation
title Validating EEG source imaging using intracranial electrical stimulation
title_full Validating EEG source imaging using intracranial electrical stimulation
title_fullStr Validating EEG source imaging using intracranial electrical stimulation
title_full_unstemmed Validating EEG source imaging using intracranial electrical stimulation
title_short Validating EEG source imaging using intracranial electrical stimulation
title_sort validating eeg source imaging using intracranial electrical stimulation
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9942548/
https://www.ncbi.nlm.nih.gov/pubmed/36824389
http://dx.doi.org/10.1093/braincomms/fcad023
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