Cargando…

Localization of beta power decrease as measure for lateralization in pre-surgical language mapping with magnetoencephalography, compared with functional magnetic resonance imaging and validated by Wada test

Objective: Atypical patterns of language lateralization due to early reorganizational processes constitute a challenge in the pre-surgical evaluation of patients with pharmaco-resistant epilepsy. There is no consensus on an optimal analysis method used for the identification of language dominance in...

Descripción completa

Detalles Bibliográficos
Autores principales: Herfurth, Kirsten, Harpaz, Yuval, Roesch, Julie, Mueller, Nadine, Walther, Katrin, Kaltenhaeuser, Martin, Pauli, Elisabeth, Goldstein, Abraham, Hamer, Hajo, Buchfelder, Michael, Doerfler, Arnd, Prell, Julian, Rampp, Stefan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9644652/
https://www.ncbi.nlm.nih.gov/pubmed/36393988
http://dx.doi.org/10.3389/fnhum.2022.996989
_version_ 1784826788175675392
author Herfurth, Kirsten
Harpaz, Yuval
Roesch, Julie
Mueller, Nadine
Walther, Katrin
Kaltenhaeuser, Martin
Pauli, Elisabeth
Goldstein, Abraham
Hamer, Hajo
Buchfelder, Michael
Doerfler, Arnd
Prell, Julian
Rampp, Stefan
author_facet Herfurth, Kirsten
Harpaz, Yuval
Roesch, Julie
Mueller, Nadine
Walther, Katrin
Kaltenhaeuser, Martin
Pauli, Elisabeth
Goldstein, Abraham
Hamer, Hajo
Buchfelder, Michael
Doerfler, Arnd
Prell, Julian
Rampp, Stefan
author_sort Herfurth, Kirsten
collection PubMed
description Objective: Atypical patterns of language lateralization due to early reorganizational processes constitute a challenge in the pre-surgical evaluation of patients with pharmaco-resistant epilepsy. There is no consensus on an optimal analysis method used for the identification of language dominance in MEG. This study examines the concordance between MEG source localization of beta power desynchronization and fMRI with regard to lateralization and localization of expressive and receptive language areas using a visual verb generation task. Methods: Twenty-five patients with pharmaco-resistant epilepsy, including six patients with atypical language lateralization, and ten right-handed controls obtained MEG and fMRI language assessment. Fourteen patients additionally underwent the Wada test. We analyzed MEG beta power desynchronization in sensor (controls) and source space (patients and controls). Beta power decrease between 13 and 35 Hz was localized applying Dynamic Imaging of Coherent Sources Beamformer technique. Statistical inferences were grounded on cluster-based permutation testing for single subjects. Results: Event-related desynchronization of beta power in MEG was seen within the language-dominant frontal and temporal lobe and within the premotor cortex. Our analysis pipeline consistently yielded left language dominance with high laterality indices in controls. Language lateralization in MEG and Wada test agreed in all 14 patients for inferior frontal, temporal and parietal language areas (Cohen’s Kappa = 1, p < 0.001). fMRI agreed with Wada test in 12 out of 14 cases (85.7%) for Broca’s area (Cohen’s Kappa = 0.71, p = 0.024), while the agreement for temporal and temporo-parietal language areas were non-significant. Concordance between MEG and fMRI laterality indices was highest within the inferior frontal gyrus, with an agreement in 19/24 cases (79.2%), and non-significant for Wernicke’s area. Spatial agreement between fMRI and MEG varied considerably between subjects and brain regions with the lowest Euclidean distances within the inferior frontal region of interest. Conclusion: Localizing the desynchronization of MEG beta power using a verb generation task is a promising tool for the identification of language dominance in the pre-surgical evaluation of epilepsy patients. The overall agreement between MEG and fMRI was lower than expected and might be attributed to differences within the baseline condition. A larger sample size and an adjustment of the experimental designs are needed to draw further conclusions.
format Online
Article
Text
id pubmed-9644652
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-96446522022-11-15 Localization of beta power decrease as measure for lateralization in pre-surgical language mapping with magnetoencephalography, compared with functional magnetic resonance imaging and validated by Wada test Herfurth, Kirsten Harpaz, Yuval Roesch, Julie Mueller, Nadine Walther, Katrin Kaltenhaeuser, Martin Pauli, Elisabeth Goldstein, Abraham Hamer, Hajo Buchfelder, Michael Doerfler, Arnd Prell, Julian Rampp, Stefan Front Hum Neurosci Human Neuroscience Objective: Atypical patterns of language lateralization due to early reorganizational processes constitute a challenge in the pre-surgical evaluation of patients with pharmaco-resistant epilepsy. There is no consensus on an optimal analysis method used for the identification of language dominance in MEG. This study examines the concordance between MEG source localization of beta power desynchronization and fMRI with regard to lateralization and localization of expressive and receptive language areas using a visual verb generation task. Methods: Twenty-five patients with pharmaco-resistant epilepsy, including six patients with atypical language lateralization, and ten right-handed controls obtained MEG and fMRI language assessment. Fourteen patients additionally underwent the Wada test. We analyzed MEG beta power desynchronization in sensor (controls) and source space (patients and controls). Beta power decrease between 13 and 35 Hz was localized applying Dynamic Imaging of Coherent Sources Beamformer technique. Statistical inferences were grounded on cluster-based permutation testing for single subjects. Results: Event-related desynchronization of beta power in MEG was seen within the language-dominant frontal and temporal lobe and within the premotor cortex. Our analysis pipeline consistently yielded left language dominance with high laterality indices in controls. Language lateralization in MEG and Wada test agreed in all 14 patients for inferior frontal, temporal and parietal language areas (Cohen’s Kappa = 1, p < 0.001). fMRI agreed with Wada test in 12 out of 14 cases (85.7%) for Broca’s area (Cohen’s Kappa = 0.71, p = 0.024), while the agreement for temporal and temporo-parietal language areas were non-significant. Concordance between MEG and fMRI laterality indices was highest within the inferior frontal gyrus, with an agreement in 19/24 cases (79.2%), and non-significant for Wernicke’s area. Spatial agreement between fMRI and MEG varied considerably between subjects and brain regions with the lowest Euclidean distances within the inferior frontal region of interest. Conclusion: Localizing the desynchronization of MEG beta power using a verb generation task is a promising tool for the identification of language dominance in the pre-surgical evaluation of epilepsy patients. The overall agreement between MEG and fMRI was lower than expected and might be attributed to differences within the baseline condition. A larger sample size and an adjustment of the experimental designs are needed to draw further conclusions. Frontiers Media S.A. 2022-10-26 /pmc/articles/PMC9644652/ /pubmed/36393988 http://dx.doi.org/10.3389/fnhum.2022.996989 Text en Copyright © 2022 Herfurth, Harpaz, Roesch, Mueller, Walther, Kaltenhaeuser, Pauli, Goldstein, Hamer, Buchfelder, Doerfler, Prell and Rampp. 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 Human Neuroscience
Herfurth, Kirsten
Harpaz, Yuval
Roesch, Julie
Mueller, Nadine
Walther, Katrin
Kaltenhaeuser, Martin
Pauli, Elisabeth
Goldstein, Abraham
Hamer, Hajo
Buchfelder, Michael
Doerfler, Arnd
Prell, Julian
Rampp, Stefan
Localization of beta power decrease as measure for lateralization in pre-surgical language mapping with magnetoencephalography, compared with functional magnetic resonance imaging and validated by Wada test
title Localization of beta power decrease as measure for lateralization in pre-surgical language mapping with magnetoencephalography, compared with functional magnetic resonance imaging and validated by Wada test
title_full Localization of beta power decrease as measure for lateralization in pre-surgical language mapping with magnetoencephalography, compared with functional magnetic resonance imaging and validated by Wada test
title_fullStr Localization of beta power decrease as measure for lateralization in pre-surgical language mapping with magnetoencephalography, compared with functional magnetic resonance imaging and validated by Wada test
title_full_unstemmed Localization of beta power decrease as measure for lateralization in pre-surgical language mapping with magnetoencephalography, compared with functional magnetic resonance imaging and validated by Wada test
title_short Localization of beta power decrease as measure for lateralization in pre-surgical language mapping with magnetoencephalography, compared with functional magnetic resonance imaging and validated by Wada test
title_sort localization of beta power decrease as measure for lateralization in pre-surgical language mapping with magnetoencephalography, compared with functional magnetic resonance imaging and validated by wada test
topic Human Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9644652/
https://www.ncbi.nlm.nih.gov/pubmed/36393988
http://dx.doi.org/10.3389/fnhum.2022.996989
work_keys_str_mv AT herfurthkirsten localizationofbetapowerdecreaseasmeasureforlateralizationinpresurgicallanguagemappingwithmagnetoencephalographycomparedwithfunctionalmagneticresonanceimagingandvalidatedbywadatest
AT harpazyuval localizationofbetapowerdecreaseasmeasureforlateralizationinpresurgicallanguagemappingwithmagnetoencephalographycomparedwithfunctionalmagneticresonanceimagingandvalidatedbywadatest
AT roeschjulie localizationofbetapowerdecreaseasmeasureforlateralizationinpresurgicallanguagemappingwithmagnetoencephalographycomparedwithfunctionalmagneticresonanceimagingandvalidatedbywadatest
AT muellernadine localizationofbetapowerdecreaseasmeasureforlateralizationinpresurgicallanguagemappingwithmagnetoencephalographycomparedwithfunctionalmagneticresonanceimagingandvalidatedbywadatest
AT waltherkatrin localizationofbetapowerdecreaseasmeasureforlateralizationinpresurgicallanguagemappingwithmagnetoencephalographycomparedwithfunctionalmagneticresonanceimagingandvalidatedbywadatest
AT kaltenhaeusermartin localizationofbetapowerdecreaseasmeasureforlateralizationinpresurgicallanguagemappingwithmagnetoencephalographycomparedwithfunctionalmagneticresonanceimagingandvalidatedbywadatest
AT paulielisabeth localizationofbetapowerdecreaseasmeasureforlateralizationinpresurgicallanguagemappingwithmagnetoencephalographycomparedwithfunctionalmagneticresonanceimagingandvalidatedbywadatest
AT goldsteinabraham localizationofbetapowerdecreaseasmeasureforlateralizationinpresurgicallanguagemappingwithmagnetoencephalographycomparedwithfunctionalmagneticresonanceimagingandvalidatedbywadatest
AT hamerhajo localizationofbetapowerdecreaseasmeasureforlateralizationinpresurgicallanguagemappingwithmagnetoencephalographycomparedwithfunctionalmagneticresonanceimagingandvalidatedbywadatest
AT buchfeldermichael localizationofbetapowerdecreaseasmeasureforlateralizationinpresurgicallanguagemappingwithmagnetoencephalographycomparedwithfunctionalmagneticresonanceimagingandvalidatedbywadatest
AT doerflerarnd localizationofbetapowerdecreaseasmeasureforlateralizationinpresurgicallanguagemappingwithmagnetoencephalographycomparedwithfunctionalmagneticresonanceimagingandvalidatedbywadatest
AT prelljulian localizationofbetapowerdecreaseasmeasureforlateralizationinpresurgicallanguagemappingwithmagnetoencephalographycomparedwithfunctionalmagneticresonanceimagingandvalidatedbywadatest
AT ramppstefan localizationofbetapowerdecreaseasmeasureforlateralizationinpresurgicallanguagemappingwithmagnetoencephalographycomparedwithfunctionalmagneticresonanceimagingandvalidatedbywadatest