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      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

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          Abstract

          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.

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              Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain.

              An anatomical parcellation of the spatially normalized single-subject high-resolution T1 volume provided by the Montreal Neurological Institute (MNI) (D. L. Collins et al., 1998, Trans. Med. Imag. 17, 463-468) was performed. The MNI single-subject main sulci were first delineated and further used as landmarks for the 3D definition of 45 anatomical volumes of interest (AVOI) in each hemisphere. This procedure was performed using a dedicated software which allowed a 3D following of the sulci course on the edited brain. Regions of interest were then drawn manually with the same software every 2 mm on the axial slices of the high-resolution MNI single subject. The 90 AVOI were reconstructed and assigned a label. Using this parcellation method, three procedures to perform the automated anatomical labeling of functional studies are proposed: (1) labeling of an extremum defined by a set of coordinates, (2) percentage of voxels belonging to each of the AVOI intersected by a sphere centered by a set of coordinates, and (3) percentage of voxels belonging to each of the AVOI intersected by an activated cluster. An interface with the Statistical Parametric Mapping package (SPM, J. Ashburner and K. J. Friston, 1999, Hum. Brain Mapp. 7, 254-266) is provided as a freeware to researchers of the neuroimaging community. We believe that this tool is an improvement for the macroscopical labeling of activated area compared to labeling assessed using the Talairach atlas brain in which deformations are well known. However, this tool does not alleviate the need for more sophisticated labeling strategies based on anatomical or cytoarchitectonic probabilistic maps.
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                Author and article information

                Contributors
                Journal
                Front Hum Neurosci
                Front Hum Neurosci
                Front. Hum. Neurosci.
                Frontiers in Human Neuroscience
                Frontiers Media S.A.
                1662-5161
                26 October 2022
                2022
                : 16
                : 996989
                Affiliations
                [1] 1Department of Neurosurgery, University Hospital Erlangen , Erlangen, Germany
                [2] 2Department of Neurosurgery, University Hospital Halle , Halle (Saale), Germany
                [3] 3The Gonda Multidisciplinary Brain Research Center, Bar-Ilan University , Ramat Gan, Israel
                [4] 4Department of Neuroradiology, University Hospital Erlangen , Erlangen, Germany
                [5] 5Epilepsy Center, Department of Neurology, University Hospital Erlangen , Erlangen, Germany
                Author notes

                Edited by: Douglas Owen Cheyne, University of Toronto, Canada

                Reviewed by: Ismail S. Mohamed, University of Alabama at Birmingham, United States; Torsten Baldeweg, University College London, United Kingdom

                *Correspondence: Kirsten Herfurth kirsten.herfurth@ 123456posteo.de

                Present addresses: Yuval Harpaz, InnerEye, Medinat ha-Yehudim, Herzliya, Israel Nadine Mueller, Department of Psychiatry and Psychotherapy, Kaiserswerther Diakonie, Florence Nightingale Hospital, Düsseldorf, Germany

                Specialty section: This article was submitted to Brain Imaging and Stimulation, a section of the journal Frontiers in Human Neuroscience

                Article
                10.3389/fnhum.2022.996989
                9644652
                36393988
                3f2bb84e-e549-442b-a885-910d0548cc26
                Copyright © 2022 Herfurth, Harpaz, Roesch, Mueller, Walther, Kaltenhaeuser, Pauli, Goldstein, Hamer, Buchfelder, Doerfler, Prell and Rampp.

                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.

                History
                : 18 July 2022
                : 04 October 2022
                Page count
                Figures: 7, Tables: 7, Equations: 1, References: 82, Pages: 21, Words: 17236
                Categories
                Human Neuroscience
                Original Research

                Neurosciences
                language lateralization,magnetoencephalography (meg),functional magnetic resonance imaging (fmri),epilepsy,epilepsy surgery,intracarotid sodium amobarbital procedure (iat),wada test,beta power decrease

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