Overt speech critically changes lateralization index and did not allow determination of hemispheric dominance for language: an fMRI study

Abstract Background Pre-surgical mapping of language using functional MRI aimed principally to determine the dominant hemisphere. This mapping is currently performed using covert linguistic task in way to avoid motion artefacts potentially biasing the results. However, overt task is closer to natura...

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Autores principales: David Hassanein Berro, Jean-Michel Lemée, Louis-Marie Leiber, Evelyne Emery, Philippe Menei, Aram Ter Minassian
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Publicado: BMC 2021
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Acceso en línea:https://doaj.org/article/be9cb89973ee4fbcb33660e157ee85d6
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spelling oai:doaj.org-article:be9cb89973ee4fbcb33660e157ee85d62021-12-05T12:21:28ZOvert speech critically changes lateralization index and did not allow determination of hemispheric dominance for language: an fMRI study10.1186/s12868-021-00671-y1471-2202https://doaj.org/article/be9cb89973ee4fbcb33660e157ee85d62021-12-01T00:00:00Zhttps://doi.org/10.1186/s12868-021-00671-yhttps://doaj.org/toc/1471-2202Abstract Background Pre-surgical mapping of language using functional MRI aimed principally to determine the dominant hemisphere. This mapping is currently performed using covert linguistic task in way to avoid motion artefacts potentially biasing the results. However, overt task is closer to natural speaking, allows a control on the performance of the task, and may be easier to perform for stressed patients and children. However, overt task, by activating phonological areas on both hemispheres and areas involved in pitch prosody control in the non-dominant hemisphere, is expected to modify the determination of the dominant hemisphere by the calculation of the lateralization index (LI). Objective Here, we analyzed the modifications in the LI and the interactions between cognitive networks during covert and overt speech task. Methods Thirty-three volunteers participated in this study, all but four were right-handed. They performed three functional sessions consisting of (1) covert and (2) overt generation of a short sentence semantically linked with an audibly presented word, from which we estimated the “Covert” and “Overt” contrasts, and a (3) resting-state session. The resting-state session was submitted to spatial independent component analysis to identify language network at rest (LANG), cingulo-opercular network (CO), and ventral attention network (VAN). The LI was calculated using the bootstrapping method. Results The LI of the LANG was the most left-lateralized (0.66 ± 0.38). The LI shifted from a moderate leftward lateralization for the Covert contrast (0.32 ± 0.38) to a right lateralization for the Overt contrast (− 0.13 ± 0.30). The LI significantly differed from each other. This rightward shift was due to the recruitment of right hemispheric temporal areas together with the nodes of the CO. Conclusion Analyzing the overt speech by fMRI allowed improvement in the physiological knowledge regarding the coordinated activity of the intrinsic connectivity networks. However, the rightward shift of the LI in this condition did not provide the basic information on the hemispheric language dominance. Overt linguistic task cannot be recommended for clinical purpose when determining hemispheric dominance for language.David Hassanein BerroJean-Michel LeméeLouis-Marie LeiberEvelyne EmeryPhilippe MeneiAram Ter MinassianBMCarticlefMRIOvertFunctional lateralityLanguage networkCingulo-opercular networkVentral attention networkNeurosciences. Biological psychiatry. NeuropsychiatryRC321-571Neurophysiology and neuropsychologyQP351-495ENBMC Neuroscience, Vol 22, Iss 1, Pp 1-16 (2021)
institution DOAJ
collection DOAJ
language EN
topic fMRI
Overt
Functional laterality
Language network
Cingulo-opercular network
Ventral attention network
Neurosciences. Biological psychiatry. Neuropsychiatry
RC321-571
Neurophysiology and neuropsychology
QP351-495
spellingShingle fMRI
Overt
Functional laterality
Language network
Cingulo-opercular network
Ventral attention network
Neurosciences. Biological psychiatry. Neuropsychiatry
RC321-571
Neurophysiology and neuropsychology
QP351-495
David Hassanein Berro
Jean-Michel Lemée
Louis-Marie Leiber
Evelyne Emery
Philippe Menei
Aram Ter Minassian
Overt speech critically changes lateralization index and did not allow determination of hemispheric dominance for language: an fMRI study
description Abstract Background Pre-surgical mapping of language using functional MRI aimed principally to determine the dominant hemisphere. This mapping is currently performed using covert linguistic task in way to avoid motion artefacts potentially biasing the results. However, overt task is closer to natural speaking, allows a control on the performance of the task, and may be easier to perform for stressed patients and children. However, overt task, by activating phonological areas on both hemispheres and areas involved in pitch prosody control in the non-dominant hemisphere, is expected to modify the determination of the dominant hemisphere by the calculation of the lateralization index (LI). Objective Here, we analyzed the modifications in the LI and the interactions between cognitive networks during covert and overt speech task. Methods Thirty-three volunteers participated in this study, all but four were right-handed. They performed three functional sessions consisting of (1) covert and (2) overt generation of a short sentence semantically linked with an audibly presented word, from which we estimated the “Covert” and “Overt” contrasts, and a (3) resting-state session. The resting-state session was submitted to spatial independent component analysis to identify language network at rest (LANG), cingulo-opercular network (CO), and ventral attention network (VAN). The LI was calculated using the bootstrapping method. Results The LI of the LANG was the most left-lateralized (0.66 ± 0.38). The LI shifted from a moderate leftward lateralization for the Covert contrast (0.32 ± 0.38) to a right lateralization for the Overt contrast (− 0.13 ± 0.30). The LI significantly differed from each other. This rightward shift was due to the recruitment of right hemispheric temporal areas together with the nodes of the CO. Conclusion Analyzing the overt speech by fMRI allowed improvement in the physiological knowledge regarding the coordinated activity of the intrinsic connectivity networks. However, the rightward shift of the LI in this condition did not provide the basic information on the hemispheric language dominance. Overt linguistic task cannot be recommended for clinical purpose when determining hemispheric dominance for language.
format article
author David Hassanein Berro
Jean-Michel Lemée
Louis-Marie Leiber
Evelyne Emery
Philippe Menei
Aram Ter Minassian
author_facet David Hassanein Berro
Jean-Michel Lemée
Louis-Marie Leiber
Evelyne Emery
Philippe Menei
Aram Ter Minassian
author_sort David Hassanein Berro
title Overt speech critically changes lateralization index and did not allow determination of hemispheric dominance for language: an fMRI study
title_short Overt speech critically changes lateralization index and did not allow determination of hemispheric dominance for language: an fMRI study
title_full Overt speech critically changes lateralization index and did not allow determination of hemispheric dominance for language: an fMRI study
title_fullStr Overt speech critically changes lateralization index and did not allow determination of hemispheric dominance for language: an fMRI study
title_full_unstemmed Overt speech critically changes lateralization index and did not allow determination of hemispheric dominance for language: an fMRI study
title_sort overt speech critically changes lateralization index and did not allow determination of hemispheric dominance for language: an fmri study
publisher BMC
publishDate 2021
url https://doaj.org/article/be9cb89973ee4fbcb33660e157ee85d6
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