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The Effect of Right Temporal Lobe Gliomas on Left and Right Hemisphere Neural Processing During Speech Perception and Production Tasks

Using fMRI, we investigated how right temporal lobe gliomas affecting the posterior superior temporal sulcus alter neural processing observed during speech perception and production tasks. Behavioural language testing showed that three pre-operative neurosurgical patients with grade 2, grade 3 or gr...

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Autores principales: Yamamoto, Adam Kenji, Sanjuán, Ana, Pope, Rebecca, Parker Jones, Oiwi, Hope, Thomas M. H., Prejawa, Susan, Oberhuber, Marion, Mancini, Laura, Ekert, Justyna O., Garjardo-Vidal, Andrea, Creasey, Megan, Yousry, Tarek A., Green, David W., Price, Cathy J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9148966/
https://www.ncbi.nlm.nih.gov/pubmed/35652007
http://dx.doi.org/10.3389/fnhum.2022.803163
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author Yamamoto, Adam Kenji
Sanjuán, Ana
Pope, Rebecca
Parker Jones, Oiwi
Hope, Thomas M. H.
Prejawa, Susan
Oberhuber, Marion
Mancini, Laura
Ekert, Justyna O.
Garjardo-Vidal, Andrea
Creasey, Megan
Yousry, Tarek A.
Green, David W.
Price, Cathy J.
author_facet Yamamoto, Adam Kenji
Sanjuán, Ana
Pope, Rebecca
Parker Jones, Oiwi
Hope, Thomas M. H.
Prejawa, Susan
Oberhuber, Marion
Mancini, Laura
Ekert, Justyna O.
Garjardo-Vidal, Andrea
Creasey, Megan
Yousry, Tarek A.
Green, David W.
Price, Cathy J.
author_sort Yamamoto, Adam Kenji
collection PubMed
description Using fMRI, we investigated how right temporal lobe gliomas affecting the posterior superior temporal sulcus alter neural processing observed during speech perception and production tasks. Behavioural language testing showed that three pre-operative neurosurgical patients with grade 2, grade 3 or grade 4 tumours had the same pattern of mild language impairment in the domains of object naming and written word comprehension. When matching heard words for semantic relatedness (a speech perception task), these patients showed under-activation in the tumour infiltrated right superior temporal lobe compared to 61 neurotypical participants and 16 patients with tumours that preserved the right postero-superior temporal lobe, with enhanced activation within the (tumour-free) contralateral left superior temporal lobe. In contrast, when correctly naming objects (a speech production task), the patients with right postero-superior temporal lobe tumours showed higher activation than both control groups in the same right postero-superior temporal lobe region that was under-activated during auditory semantic matching. The task dependent pattern of under-activation during the auditory speech task and over-activation during object naming was also observed in eight stroke patients with right hemisphere infarcts that affected the right postero-superior temporal lobe compared to eight stroke patients with right hemisphere infarcts that spared it. These task-specific and site-specific cross-pathology effects highlight the importance of the right temporal lobe for language processing and motivate further study of how right temporal lobe tumours affect language performance and neural reorganisation. These findings may have important implications for surgical management of these patients, as knowledge of the regions showing functional reorganisation may help to avoid their inadvertent damage during neurosurgery.
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spelling pubmed-91489662022-05-31 The Effect of Right Temporal Lobe Gliomas on Left and Right Hemisphere Neural Processing During Speech Perception and Production Tasks Yamamoto, Adam Kenji Sanjuán, Ana Pope, Rebecca Parker Jones, Oiwi Hope, Thomas M. H. Prejawa, Susan Oberhuber, Marion Mancini, Laura Ekert, Justyna O. Garjardo-Vidal, Andrea Creasey, Megan Yousry, Tarek A. Green, David W. Price, Cathy J. Front Hum Neurosci Human Neuroscience Using fMRI, we investigated how right temporal lobe gliomas affecting the posterior superior temporal sulcus alter neural processing observed during speech perception and production tasks. Behavioural language testing showed that three pre-operative neurosurgical patients with grade 2, grade 3 or grade 4 tumours had the same pattern of mild language impairment in the domains of object naming and written word comprehension. When matching heard words for semantic relatedness (a speech perception task), these patients showed under-activation in the tumour infiltrated right superior temporal lobe compared to 61 neurotypical participants and 16 patients with tumours that preserved the right postero-superior temporal lobe, with enhanced activation within the (tumour-free) contralateral left superior temporal lobe. In contrast, when correctly naming objects (a speech production task), the patients with right postero-superior temporal lobe tumours showed higher activation than both control groups in the same right postero-superior temporal lobe region that was under-activated during auditory semantic matching. The task dependent pattern of under-activation during the auditory speech task and over-activation during object naming was also observed in eight stroke patients with right hemisphere infarcts that affected the right postero-superior temporal lobe compared to eight stroke patients with right hemisphere infarcts that spared it. These task-specific and site-specific cross-pathology effects highlight the importance of the right temporal lobe for language processing and motivate further study of how right temporal lobe tumours affect language performance and neural reorganisation. These findings may have important implications for surgical management of these patients, as knowledge of the regions showing functional reorganisation may help to avoid their inadvertent damage during neurosurgery. Frontiers Media S.A. 2022-05-16 /pmc/articles/PMC9148966/ /pubmed/35652007 http://dx.doi.org/10.3389/fnhum.2022.803163 Text en Copyright © 2022 Yamamoto, Sanjuán, Pope, Parker Jones, Hope, Prejawa, Oberhuber, Mancini, Ekert, Garjardo-Vidal, Creasey, Yousry, Green and Price. 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
Yamamoto, Adam Kenji
Sanjuán, Ana
Pope, Rebecca
Parker Jones, Oiwi
Hope, Thomas M. H.
Prejawa, Susan
Oberhuber, Marion
Mancini, Laura
Ekert, Justyna O.
Garjardo-Vidal, Andrea
Creasey, Megan
Yousry, Tarek A.
Green, David W.
Price, Cathy J.
The Effect of Right Temporal Lobe Gliomas on Left and Right Hemisphere Neural Processing During Speech Perception and Production Tasks
title The Effect of Right Temporal Lobe Gliomas on Left and Right Hemisphere Neural Processing During Speech Perception and Production Tasks
title_full The Effect of Right Temporal Lobe Gliomas on Left and Right Hemisphere Neural Processing During Speech Perception and Production Tasks
title_fullStr The Effect of Right Temporal Lobe Gliomas on Left and Right Hemisphere Neural Processing During Speech Perception and Production Tasks
title_full_unstemmed The Effect of Right Temporal Lobe Gliomas on Left and Right Hemisphere Neural Processing During Speech Perception and Production Tasks
title_short The Effect of Right Temporal Lobe Gliomas on Left and Right Hemisphere Neural Processing During Speech Perception and Production Tasks
title_sort effect of right temporal lobe gliomas on left and right hemisphere neural processing during speech perception and production tasks
topic Human Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9148966/
https://www.ncbi.nlm.nih.gov/pubmed/35652007
http://dx.doi.org/10.3389/fnhum.2022.803163
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