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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 MH; Prejawa, Susan; Oberhuber, Marion; ... Price, Cathy J; + view all (2022) The Effect of Right Temporal Lobe Gliomas on Left and Right Hemisphere Neural Processing During Speech Perception and Production Tasks. Frontiers in Human Neuroscience , 16 , Article 803163. 10.3389/fnhum.2022.803163. Green open access

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Abstract

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.

Type: Article
Title: The Effect of Right Temporal Lobe Gliomas on Left and Right Hemisphere Neural Processing During Speech Perception and Production Tasks
Location: Switzerland
Open access status: An open access version is available from UCL Discovery
DOI: 10.3389/fnhum.2022.803163
Publisher version: https://doi.org/10.3389/fnhum.2022.803163
Language: English
Additional information: Copyright © 2022 Yamamoto, Sanjuán, Pope, Parker Jones, Hope, Prejawa, Oberhuber, Mancini, Ekert, Garjardo-Vidal, Creasey, Yousry, Green and Price. 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.
Keywords: Science & Technology, Social Sciences, Life Sciences & Biomedicine, Neurosciences, Psychology, Neurosciences & Neurology, gliomas, fMRI, language, speech perception, speech production, right temporal lobe, neurosurgery, LOW-GRADE GLIOMA, TRANSCRANIAL MAGNETIC STIMULATION, CORTICOFUGAL MODULATION, SURGICAL RESECTION, LANGUAGE FUNCTION, FUNCTIONAL MRI, AWAKE SURGERY, BRAIN-TUMORS, BROCAS AREA, II GLIOMAS
UCL classification: UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences > UCL Queen Square Institute of Neurology
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences
UCL
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences > UCL Queen Square Institute of Neurology > Brain Repair and Rehabilitation
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences > Div of Psychology and Lang Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences > UCL Queen Square Institute of Neurology > Imaging Neuroscience
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Population Health Sciences > UCL GOS Institute of Child Health > Population, Policy and Practice Dept
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Population Health Sciences > UCL GOS Institute of Child Health
URI: https://discovery.ucl.ac.uk/id/eprint/10150725
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