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Semantic retrieval during overt picture description: Left anterior temporal or the parietal lobe?

Retrieval of semantic representations is a central process during overt speech production. There is an increasing consensus that an amodal semantic ‘hub’ must exist that draws together modality-specific representations of concepts. Based on the distribution of atrophy and the behavioral deficit of p...

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Autores principales: Geranmayeh, Fatemeh, Leech, Robert, Wise, Richard J.S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Pergamon Press 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4582804/
https://www.ncbi.nlm.nih.gov/pubmed/25497693
http://dx.doi.org/10.1016/j.neuropsychologia.2014.12.012
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author Geranmayeh, Fatemeh
Leech, Robert
Wise, Richard J.S.
author_facet Geranmayeh, Fatemeh
Leech, Robert
Wise, Richard J.S.
author_sort Geranmayeh, Fatemeh
collection PubMed
description Retrieval of semantic representations is a central process during overt speech production. There is an increasing consensus that an amodal semantic ‘hub’ must exist that draws together modality-specific representations of concepts. Based on the distribution of atrophy and the behavioral deficit of patients with the semantic variant of fronto-temporal lobar degeneration, it has been proposed that this hub is localized within both anterior temporal lobes (ATL), and is functionally connected with verbal ‘output’ systems via the left ATL. An alternative view, dating from Geschwind's proposal in 1965, is that the angular gyrus (AG) is central to object-based semantic representations. In this fMRI study we examined the connectivity of the left ATL and parietal lobe (PL) with whole brain networks known to be activated during overt picture description. We decomposed each of these two brain volumes into 15 regions of interest (ROIs), using independent component analysis. A dual regression analysis was used to establish the connectivity of each ROI with whole brain-networks. An ROI within the left anterior superior temporal sulcus (antSTS) was functionally connected to other parts of the left ATL, including anterior ventromedial left temporal cortex (partially attenuated by signal loss due to susceptibility artifact), a large left dorsolateral prefrontal region (including ‘classic’ Broca's area), extensive bilateral sensory-motor cortices, and the length of both superior temporal gyri. The time-course of this functionally connected network was associated with picture description but not with non-semantic baseline tasks. This system has the distribution expected for the production of overt speech with appropriate semantic content, and the auditory monitoring of the overt speech output. In contrast, the only left PL ROI that showed connectivity with brain systems most strongly activated by the picture-description task, was in the superior parietal lobe (supPL). This region showed connectivity with predominantly posterior cortical regions required for the visual processing of the pictorial stimuli, with additional connectivity to the dorsal left AG and a small component of the left inferior frontal gyrus. None of the other PL ROIs that included part of the left AG were activated by Speech alone. The best interpretation of these results is that the left antSTS connects the proposed semantic hub (specifically localized to ventral anterior temporal cortex based on clinical neuropsychological studies) to posterior frontal regions and sensory-motor cortices responsible for the overt production of speech.
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spelling pubmed-45828042015-10-27 Semantic retrieval during overt picture description: Left anterior temporal or the parietal lobe? Geranmayeh, Fatemeh Leech, Robert Wise, Richard J.S. Neuropsychologia Article Retrieval of semantic representations is a central process during overt speech production. There is an increasing consensus that an amodal semantic ‘hub’ must exist that draws together modality-specific representations of concepts. Based on the distribution of atrophy and the behavioral deficit of patients with the semantic variant of fronto-temporal lobar degeneration, it has been proposed that this hub is localized within both anterior temporal lobes (ATL), and is functionally connected with verbal ‘output’ systems via the left ATL. An alternative view, dating from Geschwind's proposal in 1965, is that the angular gyrus (AG) is central to object-based semantic representations. In this fMRI study we examined the connectivity of the left ATL and parietal lobe (PL) with whole brain networks known to be activated during overt picture description. We decomposed each of these two brain volumes into 15 regions of interest (ROIs), using independent component analysis. A dual regression analysis was used to establish the connectivity of each ROI with whole brain-networks. An ROI within the left anterior superior temporal sulcus (antSTS) was functionally connected to other parts of the left ATL, including anterior ventromedial left temporal cortex (partially attenuated by signal loss due to susceptibility artifact), a large left dorsolateral prefrontal region (including ‘classic’ Broca's area), extensive bilateral sensory-motor cortices, and the length of both superior temporal gyri. The time-course of this functionally connected network was associated with picture description but not with non-semantic baseline tasks. This system has the distribution expected for the production of overt speech with appropriate semantic content, and the auditory monitoring of the overt speech output. In contrast, the only left PL ROI that showed connectivity with brain systems most strongly activated by the picture-description task, was in the superior parietal lobe (supPL). This region showed connectivity with predominantly posterior cortical regions required for the visual processing of the pictorial stimuli, with additional connectivity to the dorsal left AG and a small component of the left inferior frontal gyrus. None of the other PL ROIs that included part of the left AG were activated by Speech alone. The best interpretation of these results is that the left antSTS connects the proposed semantic hub (specifically localized to ventral anterior temporal cortex based on clinical neuropsychological studies) to posterior frontal regions and sensory-motor cortices responsible for the overt production of speech. Pergamon Press 2015-09 /pmc/articles/PMC4582804/ /pubmed/25497693 http://dx.doi.org/10.1016/j.neuropsychologia.2014.12.012 Text en © 2014 The Authors http://creativecommons.org/licenses/by/3.0/ This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/3.0/).
spellingShingle Article
Geranmayeh, Fatemeh
Leech, Robert
Wise, Richard J.S.
Semantic retrieval during overt picture description: Left anterior temporal or the parietal lobe?
title Semantic retrieval during overt picture description: Left anterior temporal or the parietal lobe?
title_full Semantic retrieval during overt picture description: Left anterior temporal or the parietal lobe?
title_fullStr Semantic retrieval during overt picture description: Left anterior temporal or the parietal lobe?
title_full_unstemmed Semantic retrieval during overt picture description: Left anterior temporal or the parietal lobe?
title_short Semantic retrieval during overt picture description: Left anterior temporal or the parietal lobe?
title_sort semantic retrieval during overt picture description: left anterior temporal or the parietal lobe?
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4582804/
https://www.ncbi.nlm.nih.gov/pubmed/25497693
http://dx.doi.org/10.1016/j.neuropsychologia.2014.12.012
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