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Spatiotemporally distributed frontotemporal networks for sentence reading

Reading a sentence entails integrating the meanings of individual words to infer more complex, higher-order meaning. This highly rapid and complex human behavior is known to engage the inferior frontal gyrus (IFG) and middle temporal gyrus (MTG) in the language-dominant hemisphere, yet whether there...

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Autores principales: Woolnough, Oscar, Donos, Cristian, Murphy, Elliot, Rollo, Patrick S., Roccaforte, Zachary J., Dehaene, Stanislas, Tandon, Nitin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10151604/
https://www.ncbi.nlm.nih.gov/pubmed/37068244
http://dx.doi.org/10.1073/pnas.2300252120
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author Woolnough, Oscar
Donos, Cristian
Murphy, Elliot
Rollo, Patrick S.
Roccaforte, Zachary J.
Dehaene, Stanislas
Tandon, Nitin
author_facet Woolnough, Oscar
Donos, Cristian
Murphy, Elliot
Rollo, Patrick S.
Roccaforte, Zachary J.
Dehaene, Stanislas
Tandon, Nitin
author_sort Woolnough, Oscar
collection PubMed
description Reading a sentence entails integrating the meanings of individual words to infer more complex, higher-order meaning. This highly rapid and complex human behavior is known to engage the inferior frontal gyrus (IFG) and middle temporal gyrus (MTG) in the language-dominant hemisphere, yet whether there are distinct contributions of these regions to sentence reading is still unclear. To probe these neural spatiotemporal dynamics, we used direct intracranial recordings to measure neural activity while reading sentences, meaning-deficient Jabberwocky sentences, and lists of words or pseudowords. We isolated two functionally and spatiotemporally distinct frontotemporal networks, each sensitive to distinct aspects of word and sentence composition. The first distributed network engages the IFG and MTG, with IFG activity preceding MTG. Activity in this network ramps up over the duration of a sentence and is reduced or absent during Jabberwocky and word lists, implying its role in the derivation of sentence-level meaning. The second network engages the superior temporal gyrus and the IFG, with temporal responses leading those in frontal lobe, and shows greater activation for each word in a list than those in sentences, suggesting that sentential context enables greater efficiency in the lexical and/or phonological processing of individual words. These adjacent, yet spatiotemporally dissociable neural mechanisms for word- and sentence-level processes shed light on the richly layered semantic networks that enable us to fluently read. These results imply distributed, dynamic computation across the frontotemporal language network rather than a clear dichotomy between the contributions of frontal and temporal structures.
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spelling pubmed-101516042023-10-17 Spatiotemporally distributed frontotemporal networks for sentence reading Woolnough, Oscar Donos, Cristian Murphy, Elliot Rollo, Patrick S. Roccaforte, Zachary J. Dehaene, Stanislas Tandon, Nitin Proc Natl Acad Sci U S A Biological Sciences Reading a sentence entails integrating the meanings of individual words to infer more complex, higher-order meaning. This highly rapid and complex human behavior is known to engage the inferior frontal gyrus (IFG) and middle temporal gyrus (MTG) in the language-dominant hemisphere, yet whether there are distinct contributions of these regions to sentence reading is still unclear. To probe these neural spatiotemporal dynamics, we used direct intracranial recordings to measure neural activity while reading sentences, meaning-deficient Jabberwocky sentences, and lists of words or pseudowords. We isolated two functionally and spatiotemporally distinct frontotemporal networks, each sensitive to distinct aspects of word and sentence composition. The first distributed network engages the IFG and MTG, with IFG activity preceding MTG. Activity in this network ramps up over the duration of a sentence and is reduced or absent during Jabberwocky and word lists, implying its role in the derivation of sentence-level meaning. The second network engages the superior temporal gyrus and the IFG, with temporal responses leading those in frontal lobe, and shows greater activation for each word in a list than those in sentences, suggesting that sentential context enables greater efficiency in the lexical and/or phonological processing of individual words. These adjacent, yet spatiotemporally dissociable neural mechanisms for word- and sentence-level processes shed light on the richly layered semantic networks that enable us to fluently read. These results imply distributed, dynamic computation across the frontotemporal language network rather than a clear dichotomy between the contributions of frontal and temporal structures. National Academy of Sciences 2023-04-17 2023-04-25 /pmc/articles/PMC10151604/ /pubmed/37068244 http://dx.doi.org/10.1073/pnas.2300252120 Text en Copyright © 2023 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Woolnough, Oscar
Donos, Cristian
Murphy, Elliot
Rollo, Patrick S.
Roccaforte, Zachary J.
Dehaene, Stanislas
Tandon, Nitin
Spatiotemporally distributed frontotemporal networks for sentence reading
title Spatiotemporally distributed frontotemporal networks for sentence reading
title_full Spatiotemporally distributed frontotemporal networks for sentence reading
title_fullStr Spatiotemporally distributed frontotemporal networks for sentence reading
title_full_unstemmed Spatiotemporally distributed frontotemporal networks for sentence reading
title_short Spatiotemporally distributed frontotemporal networks for sentence reading
title_sort spatiotemporally distributed frontotemporal networks for sentence reading
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10151604/
https://www.ncbi.nlm.nih.gov/pubmed/37068244
http://dx.doi.org/10.1073/pnas.2300252120
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