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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...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2023
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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. |
format | Online Article Text |
id | pubmed-10151604 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
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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