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Information flow across the cortical timescale hierarchy during narrative construction

When listening to spoken narratives, we must integrate information over multiple, concurrent timescales, building up from words to sentences to paragraphs to a coherent narrative. Recent evidence suggests that the brain relies on a chain of hierarchically organized areas with increasing temporal rec...

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Autores principales: Chang, Claire H. C., Nastase, Samuel A., Hasson, Uri
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9907070/
https://www.ncbi.nlm.nih.gov/pubmed/36508677
http://dx.doi.org/10.1073/pnas.2209307119
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author Chang, Claire H. C.
Nastase, Samuel A.
Hasson, Uri
author_facet Chang, Claire H. C.
Nastase, Samuel A.
Hasson, Uri
author_sort Chang, Claire H. C.
collection PubMed
description When listening to spoken narratives, we must integrate information over multiple, concurrent timescales, building up from words to sentences to paragraphs to a coherent narrative. Recent evidence suggests that the brain relies on a chain of hierarchically organized areas with increasing temporal receptive windows to process naturalistic narratives. We hypothesized that the structure of this cortical processing hierarchy should result in an observable sequence of response lags between networks comprising the hierarchy during narrative comprehension. This study uses functional MRI to estimate the response lags between functional networks during narrative comprehension. We use intersubject cross-correlation analysis to capture network connectivity driven by the shared stimulus. We found a fixed temporal sequence of response lags—on the scale of several seconds—starting in early auditory areas, followed by language areas, the attention network, and lastly the default mode network. This gradient is consistent across eight distinct stories but absent in data acquired during rest or using a scrambled story stimulus, supporting our hypothesis that narrative construction gives rise to internetwork lags. Finally, we build a simple computational model for the neural dynamics underlying the construction of nested narrative features. Our simulations illustrate how the gradual accumulation of information within the boundaries of nested linguistic events, accompanied by increased activity at each level of the processing hierarchy, can give rise to the observed lag gradient.
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spelling pubmed-99070702023-06-12 Information flow across the cortical timescale hierarchy during narrative construction Chang, Claire H. C. Nastase, Samuel A. Hasson, Uri Proc Natl Acad Sci U S A Biological Sciences When listening to spoken narratives, we must integrate information over multiple, concurrent timescales, building up from words to sentences to paragraphs to a coherent narrative. Recent evidence suggests that the brain relies on a chain of hierarchically organized areas with increasing temporal receptive windows to process naturalistic narratives. We hypothesized that the structure of this cortical processing hierarchy should result in an observable sequence of response lags between networks comprising the hierarchy during narrative comprehension. This study uses functional MRI to estimate the response lags between functional networks during narrative comprehension. We use intersubject cross-correlation analysis to capture network connectivity driven by the shared stimulus. We found a fixed temporal sequence of response lags—on the scale of several seconds—starting in early auditory areas, followed by language areas, the attention network, and lastly the default mode network. This gradient is consistent across eight distinct stories but absent in data acquired during rest or using a scrambled story stimulus, supporting our hypothesis that narrative construction gives rise to internetwork lags. Finally, we build a simple computational model for the neural dynamics underlying the construction of nested narrative features. Our simulations illustrate how the gradual accumulation of information within the boundaries of nested linguistic events, accompanied by increased activity at each level of the processing hierarchy, can give rise to the observed lag gradient. National Academy of Sciences 2022-12-12 2022-12-20 /pmc/articles/PMC9907070/ /pubmed/36508677 http://dx.doi.org/10.1073/pnas.2209307119 Text en Copyright © 2022 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
Chang, Claire H. C.
Nastase, Samuel A.
Hasson, Uri
Information flow across the cortical timescale hierarchy during narrative construction
title Information flow across the cortical timescale hierarchy during narrative construction
title_full Information flow across the cortical timescale hierarchy during narrative construction
title_fullStr Information flow across the cortical timescale hierarchy during narrative construction
title_full_unstemmed Information flow across the cortical timescale hierarchy during narrative construction
title_short Information flow across the cortical timescale hierarchy during narrative construction
title_sort information flow across the cortical timescale hierarchy during narrative construction
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9907070/
https://www.ncbi.nlm.nih.gov/pubmed/36508677
http://dx.doi.org/10.1073/pnas.2209307119
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