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Network modeling of dynamic brain interactions predicts emergence of neural information that supports human cognitive behavior

How cognitive task behavior is generated by brain network interactions is a central question in neuroscience. Answering this question calls for the development of novel analysis tools that can firstly capture neural signatures of task information with high spatial and temporal precision (the “where...

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Autores principales: Mill, Ravi D., Hamilton, Julia L., Winfield, Emily C., Lalta, Nicole, Chen, Richard H., Cole, Michael W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9387855/
https://www.ncbi.nlm.nih.gov/pubmed/35980898
http://dx.doi.org/10.1371/journal.pbio.3001686
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author Mill, Ravi D.
Hamilton, Julia L.
Winfield, Emily C.
Lalta, Nicole
Chen, Richard H.
Cole, Michael W.
author_facet Mill, Ravi D.
Hamilton, Julia L.
Winfield, Emily C.
Lalta, Nicole
Chen, Richard H.
Cole, Michael W.
author_sort Mill, Ravi D.
collection PubMed
description How cognitive task behavior is generated by brain network interactions is a central question in neuroscience. Answering this question calls for the development of novel analysis tools that can firstly capture neural signatures of task information with high spatial and temporal precision (the “where and when”) and then allow for empirical testing of alternative network models of brain function that link information to behavior (the “how”). We outline a novel network modeling approach suited to this purpose that is applied to noninvasive functional neuroimaging data in humans. We first dynamically decoded the spatiotemporal signatures of task information in the human brain by combining MRI-individualized source electroencephalography (EEG) with multivariate pattern analysis (MVPA). A newly developed network modeling approach—dynamic activity flow modeling—then simulated the flow of task-evoked activity over more causally interpretable (relative to standard functional connectivity [FC] approaches) resting-state functional connections (dynamic, lagged, direct, and directional). We demonstrate the utility of this modeling approach by applying it to elucidate network processes underlying sensory–motor information flow in the brain, revealing accurate predictions of empirical response information dynamics underlying behavior. Extending the model toward simulating network lesions suggested a role for the cognitive control networks (CCNs) as primary drivers of response information flow, transitioning from early dorsal attention network-dominated sensory-to-response transformation to later collaborative CCN engagement during response selection. These results demonstrate the utility of the dynamic activity flow modeling approach in identifying the generative network processes underlying neurocognitive phenomena.
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spelling pubmed-93878552022-08-19 Network modeling of dynamic brain interactions predicts emergence of neural information that supports human cognitive behavior Mill, Ravi D. Hamilton, Julia L. Winfield, Emily C. Lalta, Nicole Chen, Richard H. Cole, Michael W. PLoS Biol Methods and Resources How cognitive task behavior is generated by brain network interactions is a central question in neuroscience. Answering this question calls for the development of novel analysis tools that can firstly capture neural signatures of task information with high spatial and temporal precision (the “where and when”) and then allow for empirical testing of alternative network models of brain function that link information to behavior (the “how”). We outline a novel network modeling approach suited to this purpose that is applied to noninvasive functional neuroimaging data in humans. We first dynamically decoded the spatiotemporal signatures of task information in the human brain by combining MRI-individualized source electroencephalography (EEG) with multivariate pattern analysis (MVPA). A newly developed network modeling approach—dynamic activity flow modeling—then simulated the flow of task-evoked activity over more causally interpretable (relative to standard functional connectivity [FC] approaches) resting-state functional connections (dynamic, lagged, direct, and directional). We demonstrate the utility of this modeling approach by applying it to elucidate network processes underlying sensory–motor information flow in the brain, revealing accurate predictions of empirical response information dynamics underlying behavior. Extending the model toward simulating network lesions suggested a role for the cognitive control networks (CCNs) as primary drivers of response information flow, transitioning from early dorsal attention network-dominated sensory-to-response transformation to later collaborative CCN engagement during response selection. These results demonstrate the utility of the dynamic activity flow modeling approach in identifying the generative network processes underlying neurocognitive phenomena. Public Library of Science 2022-08-18 /pmc/articles/PMC9387855/ /pubmed/35980898 http://dx.doi.org/10.1371/journal.pbio.3001686 Text en © 2022 Mill et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Methods and Resources
Mill, Ravi D.
Hamilton, Julia L.
Winfield, Emily C.
Lalta, Nicole
Chen, Richard H.
Cole, Michael W.
Network modeling of dynamic brain interactions predicts emergence of neural information that supports human cognitive behavior
title Network modeling of dynamic brain interactions predicts emergence of neural information that supports human cognitive behavior
title_full Network modeling of dynamic brain interactions predicts emergence of neural information that supports human cognitive behavior
title_fullStr Network modeling of dynamic brain interactions predicts emergence of neural information that supports human cognitive behavior
title_full_unstemmed Network modeling of dynamic brain interactions predicts emergence of neural information that supports human cognitive behavior
title_short Network modeling of dynamic brain interactions predicts emergence of neural information that supports human cognitive behavior
title_sort network modeling of dynamic brain interactions predicts emergence of neural information that supports human cognitive behavior
topic Methods and Resources
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9387855/
https://www.ncbi.nlm.nih.gov/pubmed/35980898
http://dx.doi.org/10.1371/journal.pbio.3001686
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