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Toward naturalistic neuroscience: Mechanisms underlying the flattening of brain hierarchy in movie-watching compared to rest and task

Identifying the functional specialization of the brain has moved from using cognitive tasks and resting state to using ecological relevant, naturalistic movies. We leveraged a large-scale neuroimaging dataset to directly investigate the hierarchical reorganization of functional brain activity when w...

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Autores principales: Kringelbach, Morten L., Perl, Yonatan Sanz, Tagliazucchi, Enzo, Deco, Gustavo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Association for the Advancement of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9839335/
https://www.ncbi.nlm.nih.gov/pubmed/36638163
http://dx.doi.org/10.1126/sciadv.ade6049
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author Kringelbach, Morten L.
Perl, Yonatan Sanz
Tagliazucchi, Enzo
Deco, Gustavo
author_facet Kringelbach, Morten L.
Perl, Yonatan Sanz
Tagliazucchi, Enzo
Deco, Gustavo
author_sort Kringelbach, Morten L.
collection PubMed
description Identifying the functional specialization of the brain has moved from using cognitive tasks and resting state to using ecological relevant, naturalistic movies. We leveraged a large-scale neuroimaging dataset to directly investigate the hierarchical reorganization of functional brain activity when watching naturalistic films compared to performing seven cognitive tasks and resting. A thermodynamics-inspired whole-brain model paradigm revealed the generative underlying mechanisms for changing the balance in causal interactions between brain regions in different conditions. Paradoxically, the hierarchy is flatter for movie-watching, and the level of nonreversibility is significantly smaller in comparison to both rest and tasks, where the latter in turn have the highest levels of hierarchy and nonreversibility. The underlying mechanisms were revealed by the model-based generative effective connectivity (GEC). Naturalistic films could therefore provide a fast and convenient way to measure important changes in GEC (integrating functional and anatomical connectivity) found in, for example, neuropsychiatric disorders. Overall, this study demonstrates the benefits of moving toward a more naturalistic neuroscience.
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spelling pubmed-98393352023-01-24 Toward naturalistic neuroscience: Mechanisms underlying the flattening of brain hierarchy in movie-watching compared to rest and task Kringelbach, Morten L. Perl, Yonatan Sanz Tagliazucchi, Enzo Deco, Gustavo Sci Adv Neuroscience Identifying the functional specialization of the brain has moved from using cognitive tasks and resting state to using ecological relevant, naturalistic movies. We leveraged a large-scale neuroimaging dataset to directly investigate the hierarchical reorganization of functional brain activity when watching naturalistic films compared to performing seven cognitive tasks and resting. A thermodynamics-inspired whole-brain model paradigm revealed the generative underlying mechanisms for changing the balance in causal interactions between brain regions in different conditions. Paradoxically, the hierarchy is flatter for movie-watching, and the level of nonreversibility is significantly smaller in comparison to both rest and tasks, where the latter in turn have the highest levels of hierarchy and nonreversibility. The underlying mechanisms were revealed by the model-based generative effective connectivity (GEC). Naturalistic films could therefore provide a fast and convenient way to measure important changes in GEC (integrating functional and anatomical connectivity) found in, for example, neuropsychiatric disorders. Overall, this study demonstrates the benefits of moving toward a more naturalistic neuroscience. American Association for the Advancement of Science 2023-01-13 /pmc/articles/PMC9839335/ /pubmed/36638163 http://dx.doi.org/10.1126/sciadv.ade6049 Text en Copyright © 2023 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC). https://creativecommons.org/licenses/by-nc/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license (https://creativecommons.org/licenses/by-nc/4.0/) , which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.
spellingShingle Neuroscience
Kringelbach, Morten L.
Perl, Yonatan Sanz
Tagliazucchi, Enzo
Deco, Gustavo
Toward naturalistic neuroscience: Mechanisms underlying the flattening of brain hierarchy in movie-watching compared to rest and task
title Toward naturalistic neuroscience: Mechanisms underlying the flattening of brain hierarchy in movie-watching compared to rest and task
title_full Toward naturalistic neuroscience: Mechanisms underlying the flattening of brain hierarchy in movie-watching compared to rest and task
title_fullStr Toward naturalistic neuroscience: Mechanisms underlying the flattening of brain hierarchy in movie-watching compared to rest and task
title_full_unstemmed Toward naturalistic neuroscience: Mechanisms underlying the flattening of brain hierarchy in movie-watching compared to rest and task
title_short Toward naturalistic neuroscience: Mechanisms underlying the flattening of brain hierarchy in movie-watching compared to rest and task
title_sort toward naturalistic neuroscience: mechanisms underlying the flattening of brain hierarchy in movie-watching compared to rest and task
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9839335/
https://www.ncbi.nlm.nih.gov/pubmed/36638163
http://dx.doi.org/10.1126/sciadv.ade6049
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