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Differential contribution of between and within‐brain coupling to movement synchronization

A fundamental characteristic of the human brain that supports behavior is its capacity to create connections between brain regions. A promising approach holds that during social behavior, brain regions not only create connections with other brain regions within a brain, but also coordinate their act...

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Autores principales: Marton‐Alper, Inbar Z., Markus, Andrey, Nevat, Michael, Bennet, Rotem, Shamay‐Tsoory, Simone G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley & Sons, Inc. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10258530/
https://www.ncbi.nlm.nih.gov/pubmed/37195028
http://dx.doi.org/10.1002/hbm.26335
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author Marton‐Alper, Inbar Z.
Markus, Andrey
Nevat, Michael
Bennet, Rotem
Shamay‐Tsoory, Simone G.
author_facet Marton‐Alper, Inbar Z.
Markus, Andrey
Nevat, Michael
Bennet, Rotem
Shamay‐Tsoory, Simone G.
author_sort Marton‐Alper, Inbar Z.
collection PubMed
description A fundamental characteristic of the human brain that supports behavior is its capacity to create connections between brain regions. A promising approach holds that during social behavior, brain regions not only create connections with other brain regions within a brain, but also coordinate their activity with other brain regions of an interaction partner. Here we ask whether between‐brain and within‐brain coupling contribute differentially to movement synchronization. We focused on coupling between the inferior frontal gyrus (IFG), a brain region associated with the observation‐execution system, and the dorsomedial prefrontal cortex (dmPFC), a region associated with error‐monitoring and prediction. Participants, randomly divided into dyads, were simultaneously scanned with functional near infra‐red spectroscopy (fNIRS) while performing an open‐ended 3D hand movement task consisting of three conditions: back‐to‐back movement, free movement, or intentional synchronization. Results show that behavioral synchrony was higher in the intentional synchrony compared with the back‐to‐back and free movement conditions. Between‐brain coupling in the IFG and dmPFC was evident in the free movement and intentional synchrony conditions but not in the back‐to‐back condition. Importantly, between‐brain coupling was found to positively predict intentional synchrony, while within‐brain coupling was found to predict synchronization during free movement. These results indicate that during intentional synchronization, brain organization changes such that between‐brain networks, but not within‐brain connections, contribute to successful communication, pointing to shift from a within‐brain feedback loop to a two‐brains feedback loop.
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spelling pubmed-102585302023-06-13 Differential contribution of between and within‐brain coupling to movement synchronization Marton‐Alper, Inbar Z. Markus, Andrey Nevat, Michael Bennet, Rotem Shamay‐Tsoory, Simone G. Hum Brain Mapp Research Articles A fundamental characteristic of the human brain that supports behavior is its capacity to create connections between brain regions. A promising approach holds that during social behavior, brain regions not only create connections with other brain regions within a brain, but also coordinate their activity with other brain regions of an interaction partner. Here we ask whether between‐brain and within‐brain coupling contribute differentially to movement synchronization. We focused on coupling between the inferior frontal gyrus (IFG), a brain region associated with the observation‐execution system, and the dorsomedial prefrontal cortex (dmPFC), a region associated with error‐monitoring and prediction. Participants, randomly divided into dyads, were simultaneously scanned with functional near infra‐red spectroscopy (fNIRS) while performing an open‐ended 3D hand movement task consisting of three conditions: back‐to‐back movement, free movement, or intentional synchronization. Results show that behavioral synchrony was higher in the intentional synchrony compared with the back‐to‐back and free movement conditions. Between‐brain coupling in the IFG and dmPFC was evident in the free movement and intentional synchrony conditions but not in the back‐to‐back condition. Importantly, between‐brain coupling was found to positively predict intentional synchrony, while within‐brain coupling was found to predict synchronization during free movement. These results indicate that during intentional synchronization, brain organization changes such that between‐brain networks, but not within‐brain connections, contribute to successful communication, pointing to shift from a within‐brain feedback loop to a two‐brains feedback loop. John Wiley & Sons, Inc. 2023-05-17 /pmc/articles/PMC10258530/ /pubmed/37195028 http://dx.doi.org/10.1002/hbm.26335 Text en © 2023 The Authors. Human Brain Mapping published by Wiley Periodicals LLC. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Articles
Marton‐Alper, Inbar Z.
Markus, Andrey
Nevat, Michael
Bennet, Rotem
Shamay‐Tsoory, Simone G.
Differential contribution of between and within‐brain coupling to movement synchronization
title Differential contribution of between and within‐brain coupling to movement synchronization
title_full Differential contribution of between and within‐brain coupling to movement synchronization
title_fullStr Differential contribution of between and within‐brain coupling to movement synchronization
title_full_unstemmed Differential contribution of between and within‐brain coupling to movement synchronization
title_short Differential contribution of between and within‐brain coupling to movement synchronization
title_sort differential contribution of between and within‐brain coupling to movement synchronization
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10258530/
https://www.ncbi.nlm.nih.gov/pubmed/37195028
http://dx.doi.org/10.1002/hbm.26335
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