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On the functional brain networks involved in tool-related action understanding

Tool-use skills represent a significant cognitive leap in human evolution, playing a crucial role in the emergence of complex technologies. Yet, the neural mechanisms underlying such capabilities are still debated. Here we explore with fMRI the functional brain networks involved in tool-related acti...

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Autores principales: Federico, Giovanni, Osiurak, François, Ciccarelli, Giuseppina, Ilardi, Ciro Rosario, Cavaliere, Carlo, Tramontano, Liberatore, Alfano, Vincenzo, Migliaccio, Miriana, Di Cecca, Angelica, Salvatore, Marco, Brandimonte, Maria Antonella
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10645930/
https://www.ncbi.nlm.nih.gov/pubmed/37964121
http://dx.doi.org/10.1038/s42003-023-05518-2
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author Federico, Giovanni
Osiurak, François
Ciccarelli, Giuseppina
Ilardi, Ciro Rosario
Cavaliere, Carlo
Tramontano, Liberatore
Alfano, Vincenzo
Migliaccio, Miriana
Di Cecca, Angelica
Salvatore, Marco
Brandimonte, Maria Antonella
author_facet Federico, Giovanni
Osiurak, François
Ciccarelli, Giuseppina
Ilardi, Ciro Rosario
Cavaliere, Carlo
Tramontano, Liberatore
Alfano, Vincenzo
Migliaccio, Miriana
Di Cecca, Angelica
Salvatore, Marco
Brandimonte, Maria Antonella
author_sort Federico, Giovanni
collection PubMed
description Tool-use skills represent a significant cognitive leap in human evolution, playing a crucial role in the emergence of complex technologies. Yet, the neural mechanisms underlying such capabilities are still debated. Here we explore with fMRI the functional brain networks involved in tool-related action understanding. Participants viewed images depicting action-consistent (e.g., nail-hammer) and action-inconsistent (e.g., scarf-hammer) object-tool pairs, under three conditions: semantic (recognizing the tools previously seen in the pairs), mechanical (assessing the usability of the pairs), and control (looking at the pairs without explicit tasks). During the observation of the pairs, task-based left-brain functional connectivity differed within conditions. Compared to the control, both the semantic and mechanical conditions exhibited co-activations in dorsal (precuneus) and ventro-dorsal (inferior frontal gyrus) regions. However, the semantic condition recruited medial and posterior temporal areas, whereas the mechanical condition engaged inferior parietal and posterior temporal regions. Also, when distinguishing action-consistent from action-inconsistent pairs, an extensive frontotemporal neural circuit was activated. These findings support recent accounts that view tool-related action understanding as the combined product of semantic and mechanical knowledge. Furthermore, they emphasize how the left inferior parietal and anterior temporal lobes might be considered as hubs for the cross-modal integration of physical and conceptual knowledge, respectively.
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spelling pubmed-106459302023-11-14 On the functional brain networks involved in tool-related action understanding Federico, Giovanni Osiurak, François Ciccarelli, Giuseppina Ilardi, Ciro Rosario Cavaliere, Carlo Tramontano, Liberatore Alfano, Vincenzo Migliaccio, Miriana Di Cecca, Angelica Salvatore, Marco Brandimonte, Maria Antonella Commun Biol Article Tool-use skills represent a significant cognitive leap in human evolution, playing a crucial role in the emergence of complex technologies. Yet, the neural mechanisms underlying such capabilities are still debated. Here we explore with fMRI the functional brain networks involved in tool-related action understanding. Participants viewed images depicting action-consistent (e.g., nail-hammer) and action-inconsistent (e.g., scarf-hammer) object-tool pairs, under three conditions: semantic (recognizing the tools previously seen in the pairs), mechanical (assessing the usability of the pairs), and control (looking at the pairs without explicit tasks). During the observation of the pairs, task-based left-brain functional connectivity differed within conditions. Compared to the control, both the semantic and mechanical conditions exhibited co-activations in dorsal (precuneus) and ventro-dorsal (inferior frontal gyrus) regions. However, the semantic condition recruited medial and posterior temporal areas, whereas the mechanical condition engaged inferior parietal and posterior temporal regions. Also, when distinguishing action-consistent from action-inconsistent pairs, an extensive frontotemporal neural circuit was activated. These findings support recent accounts that view tool-related action understanding as the combined product of semantic and mechanical knowledge. Furthermore, they emphasize how the left inferior parietal and anterior temporal lobes might be considered as hubs for the cross-modal integration of physical and conceptual knowledge, respectively. Nature Publishing Group UK 2023-11-14 /pmc/articles/PMC10645930/ /pubmed/37964121 http://dx.doi.org/10.1038/s42003-023-05518-2 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Federico, Giovanni
Osiurak, François
Ciccarelli, Giuseppina
Ilardi, Ciro Rosario
Cavaliere, Carlo
Tramontano, Liberatore
Alfano, Vincenzo
Migliaccio, Miriana
Di Cecca, Angelica
Salvatore, Marco
Brandimonte, Maria Antonella
On the functional brain networks involved in tool-related action understanding
title On the functional brain networks involved in tool-related action understanding
title_full On the functional brain networks involved in tool-related action understanding
title_fullStr On the functional brain networks involved in tool-related action understanding
title_full_unstemmed On the functional brain networks involved in tool-related action understanding
title_short On the functional brain networks involved in tool-related action understanding
title_sort on the functional brain networks involved in tool-related action understanding
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10645930/
https://www.ncbi.nlm.nih.gov/pubmed/37964121
http://dx.doi.org/10.1038/s42003-023-05518-2
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