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Observed Manipulation Enhances Left Fronto-Parietal Activations in the Processing of Unfamiliar Tools

Tools represent a special class of objects, as functional details of tools can afford certain actions. In addition, information gained via prior experience with tools can be accessed on a semantic level, providing a basis for meaningful object interactions. Conceptual representations of tools also e...

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Autores principales: Rüther, Norma Naima, Tettamanti, Marco, Cappa, Stefano F., Bellebaum, Christian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4049811/
https://www.ncbi.nlm.nih.gov/pubmed/24911053
http://dx.doi.org/10.1371/journal.pone.0099401
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author Rüther, Norma Naima
Tettamanti, Marco
Cappa, Stefano F.
Bellebaum, Christian
author_facet Rüther, Norma Naima
Tettamanti, Marco
Cappa, Stefano F.
Bellebaum, Christian
author_sort Rüther, Norma Naima
collection PubMed
description Tools represent a special class of objects, as functional details of tools can afford certain actions. In addition, information gained via prior experience with tools can be accessed on a semantic level, providing a basis for meaningful object interactions. Conceptual representations of tools also encompass knowledge about tool manipulation which can be acquired via direct (active manipulation) or indirect (observation of others manipulating objects) motor experience. The present study aimed to explore the impact of observation of manipulation on the neural processing of previously unfamiliar, manipulable objects. Brain activity was assessed by means of functional magnetic resonance imaging while participants accomplished a visual matching task involving pictures of the novel objects before and after they received object-related training. Three training session in which subjects observed an experimenter manipulating one set of objects and visually explored another set of objects were used to make subjects familiar with the tools and to allow the formation of new tool representations. A control object set was not part of the training. Training-related brain activation increases were found for observed manipulation objects compared to not trained objects in a left-hemispheric network consisting of inferior frontal gyrus (iFG) pars opercularis and triangularis and supramarginal/angular gyrus. This illustrates that direct manipulation experience is not required to elicit tool-associated activation changes in the action system. While the iFG activation might indicate a close relationship between the areas involved in tool representation and those involved in observational knowledge acquisition, the parietal activation is discussed in terms of non-semantic effects of object affordances and hand-tool spatial relationships.
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spelling pubmed-40498112014-06-18 Observed Manipulation Enhances Left Fronto-Parietal Activations in the Processing of Unfamiliar Tools Rüther, Norma Naima Tettamanti, Marco Cappa, Stefano F. Bellebaum, Christian PLoS One Research Article Tools represent a special class of objects, as functional details of tools can afford certain actions. In addition, information gained via prior experience with tools can be accessed on a semantic level, providing a basis for meaningful object interactions. Conceptual representations of tools also encompass knowledge about tool manipulation which can be acquired via direct (active manipulation) or indirect (observation of others manipulating objects) motor experience. The present study aimed to explore the impact of observation of manipulation on the neural processing of previously unfamiliar, manipulable objects. Brain activity was assessed by means of functional magnetic resonance imaging while participants accomplished a visual matching task involving pictures of the novel objects before and after they received object-related training. Three training session in which subjects observed an experimenter manipulating one set of objects and visually explored another set of objects were used to make subjects familiar with the tools and to allow the formation of new tool representations. A control object set was not part of the training. Training-related brain activation increases were found for observed manipulation objects compared to not trained objects in a left-hemispheric network consisting of inferior frontal gyrus (iFG) pars opercularis and triangularis and supramarginal/angular gyrus. This illustrates that direct manipulation experience is not required to elicit tool-associated activation changes in the action system. While the iFG activation might indicate a close relationship between the areas involved in tool representation and those involved in observational knowledge acquisition, the parietal activation is discussed in terms of non-semantic effects of object affordances and hand-tool spatial relationships. Public Library of Science 2014-06-09 /pmc/articles/PMC4049811/ /pubmed/24911053 http://dx.doi.org/10.1371/journal.pone.0099401 Text en © 2014 Rüther et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Rüther, Norma Naima
Tettamanti, Marco
Cappa, Stefano F.
Bellebaum, Christian
Observed Manipulation Enhances Left Fronto-Parietal Activations in the Processing of Unfamiliar Tools
title Observed Manipulation Enhances Left Fronto-Parietal Activations in the Processing of Unfamiliar Tools
title_full Observed Manipulation Enhances Left Fronto-Parietal Activations in the Processing of Unfamiliar Tools
title_fullStr Observed Manipulation Enhances Left Fronto-Parietal Activations in the Processing of Unfamiliar Tools
title_full_unstemmed Observed Manipulation Enhances Left Fronto-Parietal Activations in the Processing of Unfamiliar Tools
title_short Observed Manipulation Enhances Left Fronto-Parietal Activations in the Processing of Unfamiliar Tools
title_sort observed manipulation enhances left fronto-parietal activations in the processing of unfamiliar tools
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4049811/
https://www.ncbi.nlm.nih.gov/pubmed/24911053
http://dx.doi.org/10.1371/journal.pone.0099401
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