Abstract

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.

Highlights

  • To interact meaningfully with objects in the environment, individuals must be able to identify interaction sites that are part of the objects’ appearances, an object-characteristic that is often related to the influential concept of ‘‘affordances’’ [1]

  • Many neuroimaging studies have shown activations in a frontoparietal network during the processing of tool stimuli, suggesting that regions involved in tool-related actions are activated when pictures of tools are seen or tool sounds are heard. It appears that this activation reflects the automatic recruitment of underlying neural motor patterns related to hand movements and grasping as well as the access to object-associated goals, which are integrated into tool concepts (e.g., [2,3,4,5,6]; for review, see [7]). In support of this view, Grezes and Decety (2002) showed that the processing of tool-stimuli leads to the activation of left inferior parietal lobule and left inferior frontal gyrus, irrespective of a specific task [8]

  • The present study aimed to elucidate the impact of observed manipulation on the neural processing of previously unfamiliar tool-like objects

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Summary

Introduction

To interact meaningfully with objects in the environment, individuals must be able to identify interaction sites that are part of the objects’ appearances, an object-characteristic that is often related to the influential concept of ‘‘affordances’’ [1]. Many neuroimaging studies have shown activations in a frontoparietal network during the processing of tool stimuli, suggesting that regions involved in tool-related actions are activated when pictures of tools are seen or tool sounds are heard It appears that this activation reflects the automatic recruitment of underlying neural motor patterns related to hand movements and grasping as well as the access to object-associated goals, which are integrated into tool concepts (e.g., [2,3,4,5,6]; for review, see [7]). In support of this view, Grezes and Decety (2002) showed that the processing of tool-stimuli leads to the activation of left inferior parietal lobule (iPL) and left inferior frontal gyrus (iFG; BA45), irrespective of a specific task [8]

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