Expert Tool Users Show Increased Differentiation between Visual Representations of Hands and Tools.

ABSTRACT

The idea that when we use a tool we incorporate it into the neural representation of our body (embodiment) has been a major inspiration for philosophy, science, and engineering. While theoretically appealing, there is little direct evidence for tool embodiment at the neural level. Using functional magnetic resonance imaging (fMRI) in male and female human subjects, we investigated whether expert tool users (London litter pickers n = 7) represent their expert tool more like a hand (neural embodiment) or less like a hand (neural differentiation), as compared with a group of tool novices (n = 12). During fMRI scans, participants viewed first-person videos depicting grasps performed by either a hand, litter picker, or a non-expert grasping tool. Using representational similarity analysis (RSA), differences in the representational structure of hands and tools were measured within occipitotemporal cortex (OTC). Contrary to the neural embodiment theory, we find that the experts group represent their own tool less like a hand (not more) relative to novices. Using a case-study approach, we further replicated this effect, independently, in five of the seven individual expert litter pickers, as compared with the novices. An exploratory analysis in left parietal cortex, a region implicated in visuomotor representations of hands and tools, also indicated that experts do not visually represent their tool more similar to hands, compared with novices. Together, our findings suggest that extensive tool use leads to an increased neural differentiation between visual representations of hands and tools. This evidence provides an important alternative framework to the prominent tool embodiment theory.SIGNIFICANCE STATEMENT It is commonly thought that tool use leads to the assimilation of the tool into the neural representation of the body, a process referred to as embodiment. Here, we demonstrate that expert tool users (London litter pickers) neurally represent their own tool less like a hand (not more), compared with novices. Our findings advance our current understanding for how experience shapes functional organization in high-order visual cortex. Further, this evidence provides an alternative framework to the prominent tool embodiment theory, suggesting instead that experience with tools leads to more distinct, separable hand and tool representations.