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.

Keywords: embodiment; experts; fMRI; neuroimaging; plasticity; tools.

Figure 1.

Neuroimaging hypotheses and experimental paradigm. A, An illustration of the predictions generated by the proposed hypotheses for the neuroimaging experiment. Under the first, embodiment prediction, extensive tool use could lead to representations of hands and tools to become neurally integrated, such that tools are represented more similarly to hands, suggesting that tools are embodied. A second prediction is that experts will show greater categorization of representations of hands and tools, such that the neural representations for hands and tools would become differentiated and more dissimilar to each other. This would suggest that perhaps that visual experience with tools leads to an increased sharpening of the representation. B, Examples of the video stimuli shown during the fMRI scan depicting grasping actions performed by each effector category: hands, litter pickers, or tongs [the videos can be downloaded on the Open Science Framework (OSF) at https://osf.io/p4q3y/]. To control for any potential laterality effects, the stimuli included both left and right-handed versions. C, ROI probability map for all participants (n = 19) showing hand and tool selective OTC, defined using independent functional data. For each participant and hemisphere, the top 100 most activated voxels of OTC were selected based on a hands + tools > objects + low-level visual stimulus contrast. ROIs from all participants were superimposed. Warmer colors represent voxels that were included in a greater number of individual ROIs. Group-specific probability maps of OTC can be downloaded on the Open Science Framework at https://osf.io/p4q3y/.

Figure 2.

Expert tool users represent tools less like hands. A, Group RDMs showing the pairwise distances (cross-validated Mahalanobis distance) between each video condition. Each element in the matrix was averaged across left and right OTC. Warmer colors indicate the conditions that evoked more dissimilar patterns of activity. Group multidimensional scaling plots derived from these group RDMs can be accessed at https://osf.io/p4q3y/. B, Bar plot of individual participants for each cross-effector category distance pair: hands ↔ litter pickers, hands ↔ tongs, and litter pickers ↔ tongs. These values are generated by averaging the 8 × 8 pairwise comparison values, for each effector category pair, for each subject individually. Dark gray values reflect expert tool users (n = 7). Light gray values reflect novices (n = 12). Circles depict individual subject means. Values indicate group means ± standard error. Asterisks denote significance as follows; *p < 0.05, ***p < 0.005.

Figure 3.

Analyses in visual cortex and left parietal cortex. A, A V1 ROI probability map was constructed for all participants (n = 19). Warmer colors represent voxels that were included in a greater number of individual ROIs. B, Group RDMs for V1 showing the pairwise distances (cross-validated Mahalanobis distance) between each video condition. Warmer colors indicate the conditions that evoked more dissimilar patterns of activity. C, A left parietal cortex ROI probability map for all participants (n = 19) showing hand and tool selective voxels was defined using independent functional data. ROIs from all participants were superimposed. Warmer colors represent voxels that were included in a greater number of individual ROIs. D, Group RDMs for left parietal cortex showing the pairwise distances (cross-validated Mahalanobis distance) between each video condition. Warmer colors indicate the conditions that evoked more dissimilar patterns of activity.