The ability to extend sensory information processing beyond the nervous system1 has been observed throughout the animal kingdom; for example, when rodents palpate objects using whiskers2 and spiders localize prey using webs3. We investigated whether the ability to sense objects with tools4,5,6,7,8,9 represents an analogous information processing scheme in humans. Here we provide evidence from behavioural psychophysics, structural mechanics and neuronal modelling, which shows that tools are treated by the nervous system as sensory extensions of the body rather than as simple distal links between the hand and the environment10,11. We first demonstrate that tool users can accurately sense where an object contacts a wooden rod, just as is possible on the skin. We next demonstrate that the impact location is encoded by the modal response of the tool upon impact, reflecting a pre-neuronal stage of mechanical information processing akin to sensing with whiskers2 and webs3. Lastly, we use a computational model of tactile afferents12 to demonstrate that impact location can be rapidly re-encoded into a temporally precise spiking code. This code predicts the behaviour of human participants, providing evidence that the information encoded in motifs shapes localization. Thus, we show that this sensory capability emerges from the functional coupling between the material, biomechanical and neural levels of information processing13,14.
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We thank F. Volland for his help constructing the experimental setup; B. Miller and A. Schork for their statistical advice; and L. Quadt, A. Roy, E. Leonardis and K. Kilteni for their feedback on an earlier version of the manuscript. This work was supported by an FRM postdoctoral fellowship to L.E.M., ANR-16-CE28-0015 Developmental Tool Mastery to A.F. and V.H., a Leverhulme Trust Visiting Professorship Grant to V.H. and IHU CeSaMe ANR-10-IBHU-0003, Defi Auton Sublima and the James S. McDonnell Scholar Award to A.F. All work was performed within the framework of the LABEX CORTEX (ANR-11-LABX-0042) of Université de Lyon.
Nature thanks S. Bensmaia and G. Stanley for their contribution to the peer review of this work.
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Scientific Reports (2019)