Sensing with tools extends somatosensory processing beyond the body

• Published in: Nature (London) 2018-09, Vol.561 (7722), p.239-242
• Main Authors: Miller, Luke E., Montroni, Luca, Koun, Eric, Salemme, Romeo, Hayward, Vincent, Farnè, Alessandro
• Format: Article
• Language: English
• Subjects: 631/378/2620/2621; 631/378/2649/1723; 631/477/2811; Action Potentials; Adult; Analysis; Animals; Biomechanical Phenomena - physiology; Biomechanics; Blindness - physiopathology; Coding; Cognitive science; Computational neuroscience; Data processing; Experiments; Female; Hand - physiology; Human behavior; Human body; Humanities and Social Sciences; Humans; Hypotheses; Information processing; Letter; Localization; Male; Mechanoreceptors - metabolism; Modal response; multidisciplinary; Nervous system; Neurons; Neuroscience; Object recognition; Perception (Psychology); Perception - physiology; Prey; Psychophysics; Rodents; Science; Science (multidisciplinary); Senses; Sensory integration; Skin; Somatosensory Cortex - physiology; Spiders; Touch - physiology; Vibration; Vibrissae - physiology; Wood; Young Adult
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/s41586-018-0460-0

The ability to extend sensory information processing beyond the nervous system 1 has been observed throughout the animal kingdom; for example, when rodents palpate objects using whiskers 2 and spiders localize prey using webs 3 . We investigated whether the ability to sense objects with tools 4 – 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 environment 10 , 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 whiskers 2 and webs 3 . Lastly, we use a computational model of tactile afferents 12 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 processing 13 , 14 . Tools are embodied by the human somatosensory system, serving as sensory extensions of the human body.