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Research ArticleResearch Article: New Research, Sensory and Motor Systems

A Somatosensory Computation That Unifies Limbs and Tools

Luke E. Miller, Cécile Fabio, Frédérique de Vignemont, Alice Roy, W. Pieter Medendorp and Alessandro Farnè
eNeuro 17 October 2023, 10 (11) ENEURO.0095-23.2023; https://doi.org/10.1523/ENEURO.0095-23.2023
Luke E. Miller
1Integrative Multisensory Perception Action and Cognition Team-ImpAct, Lyon Neuroscience Research Center, Institut National de la Santé et de la Recherche Médicale Unité 1028, Centre National de la Recherche Scientifique Unité 5292, 69500 Bron, France
2UCBL, University of Lyon 1, 69100 Villeurbanne, France
3Neuro-immersion, Hospices Civils de Lyon, 69500 Bron, France
4Donders Institute for Brain, Cognition and Behaviour, Radboud University, 6525 GD, Nijmegen, The Netherlands
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Cécile Fabio
1Integrative Multisensory Perception Action and Cognition Team-ImpAct, Lyon Neuroscience Research Center, Institut National de la Santé et de la Recherche Médicale Unité 1028, Centre National de la Recherche Scientifique Unité 5292, 69500 Bron, France
2UCBL, University of Lyon 1, 69100 Villeurbanne, France
3Neuro-immersion, Hospices Civils de Lyon, 69500 Bron, France
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Frédérique de Vignemont
7Institut Jean Nicod, Department of Cognitive Studies, Ecole Normale Superieure, Paris Sciences et Lettres University, 75005 Paris, France
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Alice Roy
6Laboratoire Dynamique du Langage, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5596, 69007 Lyon, France
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W. Pieter Medendorp
4Donders Institute for Brain, Cognition and Behaviour, Radboud University, 6525 GD, Nijmegen, The Netherlands
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Alessandro Farnè
1Integrative Multisensory Perception Action and Cognition Team-ImpAct, Lyon Neuroscience Research Center, Institut National de la Santé et de la Recherche Médicale Unité 1028, Centre National de la Recherche Scientifique Unité 5292, 69500 Bron, France
2UCBL, University of Lyon 1, 69100 Villeurbanne, France
3Neuro-immersion, Hospices Civils de Lyon, 69500 Bron, France
5Center for Mind/Brain Sciences, University of Trento, 38068 Rovereto, Italy
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Abstract

It is often claimed that tools are embodied by their user, but whether the brain actually repurposes its body-based computations to perform similar tasks with tools is not known. A fundamental computation for localizing touch on the body is trilateration. Here, the location of touch on a limb is computed by integrating estimates of the distance between sensory input and its boundaries (e.g., elbow and wrist of the forearm). As evidence of this computational mechanism, tactile localization on a limb is most precise near its boundaries and lowest in the middle. Here, we show that the brain repurposes trilateration to localize touch on a tool, despite large differences in initial sensory input compared with touch on the body. In a large sample of participants, we found that localizing touch on a tool produced the signature of trilateration, with highest precision close to the base and tip of the tool. A computational model of trilateration provided a good fit to the observed localization behavior. To further demonstrate the computational plausibility of repurposing trilateration, we implemented it in a three-layer neural network that was based on principles of probabilistic population coding. This network determined hit location in tool-centered coordinates by using a tool’s unique pattern of vibrations when contacting an object. Simulations demonstrated the expected signature of trilateration, in line with the behavioral patterns. Our results have important implications for how trilateration may be implemented by somatosensory neural populations. We conclude that trilateration is likely a fundamental spatial computation that unifies limbs and tools.

  • computation
  • embodiment
  • space
  • tactile localization
  • tool use

Footnotes

  • The authors declare no competing financial interests.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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A Somatosensory Computation That Unifies Limbs and Tools
Luke E. Miller, Cécile Fabio, Frédérique de Vignemont, Alice Roy, W. Pieter Medendorp, Alessandro Farnè
eNeuro 17 October 2023, 10 (11) ENEURO.0095-23.2023; DOI: 10.1523/ENEURO.0095-23.2023

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A Somatosensory Computation That Unifies Limbs and Tools
Luke E. Miller, Cécile Fabio, Frédérique de Vignemont, Alice Roy, W. Pieter Medendorp, Alessandro Farnè
eNeuro 17 October 2023, 10 (11) ENEURO.0095-23.2023; DOI: 10.1523/ENEURO.0095-23.2023
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Keywords

  • computation
  • embodiment
  • space
  • tactile localization
  • tool use

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