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A Somatosensory Computation That Unifies Limbs and Tools

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 com...

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Autores principales: Miller, Luke E., Fabio, Cécile, de Vignemont, Frédérique, Roy, Alice, Medendorp, W. Pieter, Farnè, Alessandro
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10668222/
https://www.ncbi.nlm.nih.gov/pubmed/37848289
http://dx.doi.org/10.1523/ENEURO.0095-23.2023
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author Miller, Luke E.
Fabio, Cécile
de Vignemont, Frédérique
Roy, Alice
Medendorp, W. Pieter
Farnè, Alessandro
author_facet Miller, Luke E.
Fabio, Cécile
de Vignemont, Frédérique
Roy, Alice
Medendorp, W. Pieter
Farnè, Alessandro
author_sort Miller, Luke E.
collection PubMed
description 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.
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spelling pubmed-106682222023-11-10 A Somatosensory Computation That Unifies Limbs and Tools Miller, Luke E. Fabio, Cécile de Vignemont, Frédérique Roy, Alice Medendorp, W. Pieter Farnè, Alessandro eNeuro Research Article: New Research 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. Society for Neuroscience 2023-11-10 /pmc/articles/PMC10668222/ /pubmed/37848289 http://dx.doi.org/10.1523/ENEURO.0095-23.2023 Text en Copyright © 2023 Miller et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article: New Research
Miller, Luke E.
Fabio, Cécile
de Vignemont, Frédérique
Roy, Alice
Medendorp, W. Pieter
Farnè, Alessandro
A Somatosensory Computation That Unifies Limbs and Tools
title A Somatosensory Computation That Unifies Limbs and Tools
title_full A Somatosensory Computation That Unifies Limbs and Tools
title_fullStr A Somatosensory Computation That Unifies Limbs and Tools
title_full_unstemmed A Somatosensory Computation That Unifies Limbs and Tools
title_short A Somatosensory Computation That Unifies Limbs and Tools
title_sort somatosensory computation that unifies limbs and tools
topic Research Article: New Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10668222/
https://www.ncbi.nlm.nih.gov/pubmed/37848289
http://dx.doi.org/10.1523/ENEURO.0095-23.2023
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