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A neural surveyor to map touch on the body

Perhaps the most recognizable sensory map in all of neuroscience is the somatosensory homunculus. Although it seems straightforward, this simple representation belies the complex link between an activation in a somatotopic map and the associated touch location on the body. Any isolated activation is...

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Autores principales: Miller, Luke E., Fabio, Cécile, Azaroual, Malika, Muret, Dollyane, van Beers, Robert J., Farnè, Alessandro, Medendorp, W. Pieter
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8740579/
https://www.ncbi.nlm.nih.gov/pubmed/34983835
http://dx.doi.org/10.1073/pnas.2102233118
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author Miller, Luke E.
Fabio, Cécile
Azaroual, Malika
Muret, Dollyane
van Beers, Robert J.
Farnè, Alessandro
Medendorp, W. Pieter
author_facet Miller, Luke E.
Fabio, Cécile
Azaroual, Malika
Muret, Dollyane
van Beers, Robert J.
Farnè, Alessandro
Medendorp, W. Pieter
author_sort Miller, Luke E.
collection PubMed
description Perhaps the most recognizable sensory map in all of neuroscience is the somatosensory homunculus. Although it seems straightforward, this simple representation belies the complex link between an activation in a somatotopic map and the associated touch location on the body. Any isolated activation is spatially ambiguous without a neural decoder that can read its position within the entire map, but how this is computed by neural networks is unknown. We propose that the somatosensory system implements multilateration, a common computation used by surveying and global positioning systems to localize objects. Specifically, to decode touch location on the body, multilateration estimates the relative distance between the afferent input and the boundaries of a body part (e.g., the joints of a limb). We show that a simple feedforward neural network, which captures several fundamental receptive field properties of cortical somatosensory neurons, can implement a Bayes-optimal multilateral computation. Simulations demonstrated that this decoder produced a pattern of localization variability between two boundaries that was unique to multilateration. Finally, we identify this computational signature of multilateration in actual psychophysical experiments, suggesting that it is a candidate computational mechanism underlying tactile localization.
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spelling pubmed-87405792022-06-30 A neural surveyor to map touch on the body Miller, Luke E. Fabio, Cécile Azaroual, Malika Muret, Dollyane van Beers, Robert J. Farnè, Alessandro Medendorp, W. Pieter Proc Natl Acad Sci U S A Biological Sciences Perhaps the most recognizable sensory map in all of neuroscience is the somatosensory homunculus. Although it seems straightforward, this simple representation belies the complex link between an activation in a somatotopic map and the associated touch location on the body. Any isolated activation is spatially ambiguous without a neural decoder that can read its position within the entire map, but how this is computed by neural networks is unknown. We propose that the somatosensory system implements multilateration, a common computation used by surveying and global positioning systems to localize objects. Specifically, to decode touch location on the body, multilateration estimates the relative distance between the afferent input and the boundaries of a body part (e.g., the joints of a limb). We show that a simple feedforward neural network, which captures several fundamental receptive field properties of cortical somatosensory neurons, can implement a Bayes-optimal multilateral computation. Simulations demonstrated that this decoder produced a pattern of localization variability between two boundaries that was unique to multilateration. Finally, we identify this computational signature of multilateration in actual psychophysical experiments, suggesting that it is a candidate computational mechanism underlying tactile localization. National Academy of Sciences 2021-12-30 2022-01-04 /pmc/articles/PMC8740579/ /pubmed/34983835 http://dx.doi.org/10.1073/pnas.2102233118 Text en Copyright © 2021 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Miller, Luke E.
Fabio, Cécile
Azaroual, Malika
Muret, Dollyane
van Beers, Robert J.
Farnè, Alessandro
Medendorp, W. Pieter
A neural surveyor to map touch on the body
title A neural surveyor to map touch on the body
title_full A neural surveyor to map touch on the body
title_fullStr A neural surveyor to map touch on the body
title_full_unstemmed A neural surveyor to map touch on the body
title_short A neural surveyor to map touch on the body
title_sort neural surveyor to map touch on the body
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8740579/
https://www.ncbi.nlm.nih.gov/pubmed/34983835
http://dx.doi.org/10.1073/pnas.2102233118
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