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Somatosensory neurons integrate the geometry of skin deformation and mechanotransduction channels to shape touch sensing

Touch sensation hinges on force transfer across the skin and activation of mechanosensitive ion channels along the somatosensory neurons that invade the skin. This skin-nerve sensory system demands a quantitative model that spans the application of mechanical loads to channel activation. Unlike prio...

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Autores principales: Sanzeni, Alessandro, Katta, Samata, Petzold, Bryan, Pruitt, Beth L, Goodman, Miriam B, Vergassola, Massimo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6692131/
https://www.ncbi.nlm.nih.gov/pubmed/31407662
http://dx.doi.org/10.7554/eLife.43226
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author Sanzeni, Alessandro
Katta, Samata
Petzold, Bryan
Pruitt, Beth L
Goodman, Miriam B
Vergassola, Massimo
author_facet Sanzeni, Alessandro
Katta, Samata
Petzold, Bryan
Pruitt, Beth L
Goodman, Miriam B
Vergassola, Massimo
author_sort Sanzeni, Alessandro
collection PubMed
description Touch sensation hinges on force transfer across the skin and activation of mechanosensitive ion channels along the somatosensory neurons that invade the skin. This skin-nerve sensory system demands a quantitative model that spans the application of mechanical loads to channel activation. Unlike prior models of the dynamic responses of touch receptor neurons in Caenorhabditis elegans (Eastwood et al., 2015), which substituted a single effective channel for the ensemble along the TRNs, this study integrates body mechanics and the spatial recruitment of the various channels. We demonstrate that this model captures mechanical properties of the worm’s body and accurately reproduces neural responses to simple stimuli. It also captures responses to complex stimuli featuring non-trivial spatial patterns, like extended or multiple contacts that could not be addressed otherwise. We illustrate the importance of these effects with new experiments revealing that skin-neuron composites respond to pre-indentation with increased currents rather than adapting to persistent stimulation.
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spelling pubmed-66921312019-08-16 Somatosensory neurons integrate the geometry of skin deformation and mechanotransduction channels to shape touch sensing Sanzeni, Alessandro Katta, Samata Petzold, Bryan Pruitt, Beth L Goodman, Miriam B Vergassola, Massimo eLife Physics of Living Systems Touch sensation hinges on force transfer across the skin and activation of mechanosensitive ion channels along the somatosensory neurons that invade the skin. This skin-nerve sensory system demands a quantitative model that spans the application of mechanical loads to channel activation. Unlike prior models of the dynamic responses of touch receptor neurons in Caenorhabditis elegans (Eastwood et al., 2015), which substituted a single effective channel for the ensemble along the TRNs, this study integrates body mechanics and the spatial recruitment of the various channels. We demonstrate that this model captures mechanical properties of the worm’s body and accurately reproduces neural responses to simple stimuli. It also captures responses to complex stimuli featuring non-trivial spatial patterns, like extended or multiple contacts that could not be addressed otherwise. We illustrate the importance of these effects with new experiments revealing that skin-neuron composites respond to pre-indentation with increased currents rather than adapting to persistent stimulation. eLife Sciences Publications, Ltd 2019-08-13 /pmc/articles/PMC6692131/ /pubmed/31407662 http://dx.doi.org/10.7554/eLife.43226 Text en © 2019, Sanzeni et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Physics of Living Systems
Sanzeni, Alessandro
Katta, Samata
Petzold, Bryan
Pruitt, Beth L
Goodman, Miriam B
Vergassola, Massimo
Somatosensory neurons integrate the geometry of skin deformation and mechanotransduction channels to shape touch sensing
title Somatosensory neurons integrate the geometry of skin deformation and mechanotransduction channels to shape touch sensing
title_full Somatosensory neurons integrate the geometry of skin deformation and mechanotransduction channels to shape touch sensing
title_fullStr Somatosensory neurons integrate the geometry of skin deformation and mechanotransduction channels to shape touch sensing
title_full_unstemmed Somatosensory neurons integrate the geometry of skin deformation and mechanotransduction channels to shape touch sensing
title_short Somatosensory neurons integrate the geometry of skin deformation and mechanotransduction channels to shape touch sensing
title_sort somatosensory neurons integrate the geometry of skin deformation and mechanotransduction channels to shape touch sensing
topic Physics of Living Systems
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6692131/
https://www.ncbi.nlm.nih.gov/pubmed/31407662
http://dx.doi.org/10.7554/eLife.43226
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