Literature DB >> 31407662

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

Alessandro Sanzeni1,2, Samata Katta3, Bryan Petzold4, Beth L Pruitt4,5, Miriam B Goodman6, Massimo Vergassola1.   

Abstract

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.
© 2019, Sanzeni et al.

Entities:  

Keywords:  C. elegans; physics of living systems; somatosensory neurons response; tissue mechanics; touch sensation

Mesh:

Year:  2019        PMID: 31407662      PMCID: PMC6692131          DOI: 10.7554/eLife.43226

Source DB:  PubMed          Journal:  Elife        ISSN: 2050-084X            Impact factor:   8.140


  46 in total

1.  Mechanical signatures of transducer gating in the Drosophila ear.

Authors:  Jörg T Albert; Björn Nadrowski; Martin C Göpfert
Journal:  Curr Biol       Date:  2007-05-24       Impact factor: 10.834

Review 2.  Neurosensory mechanotransduction.

Authors:  Martin Chalfie
Journal:  Nat Rev Mol Cell Biol       Date:  2009-01       Impact factor: 94.444

3.  Worms under Pressure: Bulk Mechanical Properties of C. elegans Are Independent of the Cuticle.

Authors:  William Gilpin; Sravanti Uppaluri; Clifford P Brangwynne
Journal:  Biophys J       Date:  2015-04-21       Impact factor: 4.033

4.  Biomechanical analysis of gait adaptation in the nematode Caenorhabditis elegans.

Authors:  Christopher Fang-Yen; Matthieu Wyart; Julie Xie; Risa Kawai; Tom Kodger; Sway Chen; Quan Wen; Aravinthan D T Samuel
Journal:  Proc Natl Acad Sci U S A       Date:  2010-11-03       Impact factor: 11.205

5.  Active currents regulate sensitivity and dynamic range in C. elegans neurons.

Authors:  M B Goodman; D H Hall; L Avery; S R Lockery
Journal:  Neuron       Date:  1998-04       Impact factor: 17.173

6.  Indentation of ellipsoidal and cylindrical elastic shells.

Authors:  Dominic Vella; Amin Ajdari; Ashkan Vaziri; Arezki Boudaoud
Journal:  Phys Rev Lett       Date:  2012-10-05       Impact factor: 9.161

7.  The MEC-4 DEG/ENaC channel of Caenorhabditis elegans touch receptor neurons transduces mechanical signals.

Authors:  Robert O'Hagan; Martin Chalfie; Miriam B Goodman
Journal:  Nat Neurosci       Date:  2004-12-05       Impact factor: 24.884

8.  Caenorhabditis elegans exoskeleton collagen COL-19: an adult-specific marker for collagen modification and assembly, and the analysis of organismal morphology.

Authors:  Melanie C Thein; Gillian McCormack; Alan D Winter; Iain L Johnstone; Charles B Shoemaker; Antony P Page
Journal:  Dev Dyn       Date:  2003-03       Impact factor: 3.780

9.  A NOMPC-dependent membrane-microtubule connector is a candidate for the gating spring in fly mechanoreceptors.

Authors:  Xin Liang; Johnson Madrid; Roland Gärtner; Jean-Marc Verbavatz; Christoph Schiklenk; Michaela Wilsch-Bräuninger; Aliona Bogdanova; Florian Stenger; Axel Voigt; Jonathon Howard
Journal:  Curr Biol       Date:  2013-04-11       Impact factor: 10.834

10.  The multipurpose 15-protofilament microtubules in C. elegans have specific roles in mechanosensation.

Authors:  Alexander Bounoutas; Robert O'Hagan; Martin Chalfie
Journal:  Curr Biol       Date:  2009-07-16       Impact factor: 10.834

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  5 in total

1.  Reciprocal interactions between transforming growth factor beta signaling and collagens: Insights from Caenorhabditis elegans.

Authors:  Miriam B Goodman; Cathy Savage-Dunn
Journal:  Dev Dyn       Date:  2021-09-28       Impact factor: 3.780

2.  Progressive recruitment of distal MEC-4 channels determines touch response strength in C. elegans.

Authors:  Samata Katta; Alessandro Sanzeni; Alakananda Das; Massimo Vergassola; Miriam B Goodman
Journal:  J Gen Physiol       Date:  2019-09-18       Impact factor: 4.086

3.  Touch-induced mechanical strain in somatosensory neurons is independent of extracellular matrix mutations in Caenorhabditis elegans.

Authors:  Adam L Nekimken; Beth L Pruitt; Miriam B Goodman
Journal:  Mol Biol Cell       Date:  2020-06-24       Impact factor: 4.138

Review 4.  The Rheology of the Carotid Sinus: A Path Toward Bioinspired Intervention.

Authors:  Andrew Iskander; Coskun Bilgi; Rotem Naftalovich; Ilker Hacihaliloglu; Tolga Berkman; Daniel Naftalovich; Niema Pahlevan
Journal:  Front Bioeng Biotechnol       Date:  2021-06-10

5.  A quantal code for touch intensity in C. elegans.

Authors:  Katherine M Perks; Jonathan T Pierce
Journal:  J Gen Physiol       Date:  2019-10-25       Impact factor: 4.086

  5 in total

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