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

View ORCID ProfileKatta S., View ORCID ProfileSanzeni A., Vergassola M., View ORCID ProfileGoodman M.B.
doi: https://doi.org/10.1101/587014
Katta S.
Neuroscience Program, Stanford University, Stanford, CA 94025
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Sanzeni A.
National Institute of Mental Health Intramural Program, National Institutes of Health, Bethesda, MD 20892
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Vergassola M.
Department of Physics, University of California, San Diego, La Jolla, CA 92093
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Goodman M.B.
Neuroscience Program, Stanford University, Stanford, CA 94025Molecular and Cellular Physiology, Stanford University, Stanford, CA 94025
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  • For correspondence: mbgoodman@stanford.edu
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Abstract

Touch deforms, or strains, the skin beyond the immediate point of contact. The spatiotemporal nature of the strain field induced by touch depends on the mechanical properties of the skin and the tissues below. Somatosensory neurons that sense touch often innervate large regions of skin and rely on a set of mechano-electrical transduction channels distributed within their dendrites to detect mechanical stimuli. We sought to understand how tissue mechanics shape touch-induced mechanical strain across the skin over time and how individual channels located in different regions of the strain field contribute to the overall touch response. We leveraged C. elegans’ touch receptor neurons (TRNs) as a morphologically simple model and employed an integrated experimental-computational approach. Measuring mechanoreceptor currents (MRCs) in TRNs and performing biophysical modeling enabled us to dissect the mechanisms underlying the spatial and temporal dynamics that we observed. Consistent with the idea that strain is produced at a distance, we were able to elicit MRCs by delivering stimuli outside the anatomical receptive field. The amplitude and kinetics of the MRCs depended on both stimulus displacement and speed. Finally, we found that the main factor responsible for touch sensitivity is the recruitment of progressively more distant channels by stronger stimuli, rather than modulation of channel open probability. This principle may generalize to somatosensory neurons with more complex morphologies.

Summary Through experiment and simulation, Katta, et al. reveal that pushing faster and deeper recruits more and more distant mechano-electrical transduction channels during touch. The net result is a dynamic receptive field whose size and shape depends on tissue mechanics, stimulus parameters, and channel distribution within sensory neurons.

  • Abbreviations

    MeT
    mechano-electrical transduction
    MRC
    mechanoreceptor current
    TRN
    touch receptor neuron
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    The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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    Posted March 24, 2019.
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    Progressive recruitment of distal MEC-4 channels determines touch response strength in C. elegans
    Katta S., Sanzeni A., Vergassola M., Goodman M.B.
    bioRxiv 587014; doi: https://doi.org/10.1101/587014
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    Progressive recruitment of distal MEC-4 channels determines touch response strength in C. elegans
    Katta S., Sanzeni A., Vergassola M., Goodman M.B.
    bioRxiv 587014; doi: https://doi.org/10.1101/587014

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