Touch deforms, or strains, the skin beyond the immediate point of contact. The spatiotemporal nature of the touch-induced strain fields depend on the mechanical properties of the skin and the tissues below. Somatosensory neurons that sense touch branch out within the skin and rely on a set of mechano-electrical transduction channels distributed within their dendrites to detect mechanical stimuli. Here, 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 Caenorhabditis elegans’ touch receptor neurons as a simple model amenable to in vivo whole-cell patch-clamp recording and an integrated experimental-computational approach to dissect the mechanisms underlying the spatial and temporal dynamics we observed. Consistent with the idea that strain is produced at a distance, we show that delivering strong stimuli outside the anatomical extent of the neuron is sufficient to evoke MRCs. 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.
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September 18 2019
Progressive recruitment of distal MEC-4 channels determines touch response strength in C. elegans
Samata Katta
,
Samata Katta
1
Neuroscience Program, Stanford University, Stanford, CA
4
Department of Molecular and Cellular Physiology, Stanford University, Stanford, CA
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Alessandro Sanzeni
,
Alessandro Sanzeni
2
National Institute of Mental Health Intramural Program, National Institutes of Health, Bethesda, MD
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Alakananda Das
,
Alakananda Das
4
Department of Molecular and Cellular Physiology, Stanford University, Stanford, CA
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Massimo Vergassola
,
Massimo Vergassola
3
Department of Physics, University of California, San Diego, La Jolla, CA
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Miriam B. Goodman
1
Neuroscience Program, Stanford University, Stanford, CA
4
Department of Molecular and Cellular Physiology, Stanford University, Stanford, CA
Correspondence to Miriam B. Goodman: mbgoodman@stanford.edu
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Samata Katta
1
Neuroscience Program, Stanford University, Stanford, CA
4
Department of Molecular and Cellular Physiology, Stanford University, Stanford, CA
Alessandro Sanzeni
2
National Institute of Mental Health Intramural Program, National Institutes of Health, Bethesda, MD
Alakananda Das
4
Department of Molecular and Cellular Physiology, Stanford University, Stanford, CA
Massimo Vergassola
3
Department of Physics, University of California, San Diego, La Jolla, CA
Miriam B. Goodman
1
Neuroscience Program, Stanford University, Stanford, CA
4
Department of Molecular and Cellular Physiology, Stanford University, Stanford, CA
Correspondence to Miriam B. Goodman: mbgoodman@stanford.edu
J Gen Physiol (2019) 151 (10): 1213–1230.
Article history
Received:
March 25 2019
Accepted:
August 23 2019
Connected Content
Commentary:
A quantal code for touch intensity in C. elegans
Citation
Samata Katta, Alessandro Sanzeni, Alakananda Das, Massimo Vergassola, Miriam B. Goodman; Progressive recruitment of distal MEC-4 channels determines touch response strength in C. elegans. J Gen Physiol 7 October 2019; 151 (10): 1213–1230. doi: https://doi.org/10.1085/jgp.201912374
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