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

Abstract

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. AbstractTouch 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.

Touch-induced mechanical strain in somatosensory neurons is independent of extracellular matrix mutations inCaenorhabditis elegans

“…Such global changes in strain are too slow to activate the TRNs ( Eastwood et al. , 2015 ; Katta et al. , 2019 ).…”

“…, 2004 ; Cueva et al. , 2007 ; Katta et al. , 2019 ), but are disrupted in ECM mutants ( Emtage et al.…”

“…Slow stimuli fail to activate MeT currents and their size increases with stimulus frequency, indicating that activation of MeT channels in their native environment depends on tissue viscoelasticity ( Eastwood et al. , 2015 ; Katta et al. , 2019 ; Sanzeni et al.…”

“…Although slow, movement-induced physical deformations of the worm’s body and its neurons are too slow to activate MeT currents in the TRNs ( Eastwood et al. , 2015 ; Katta et al. , 2019 ), these undulatory movements produce mechanical strains of up to 40% ( Krieg et al.…”

Conserved basal lamina proteins, laminin and nidogen, are repurposed to organize mechanosensory complexes responsible for touch sensation

“…To learn more, we directly recorded MRCs in control and nid-1 mutant mutants. To optimize our ability to detect a partial loss-of-function, we used an ultrafast mechanical stimulator that evokes currents that are approximately five-fold larger than those evoked by slower stimuli (Katta et al, 2019). Using this approach, we found that MRCs were qualitatively similar in nid-1 mutants and wild-type controls (Figure 5H), but that MRCs were smaller in nid-1 mutants (Figure 5I).…”