Resin models of Drosophila strain sensors highlight mechanical pre-filtering of sensory inputs

Locomotion can be modified and reinforced through the utilization of sensory feedback. A type of sensory structure, commonly found in the legs of insects, is strain sensors called campaniform sensilla (CS). These are embedded in the rigid cuticle and commonly found in groups and fields, some of which contain a variety of CS sizes and orientations. The CS groups and fields on the legs are consistent across individuals of the same species, but the topography of the local cuticle and the number of sensilla may vary. In order to investigate the effect of these variations on force encoding, we utilize a previously published physical modeling approach to begin to address three questions: (i) how might the cuticular contour (i.e. deviation in elevation from the local cuticle patch) amplify and reorient the strain that CS encode? (ii) How might the absence of some CS impact the strain encoded by the remaining CS in that field? and (iii) How might these two mechanisms impact how a field encodes the direction of loading on a limb? Using 3D printed resin mechanical models of aDrosophilaCS field with 11 CS, we measured the displacement at each sensillum's location via a corresponding strain gauge rosette (i.e. nonparallel strain gauges). We 3D printed additional 'block' models that flattened the contour and further "reduced" models that omitted some caps from the field. Comparing the realistic, block, and reduced models revealed that, as predicted, raised cuticular contouring can rotate the directional sensitivity of a single CS. Removing some caps from the field changed the magnitude, but rarely the directional sensitivity, of cap strain. Both contour and cap removal alter the population response to different loading directions. These results suggest that inter-individual differences could greatly impact strain sensingin vivoand provide concrete hypotheses for future biological experiments. We conclude by discussing implications for motor control and robotics, as well as limitations and improvements to our method.