Sensory signals of unloading in insects are tuned to distinguish leg slipping from load variations in gait: experimental and modeling studies.

In control of walking, sensory signals of decreasing forces are used to regulate leg lifting in initiation of swing and to detect loss of substrate grip (leg slipping). We used extracellular recordings in two insect species to characterize and model responses to force decrements of tibial campaniform sensilla, receptors that detect forces as cuticular strains. Discharges to decreasing forces did not occur upon direct stimulation of the sites of mechanotransduction (cuticular caps) but were readily elicited by bending forces applied to the leg. Responses to bending force decreases were phasic but had rate sensitivities similar to discharges elicited by force increases in the opposite direction. Application of stimuli of equivalent amplitude at different offset levels showed that discharges were strongly dependent upon the tonic level of loading: firing was maximal to complete unloading of the leg but substantially decreased or eliminated by sustained loads. The contribution of cuticle properties to sensory responses was also evaluated: discharges to force increases showed decreased adaptation when mechanical stress relaxation was minimized; firing to force decreases could be related to viscoelastic "creep" in the cuticle. Discharges to force decrements apparently occur due to cuticle viscoelasticity that generates transient strains similar to bending in the opposite direction. Tuning of sensory responses through cuticular and membrane properties effectively distinguishes loss of substrate grip/complete unloading from force variations due to gait in walking. We have successfully reproduced these properties in a mathematical model of the receptors. Sensors with similar tuning could fulfil these functions in legs of walking machines.NEW & NOTEWORTHY Decreases in loading of legs are important in the regulation of posture and walking in both vertebrates and invertebrates. Recordings of activities of tibial campaniform sensilla, which encode forces in insects, showed that their responses are specifically tuned to detect force decreases at the end of the stance phase of walking or when a leg slips. These results have been reproduced in a mathematical model of the receptors and also have potential applications in robotics.

Gradients in mechanotransduction of force and body weight in insects.

Posture and walking require support of the body weight, which is thought to be detected by sensory receptors in the legs. Specificity in sensory encoding occurs through the numerical distribution, size and response range of sense organs. We have studied campaniform sensilla, receptors that detect forces as strains in the insect exoskeleton. The sites of mechanotransduction (cuticular caps) were imaged by light and confocal microscopy in four species (stick insects, cockroaches, blow flies and Drosophila). The numbers of receptors and cap diameters were determined in projection images. Similar groups of receptors are present in the legs of each species (flies lack Group 2 on the anterior trochanter). The number of receptors is generally related to the body weight but similar numbers are found in blow flies and Drosophila, despite a 30 fold difference in their weight. Imaging data indicate that the gradient (range) of cap sizes may more closely correlate with the body weight: the range of cap sizes is larger in blow flies than in Drosophila but similar to that found in juvenile cockroaches. These studies support the idea that morphological properties of force-detecting sensory receptors in the legs may be tuned to reflect the body weight.