Force sensing in small animals: recording response properties and modeling of tibial campaniform sensilla in blow flies

Abstract

Detecting force is an essential part of control of posture and walking in many animals. We have characterized and modeled sense organs (campaniform sensilla) that detect forces in larger insects. In the present study, we have recorded the activities of the hindleg tibial group of sensilla in blow flies (Calliphora vicina), animals with very low body weight. Forces applied to the leg as ramp and hold functions, with joint movements resisted, elicited discharges that reflected both the force magnitude and rate of change of forces. Furthermore, sensory signals showed hysteresis and firing was strongly inhibited by small phasic decreases when forces were applied as waveforms that gradually increased to reach a level (asymptotic exponential functions). These results were also tested in a mathematical model of force encoding by campaniform sensilla in larger insects, which successfully reproduced the receptor responses. These findings support the idea that force detection scales to body weight and that monitoring force magnitude and dynamics may be necessary even in animals with minimal mass. Force detection may be ubiquitous because it monitors the effectiveness of muscle contractions. It can also alert the nervous system to leg slipping or destabilizing perturbations and, thus, be advantageous in both small and large animals and in walking machines.NEW & NOTEWORTHY Force sensing is advantageous in walking and can signal leg slipping that could destabilize support of body weight, prior to changes in body position. Recordings of strain-detecting campaniform sensilla in blow fly legs showed force encoding in ranges reflecting their minimal body weight but firing was also inhibited by very small transient force decreases. A mathematical model of the receptors reproduced these characteristics and could aid in control of walking machines, independent of size and mass.

Keywords: blow fly; campaniform sensilla; force encoding; mathematical model; walking.