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ABSTRACT Legged locomotion in terrestrial animals is often essential for mating and survival, and locomotor behavior must be robust and adaptable to be successful. This adaptability is largely provided by proprioceptors monitoring positions and movements of body parts and providing feedback to other components of locomotor networks. In insects, proprioceptive chordotonal organs span joints and encode parameters of relative movement between segments. Previous studies have used whole-organ ablation, reduced preparations or broad physiological manipulations to impair the function of the femoral chordotonal organ (fCO), which monitors the femur–tibia joint, and have demonstrated its contribution to interleg coordination and walking behavior. The fCO in Drosophila melanogaster comprises groups of neurons that differ in their morphology and encoding properties (club, hook, claw); sub-population-level manipulations of fCO function have not been methodologically accessible. Here, we took advantage of the genetic toolkit available in D. melanogaster to identify sub-populations of fCO neurons and used transient optogenetic inhibition to investigate their roles in locomotor coordination. Our findings demonstrate that optogenetic inhibition of a subset of club and hook neurons replicates the effects of inhibiting the whole fCO; when inhibited alone, however, the individual subset types did not strongly affect spatial aspects of single-leg kinematics. Moreover, fCO subsets seem to play only a minor role in interleg temporal coordination. Thus, the fCO contains functionally distinct subgroups, and this functional classification may differ from those based on anatomy and encoding properties; this should be investigated in future studies of proprioceptors and their involvement in locomotor networks. 

Insect load sensors, called campaniform sensilla (CS), measure strain changes within the cuticle of appendages. This mechanotransduction provides the neuromuscular system with feedback for posture and locomotion. Owing to their diverse morphology and arrangement, CS can encode different strain directions. We used nano-computed tomography and finite-element analysis to investigate how different CS morphologies within one location—the femoral CS field of the leg in the fruit fly Drosophila —interact under load. By investigating the influence of CS substructures' material properties during simulated limb displacement with naturalistic forces, we could show that CS substructures (i.e. socket and collar) influence strain distribution throughout the whole CS field. Altered socket and collar elastic moduli resulted in 5% relative differences in displacement, and the artificial removal of all sockets caused differences greater than 20% in cap displacement. Apparently, CS sockets support the distribution of distal strain to more proximal CS, while collars alter CS displacement more locally. Harder sockets can increase or decrease CS displacement depending on sensor location. Furthermore, high-resolution imaging revealed that sockets are interconnected in subcuticular rows. In summary, the sensitivity of individual CS is dependent on the configuration of other CS and their substructures.