Subsets of leg proprioceptors influence leg kinematics but not interleg coordination in Drosophila melanogaster walking.

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.

Location and arrangement of campaniform sensilla in Drosophila melanogaster.

Sensory systems provide input to motor networks on the state of the body and environment. One such sensory system in insects is the campaniform sensilla (CS), which detect deformations of the exoskeleton arising from resisted movements or external perturbations. When physical strain is applied to the cuticle, CS external structures are compressed, leading to transduction in an internal sensory neuron. In Drosophila melanogaster, the distribution of CS on the exoskeleton has not been comprehensively described. To investigate CS number, location, spatial arrangement, and potential differences between individuals, we compared the front, middle, and hind legs of multiple flies using scanning electron microscopy. Additionally, we imaged the entire body surface to confirm known CS locations. On the legs, the number and relative arrangement of CS varied between individuals, and single CS of corresponding segments showed characteristic differences between legs. This knowledge is fundamental for studying the relevance of cuticular strain information within the complex neuromuscular networks controlling posture and movement. This comprehensive account of all D. melanogaster CS helps set the stage for experimental investigations into their responsivity, sensitivity, and roles in sensory acquisition and motor control in a light-weight model organism.

Static stability predicts the continuum of interleg coordination patterns in Drosophila.

During walking, insects must coordinate the movements of their six legs for efficient locomotion. This interleg coordination is speed dependent: fast walking in insects is associated with tripod coordination patterns, whereas slow walking is associated with more variable, tetrapod-like patterns. To date, however, there has been no comprehensive explanation as to why these speed-dependent shifts in interleg coordination should occur in insects. Tripod coordination would be sufficient at low walking speeds. The fact that insects use a different interleg coordination pattern at lower speeds suggests that it is more optimal or advantageous at these speeds. Furthermore, previous studies focused on discrete tripod and tetrapod coordination patterns. Experimental data, however, suggest that changes observed in interleg coordination are part of a speed-dependent spectrum. Here, we explore these issues in relation to static stability as an important aspect for interleg coordination in Drosophila We created a model that uses basic experimentally measured parameters in fruit flies to find the interleg phase relationships that maximize stability for a given walking speed. The model predicted a continuum of interleg coordination patterns spanning the complete range of walking speeds as well as an anteriorly directed swing phase progression. Furthermore, for low walking speeds, the model predicted tetrapod-like patterns to be most stable, whereas at high walking speeds, tripod coordination emerged as most optimal. Finally, we validated the basic assumption of a continuum of interleg coordination patterns in a large set of experimental data from walking fruit flies and compared these data with the model-based predictions.