Distributed processing of load and movement feedback in the premotor network controlling an insect leg joint

In legged animals, integration of information from various proprioceptors in and on the appendages by local premotor networks in the central nervous system is crucial for controlling motor output. To ensure posture maintenance and precise active movements, information about limb loading and movement is required. In insects, various groups of campaniform sensilla (CS) measure forces and loads acting in different directions on the leg, and the femoral chordotonal organ (fCO) provides information about movement of the femur-tibia (FTi) joint. In this study, we used extra- and intracellular recordings of extensor tibiae (ExtTi) and retractor coxae (RetCx) motor neurons (MNs) and identified local premotor nonspiking interneurons (NSIs) and mechanical stimulation of the fCO and tibial or trochanterofemoral CS (tiCS, tr/fCS), to investigate the premotor network architecture underlying multimodal proprioceptive integration. We found that load feedback from tiCS altered the strength of movement-elicited resistance reflexes and determined the specificity of ExtTi and RetCx MN responses to various load and movement stimuli. These responses were mediated by a common population of identified NSIs into which synaptic inputs from the fCO, tiCS, and tr/fCS are distributed, and whose effects onto ExtTi MNs can be antagonistic for both stimulus modalities. Multimodal sensory signal interaction was found at the level of single NSIs and MNs. The results provide evidence that load and movement feedback are integrated in a multimodal, distributed local premotor network consisting of antagonistic elements controlling movements of the FTi joint, thus substantially extending current knowledge on how legged motor systems achieve fine-tuned motor control.NEW & NOTEWORTHY Proprioception is crucial for motor control in legged animals. We show the extent to which processing of movement (fCO) and load (CS) signals overlaps in the local premotor network of an insect leg. Multimodal signals converge onto the same set of interneurons, and our knowledge about distributed, antagonistic processing is extended to incorporate multiple modalities within one perceptual neuronal framework.