Divergent neural circuits for proprioceptive and exteroceptive sensing of the Drosophila leg

Somatosensory neurons provide the nervous system with information about mechanical forces originating inside and outside the body. Here, we use connectomics from electron microscopy to reconstruct and analyze neural circuits downstream of the largest somatosensory organ in the Drosophila leg, the femoral chordotonal organ (FeCO). The FeCO has been proposed to support both proprioceptive sensing of the fly's femur-tibia joint and exteroceptive sensing of substrate vibrations, but it was unknown which sensory neurons and central circuits contribute to each of these functions. We found that different subtypes of FeCO sensory neurons feed into distinct proprioceptive and exteroceptive pathways. Position- and movement-encoding FeCO neurons connect to local leg motor control circuits in the ventral nerve cord (VNC), indicating a proprioceptive function. In contrast, signals from the vibration-encoding FeCO neurons are integrated across legs and transmitted to mechanosensory regions in the brain, indicating an exteroceptive function. Overall, our analyses reveal the structure of specialized circuits for processing proprioceptive and exteroceptive signals from the fly leg. These findings are consistent with a growing body of work in invertebrate and vertebrate species demonstrating the existence of specialized limb mechanosensory pathways for sensing external vibrations.