Neural coding of leg proprioception in Drosophila

Abstract

Animals rely on an internal sense of body position and movement to effectively control motor behavior. This sense of proprioception relies on diverse populations of mechanosensory neurons distributed throughout the body. However, little is known about how proprioceptor neurons collectively encode sensory stimuli. Here, we investigate neural coding of leg proprioception in Drosophila, using in vivo two-photon calcium imaging of proprioceptors during controlled movements of the fly tibia. We found that the axons of leg proprioceptors are organized into distinct functional projections that contain topographic representations of specific kinematic features. Using subtype-specific genetic driver lines, we show that one group of axons encodes tibia position (flexion/extension), another encodes movement direction, and a third encodes bidirectional movement and vibration frequency. Thus, proprioceptive sensing of a single leg joint is mediated by multiple subtypes of specialized sensory neurons. This architecture may help to maximize information transmission, processing speed, and robustness, which are critical for feedback control of the limbs during locomotion.