Biomechanical origins of proprioceptor feature selectivity and topographic maps in the Drosophila leg

Our ability to sense and move our bodies relies on proprioceptors, sensory neurons that detect mechanical forces within the body. Different subtypes of proprioceptors detect different kinematic features, such as joint position, movement, and vibration, but the mechanisms that underlie proprioceptor feature selectivity remain poorly understood. Using single-nucleus RNA sequencing (RNA-seq), we found that proprioceptor subtypes in the Drosophila leg lack differential expression of mechanosensitive ion channels. However, anatomical reconstruction of the proprioceptors and connected tendons revealed major biomechanical differences between subtypes. We built a model of the proprioceptors and tendons that identified a biomechanical mechanism for joint angle selectivity and predicted the existence of a topographic map of joint angle, which we confirmed using calcium imaging. Our findings suggest that biomechanical specialization is a key determinant of proprioceptor feature selectivity in Drosophila. More broadly, the discovery of proprioceptive maps reveals common organizational principles between proprioception and other topographically organized sensory systems. [Display omitted] •Proprioceptors in the Drosophila leg are organized into three groups•Each group is biomechanically specialized to detect distinct features of leg joint kinematics•A mechanical doohickey in the femur decomposes tibia joint movements into orthogonal components•The cell bodies of position-tuned proprioceptors form a goniotopic map of joint angle The sense of self relies on proprioceptors, sensory neurons that detect mechanical forces within the body. Mamiya and colleagues investigate how proprioceptors detect specific mechanical features, such as joint position and movement. They show how feature selectivity arises from the biomechanics of the proprioceptive organ and discover topographic neural maps of leg joint angle and vibration frequency.