Mechanosensory encoding of surface mechanics optimizes locomotion

Abstract Locomotion - whether walking, running, or crawling - depends on the precise coordination of forces between the body and its surroundings. Two critical factors in this process are the force that resists the relative motion between two bodies, and mechanosensation, the body’s ability to sense and respond to mechanical forces. Together, these processes enable efficient locomotion across diverse environments, yet how body-environment interaction forces shape neural activity in freely moving animals remains poorly understood. Here we show that the ‘gentle touch’ receptor neurons (TRNs) in the Caenorhabditis elegans body wall are sensitive to dynamic surface mechanics. Using a combination of calcium imaging and traction force microscopy in freely behaving animals informed by micromechanical stimulation, connectome-scale simulations, and optimal control theory, we identify friction force and crawling velocity as key determinants of mechanoreceptor activity. Mutations disrupting MEC-4 DEG/ENaC ion channel activity in body wall mechanoreceptors produce lethargic animals with impaired proprioceptive regulation, suggesting functional coupling between surface mechanoreceptors and proprioceptors. Together, our findings reveal that gentle ‘touch’ receptors encode body-environment interaction forces during movement to optimize locomotor energetics.