Neural sensing of surface mechanics modulates proprioceptive activity and locomotion in Caenorhabditis elegans

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, they allow organisms to move efficiently, adapt to varying environments, and maintain balance. Here we show that the ‘gentle touch’ receptor neurons (TRNs) in the Caenorhabditis elegans body wall are sensitive to dynamic surface traction. Using a combination of calcium recordings and traction force microscopy in freely moving animals, microfluidics, and whole connectome computer simulations, we show that MEC-4 DEG/ENaC ion channel activity depends on the crawling velocity and friction force. Mutations disrupting MEC-4 activity and body wall mechanoreceptor function produce lethargic worms with impaired proprioceptive regulation, suggesting functional coupling between surface mechanoreceptors and proprioceptors. Our data reveal a new role for classical touch receptors in locomotion and critically define the mechanical modality sensed by skin mechanosensors. Competing Interest Statement The authors have declared no competing interest.