Tendon-specific PIEZO1 activation enhances neural drive to muscle during ballistic movement

Abstract

Tendons are generally regarded as passive structures that transmit muscle force to bone, yet they contain the Golgi tendon organ (GTO), whose Ib afferents act on motor neurons either inhibitory or excitatory depending on movement context. Whether a change in tendon mechanical properties alters the neural drive to muscle during movement remains unknown. We therefore recorded electromyography (EMG) and ankle kinematics during jumping in male mice carrying a tendon-specific gain-of-function (GOF) mutation in the mechanosensitive channel PIEZO1, which renders the tendon more compliant. In wild-type (WT) mice, gastrocnemius EMG amplitude increased with jump distance but not tibialis anterior activity, identifying the gastrocnemius as the muscle that scales with jump demand. At their maximum jump distance, which was longer in GOF than in WT mice, GOF mice showed a larger gastrocnemius EMG amplitude with unchanged burst duration. No genotype difference was detected at a submaximal distance, indicating that this enhancement depends on load. Kinematics showed the same specificity: GOF mice reached a deeper peak dorsiflexion before takeoff only at maximum jump distance, and the EMG difference emerged only after maximal dorsiflexion, not at burst onset. Muscle mass and myogenic gene expression were unchanged, whereas tendon marker genes were elevated, indicating that the enhancement was not of muscular origin. These findings indicate that a change in tendon mechanical properties alters the neural drive to muscle in a load-dependent manner, most plausibly through positive force feedback from the GTO, and identify the tendon as a sensory organ whose mechanical properties shape motor output.