Diverse muscle spindle firing properties emerge from multiscale muscle mechanics

Sensory information about the body and its mechanical interactions with the environment are critical for neural control of movement. Muscle spindle sensory neurons richly innervate muscles in vertebrates; their firing patterns as muscles stretch have been well characterized experimentally, but have not been fully explained mechanistically. Here, we show that a diverse range of muscle spindle firing characteristics are emergent from first principles of muscle contractile mechanics. We develop a mechanistic muscle spindle model that predicts well-known phenomena such as variations in muscle spindle sensitivity due to prior movement history and nonlinear scaling with muscle stretch velocity. The model further predicts how central commands to muscle spindles, fusimotor drive, alters their firing responses, and shows how seemingly paradoxical muscle spindle firing during voluntary force production in humans can arise. Our multiscale muscle spindle model provides a unifying biophysical framework that may broadly explain and predict movement-related sensory signals in health and disease.