Tuning of feedforward control enables stable muscle force length dynamics after loss of autogenic proprioceptive feedback

Animals must integrate feedforward, feedback and intrinsic mechanical control mechanisms to maintain stable locomotion. Recent studies of guinea fowl (Numida meleagris) revealed that the distal leg muscles rapidly modulate force and work output to minimize perturbations in uneven terrain. Here we probe the role of reflexes in the rapid perturbation response of muscle by studying the effects of proprioceptive loss. We induced bilateral loss of autogenic proprioception in the lateral gastrocnemius muscle (LG) using self-reinnervation. We compared ankle kinematics and in vivo muscle dynamics in birds with reinnervated LG and intact LG. Reinnervated and intact muscles exhibit similar force-length dynamics, with rapid changes in work to stabilize running obstacle terrain. Reinnervated LG exhibits 23ms earlier steady-state activation, consistent with feedforward tuning of activation phase to compensate for lost proprioception. Modulation of force duration is impaired in rLG, confirming the role of reflex feedback in regulating force duration in intact muscle.