Muscle force-length dynamics during walking over obstacles indicates delayed recovery and a shift towards more 'strut-like' function in birds with proprioceptive deficit.

Recent studies of in vivo muscle function in guinea fowl revealed that distal leg muscles rapidly modulate force and work to stabilize running in uneven terrain. Previous studies focused on running only, and it remains unclear how muscular mechanisms for stability differ between walking and running. Here, we investigated in vivo function of the lateral gastrocnemius (LG) during walking over obstacles. We compared muscle function in birds with intact (iLG) versus self-reinnervated LG (rLG). Self-reinnervation results in proprioceptive feedback deficit due to loss of monosynaptic stretch reflex. We tested the hypothesis that proprioceptive deficit results in decreased modulation of EMG activity in response to obstacle contact, and a delayed obstacle recovery compared with that for iLG. We found that total myoelectric intensity (Etot) of iLG increased by 68% in obstacle strides (S 0) compared with level terrain, suggesting a substantial reflex-mediated response. In contrast, Etot of rLG increased by 31% in S 0 strides compared with level walking, but also increased by 43% in the first post-obstacle (S +1) stride. In iLG, muscle force and work differed significantly from level walking only in the S 0 stride, indicating a single-stride recovery. In rLG, force increased in S 0, S +1 and S +2 compared with level walking, indicating three-stride obstacle recovery. Interestingly, rLG showed little variation in work output and shortening velocity in obstacle terrain, indicating a shift towards near-isometric strut-like function. Reinnervated birds also adopted a more crouched posture across level and obstacle terrains compared with intact birds. These findings suggest gait-specific control mechanisms in walking and running.

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 responses 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 in vivo muscle dynamics and ankle kinematics in birds with reinnervated and intact LG. Reinnervated and intact LG exhibit similar steady state mechanical function and similar work modulation in response to obstacle encounters. Reinnervated LG exhibits 23ms earlier steady-state activation, consistent with feedforward tuning of activation phase to compensate for lost proprioception. Modulation of activity duration is impaired in rLG, confirming the role of reflex feedback in regulating force duration in intact muscle.

How do treadmill speed and terrain visibility influence neuromuscular control of guinea fowl locomotion?

Locomotor control mechanisms must flexibly adapt to both anticipated and unexpected terrain changes to maintain movement and avoid a fall. Recent studies revealed that ground birds alter movement in advance of overground obstacles, but not treadmill obstacles, suggesting context-dependent shifts in the use of anticipatory control. We hypothesized that differences between overground and treadmill obstacle negotiation relate to differences in visual sensory information, which influence the ability to execute anticipatory manoeuvres. We explored two possible explanations: (1) previous treadmill obstacles may have been visually imperceptible, as they were low contrast to the tread, and (2) treadmill obstacles are visible for a shorter time compared with runway obstacles, limiting time available for visuomotor adjustments. To investigate these factors, we measured electromyographic activity in eight hindlimb muscles of the guinea fowl (Numida meleagris, N=6) during treadmill locomotion at two speeds (0.7 and 1.3 m s(-1)) and three terrain conditions at each speed: (i) level, (ii) repeated 5 cm low-contrast obstacles (<10% contrast, black/black), and (iii) repeated 5 cm high-contrast obstacles (>90% contrast, black/white). We hypothesized that anticipatory changes in muscle activity would be higher for (1) high-contrast obstacles and (2) the slower treadmill speed, when obstacle viewing time is longer. We found that treadmill speed significantly influenced obstacle negotiation strategy, but obstacle contrast did not. At the slower speed, we observed earlier and larger anticipatory increases in muscle activity and shifts in kinematic timing. We discuss possible visuomotor explanations for the observed context-dependent use of anticipatory strategies.