Linking in vivo muscle dynamics to force-length and force-velocity properties reveals that guinea fowl lateral gastrocnemius operates at shorter than optimal lengths.

The isometric force-length (F-L) and isotonic force-velocity (F-V) relationships characterize the contractile properties of skeletal muscle under controlled conditions, yet it remains unclear how these properties relate to in vivo muscle function. Here, we map the in situ F-L and F-V characteristics of guinea fowl (Numida meleagris) lateral gastrocnemius (LG) to the in vivo operating range during walking and running. We test the hypothesis that muscle fascicles operate on the F-L plateau, near the optimal length for force (L0) and near velocities that maximize power output (Vopt) during walking and running. We found that in vivo LG velocities are consistent with optimizing power during work production, and economy of force at higher loads. However, LG does not operate near L0 at higher loads. LG length was near L0 at the time of electromyography (EMG) onset but shortened rapidly such that force development during stance occurred on the ascending limb of the F-L curve, around 0.8L0. Shortening across L0 in late swing might optimize potential for rapid force development near the swing-stance transition, providing resistance to unexpected perturbations that require rapid force development. We also found evidence of in vivo passive force rise in late swing, without EMG activity, at lengths where in situ passive force is zero, suggesting that dynamic viscoelastic effects contribute to in vivo force development. Comparison of in vivo operating ranges with F-L and F-V properties suggests the need for new approaches to characterize muscle properties in controlled conditions that more closely resemble in vivo dynamics.

Viscoelastic materials are most energy efficient when loaded and unloaded at equal rates.

Biological springs can be used in nature for energy conservation and ultra-fast motion. The loading and unloading rates of elastic materials can play an important role in determining how the properties of these springs affect movements. We investigate the mechanical energy efficiency of biological springs (American bullfrog plantaris tendons and guinea fowl lateral gastrocnemius tendons) and synthetic elastomers. We measure these materials under symmetric rates (equal loading and unloading durations) and asymmetric rates (unequal loading and unloading durations) using novel dynamic mechanical analysis measurements. We find that mechanical efficiency is highest at symmetric rates and significantly decreases with a larger degree of asymmetry. A generalized one-dimensional Maxwell model with no fitting parameters captures the experimental results based on the independently characterized linear viscoelastic properties of the materials. The model further shows that a broader viscoelastic relaxation spectrum enhances the effect of rate-asymmetry on efficiency. Overall, our study provides valuable insights into the interplay between material properties and unloading dynamics in both biological and synthetic elastic systems.