The isometric force–length (FL) and isotonic force–velocity (FV) 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 FL and FV 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 FL 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 FL 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 FL and FV properties suggests the need for new approaches to characterize muscle properties in controlled conditions that more closely resemble in vivo dynamics.

Author contributions

Conceptualization: M.J.S., D.L.M., E.A., M.A.D.; Methodology: M.J.S., D.L.M., E.A., M.A.D.; Software: M.A.D., E.A.; Validation: M.J.S., D.L.M., E.A., M.A.D.; Formal analysis: M.J.S.; Investigation: M.J.S., D.L.M.; Resources: E.A., M.A.D.; Data curation: M.J.S., M.A.D.; Writing - original draft: M.J.S.; Writing - review & editing: M.J.S., D.L.M., E.A., M.A.D.; Visualization: M.J.S.; Supervision: E.A., M.A.D.; Project administration: M.A.D.; Funding acquisition: E.A., M.A.D.

Funding

This work is funded by a postdoctoral PDM-II fellowship from KU Leuven (to M.J.S.), the National Science Foundation (NSF) (grant 2016049 and 2319710 to M.A.D.) and the National Institutes of Health (NIH) (grant R01 AR055295-09 to E.A.). Deposited in PMC for release after 12 months.

Data availability

The data underlying this research article, including MATLAB files containing continuous in vivo recordings of muscle length, force and activation of running and walking guinea fowl, and the measured characteristics from the in situ FL and FV experiments, plus an Excel file of the data underlying our statistical tests, are available from the Dryad digital repository (Schwaner et al., 2024): https://doi.org/10.5061/dryad.0p2ngf26p

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