Relatively Shorter Muscle Lengths Increase the Metabolic Rate of Cyclic Force Production

During animal locomotion, force-producing leg muscles are almost exclusively responsible for the whole-bodys metabolic energy expenditure. Animals can change the length of these leg muscles by altering body posture (e.g., joint angles), kinetics (e.g., body weight), or the structural properties of their biological tissues (e.g., tendon stiffness). Currently, it is uncertain whether relative muscle fascicle operating length has a measurable effect on the metabolic energy expenditure of cyclic locomotion-like contractions. To address this uncertainty, we measured the metabolic energy expenditure of human participants as they cyclically produce two distinct ankle moments at three separate ankle angles (90{degrees}, 105{degrees}, 120{degrees}) on a fixed-position dynamometer exclusively using their soleus. Overall, increasing participant ankle angle from 90{degrees} to 120{degrees} (more plantar flexion) reduced minimum soleus fascicle length by 17% (both moment levels, p<0.001) and increased metabolic energy expenditure by an average of 208% (both p<0.001). Across both moment levels, the increased metabolic energy expenditure was not driven by greater fascicle positive mechanical work (higher moment level, p=0.591), fascicle force rate (both p[≥]0.235), or active muscle volume (both p[≥]0.122); but it was correlated with average relative soleus fascicle length (r=-179, p=0.002) and activation (r=0.51, p<0.001). Therefore, the metabolic energy expended during locomotion can likely be reduced by lengthening active muscles that operate on the ascending-limb of their force-length relationship.