Shorter muscle fascicle operating lengths increase the metabolic cost of cyclic force production

Abstract

During locomotion, force-producing limb muscles are predominantly responsible for an animal's whole body metabolic energy expenditure. Animals can change the length of their force-producing muscle fascicles by altering body posture (e.g., joint angles), the structural properties of their biological tissues over time (e.g., tendon stiffness), or the body's kinetics (e.g., body weight). Currently, it is uncertain whether relative muscle fascicle operating lengths have a measurable effect on the metabolic energy expended during cyclic locomotion-like contractions. To address this uncertainty, we quantified the metabolic energy expenditure of human participants, as they cyclically produced two distinct ankle moments at three ankle angles (90°, 105°, and 120°) on a fixed-position dynamometer using their soleus. Overall, increasing participant ankle angle from 90° to 120° (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% across both moment levels (both P < 0.001). For both moment levels, the increased metabolic energy expenditure was not related to greater fascicle positive mechanical work (higher moment level, P = 0.591), fascicle force rate (both P ≥ 0.235), or model-estimated active muscle volume (both P ≥ 0.122). Alternatively, metabolic energy expenditure correlated with average relative soleus fascicle length (r = -0.72, P = 0.002) and activation (r = 0.51, P < 0.001). Therefore, increasing active muscle fascicle operating lengths may reduce metabolic energy expended during locomotion.NEW & NOTEWORTHY During locomotion, active muscles undergo cyclic length-changing contractions. In this study, we isolated confounding variables and revealed that cyclically producing force at relatively shorter fascicle lengths increases metabolic energy expenditure. Therefore, muscle fascicle operating lengths likely have a measurable effect on the metabolic energy expenditure during locomotion.

Keywords: dynamometer; economy; efficiency; energetic; length.

Graphical abstract

Figure 1.

Representation of soleus fascicle length during midstance of walking in high-heeled shoes (14, 15), barefoot, and with an ankle exoskeleton (; A). B: conceptual graph showing isometric muscle fascicle force production and adenosine triphosphate (ATP) utilization relative to muscle length (10). C: actin-myosin ATP utilization per net isometric muscle fascicle force production at a given activation vs. muscle fascicle operating length (10). L and L₀ indicate actual and optimal muscle fascicle length, respectively.

Figure 2.

A: experimental setup of a participant cyclically generating soleus muscle force to produce a plantar flexor moment that exerts an external torque on a fixed dynamometer pedal following the cues of an audible metronome and visual feedback. B: illustrations of the two target torque levels (peak torque: 10 N·m and 15 N·m), three ankle angles (90°, 105°, and 120°) with the corresponding hypothetical minimum soleus fascicle operating lengths and their respective location on a muscle force-length relationship. EMG, electromyography; LG, lateral gastrocnemius; SOL, soleus; TA, tibialis anterior.

Figure 3.

Top row: time-series plots of average ankle moment (m_ank; A), muscle-tendon force (F_MT; B), soleus fascicle pennation angle (C), and active soleus fascicle force (F_M; D). Bottom row: average ± SE average ankle moment (E), average MT force (F), maximum fascicle pennation angle (G), and average soleus fascicle force vs. ankle angle (H). Black and red symbols are offset for clarity and indicate the lower and higher ankle moment levels, respectively. Lighter to darker colors indicate more dorsiflexed to plantar-flexed ankle angles per moment level. Figure details: sample size: 9; sex: 8 male/1 female; statistical tests: linear mixed model. Black and red asterisks (*) indicate that there is an effect of ankle angle on the indicated moment level’s dependent variable (P < 0.05). MT, muscle-tendon.

Figure 4.

Time-series plots of average soleus fascicle force (A) and power (D), as well as average ± SE soleus fascicle total force-time integral (B), force rate (C), and positive mechanical work (E). Black and red symbols are offset for clarity and indicate the lower and higher ankle moment levels, respectively. Lighter to darker colors indicate more dorsiflexed to plantar-flexed ankle angles per moment level. Figure details: sample size: 9; sex: 8 male/1 female; statistical tests: linear mixed model. Black and red asterisks (*) indicate that there is an effect of ankle angle on the indicated moment level’s dependent variable (P < 0.05).

Figure 5.

Top row: time-series plots of average soleus fascicle length (A), fascicle velocity (B), and active muscle volume (C). Bottom row: average ± SE minimum Hill-type force-length potential (D), minimum Hill-type force-velocity potential (E), and average active muscle volume vs. ankle angle (F). Within D and E are the respective force-potentials plotted on the force-length and force-velocity curves, respectively. Regarding fascicle velocity, shortening and lengthening equals positive and negative velocity, respectively. Black and red symbols are offset for clarity and indicate the lower and higher ankle moment levels, respectively. Lighter to darker colors indicate more dorsiflexed to plantar-flexed ankle angles per moment level. Figure details: sample size: 9; sex: 8 male/1 female; statistical tests: linear mixed model. Black and red asterisks (*) indicate that there is an effect of ankle angle on the indicated moment level’s dependent variable (P < 0.05).

Figure 6.

Average ± SE net metabolic power (A), minimum fascicle length (B), and average soleus activation (C) vs. ankle angle. Black and red symbols are offset for clarity and indicate the lower and higher ankle moment levels, respectively. Lighter to darker colors indicate more dorsiflexed to plantar-flexed ankle angles per moment level. Figure details: sample size: 9; sex: 8 male/1 female; statistical tests: linear mixed model. Black and red asterisks (*) indicate that there is an effect of ankle angle on the indicated moment level’s dependent variable (P < 0.05). MVC, maximum voluntary contraction.

Figure 7.

Top row: time-series plots of average soleus (SOL) activation (Act; A), lateral gastrocnemius (LG) activation (B), and tibialis anterior (TA) activation (C). Bottom row: average ± SE SOL activation (D), LG activation (E), and TA activation vs. ankle angle (F). MVC is maximum voluntary contraction. Black and red symbols are offset for clarity and indicate the lower and higher ankle moment levels, respectively. Lighter to darker colors indicate more dorsiflexed to plantar flexed ankle angles per moment level. Figure details: sample size: 9; sex: 8 male/1 female; statistical tests: linear mixed model. Black and red asterisks (*) indicate that there is an effect of ankle angle on the indicated moment level’s dependent variable (P < 0.05).