On the ascent: the soleus operating length is conserved to the ascending limb of the force-length curve across gait mechanics in humans

Abstract

SUMMARYThe region over which skeletal muscles operate on their force-length (F-L) relationship is fundamental to the mechanics, control and economy of movement. Yet surprisingly little experimental data exist on normalized length operating ranges of muscle during human gait, or how they are modulated when mechanical demands (such as force output) change. Here we explored the soleus muscle (SOL) operating lengths experimentally in a group of healthy young adults by combining subject-specific F-L relationships with in vivo muscle imaging during gait. We tested whether modulation of operating lengths occurred between walking and running, two gaits that require different levels of force production and different muscle-tendon mechanics, and examined the relationship between optimal fascicle lengths (L 0 ) and normalized operating lengths during these gaits. We found that the mean active muscle lengths reside predominantly on the ascending limbs of the F-L relationship in both gaits (walk, 0.70-0.94 L 0 ; run, 0.65-0.99 L 0 ). Furthermore, the mean normalized muscle length at the time of the peak activation of the muscle was the same between the two gaits (0.88 L 0 ). The active operating lengths were conserved, despite a fundamentally different fascicle strain pattern between walking (stretch-shorten cycle) and running (near continuous shortening). Taken together, these findings indicate that the SOL operating length is highly conserved, despite gait-dependent differences in muscle-tendon dynamics, and appear to be preferentially selected for stable force production compared with optimal force output (although length-dependent force capacity is high when maximal forces are expected to occur). Individuals with shorter L 0 undergo smaller absolute muscle excursions (P<0.05) so that the normalized length changes during walking and running remain independent of L 0 . The correlation between L 0 and absolute length change was not explained on the basis of muscle moment arms or joint excursion, suggesting that regulation of muscle strain may occur via tendon stretch.

Muscle-tendon mechanics explain unexpected effects of exoskeleton assistance on metabolic rate during walking

“…The soleus, lateral gastrocnemius and medial gastrocnemius were each modelled with a separate tendon, as opposed to one shared tendon. It is unclear which modelling choice is more appropriate for our study, but our fiber and tendon excursions were consistent with experimental ultrasound studies (Fukunaga et al, 2001;Lichtwark and Wilson, 2006;Cronin et al, 2010;Rubenson et al, 2012;Cronin et al, 2013). Moreover, qualitative trends in elastic element negative, positive and net work (Fig.…”

“…This isometric muscle force production is economical because muscles consume relatively little energy to produce force at constant length (Biewener, 1998;Biewener and Roberts, 2000). At the end of stance, the plantarflexor muscles actively shorten and the Achilles tendon simultaneously recoils (Fukunaga et al, 2001;Ishikawa et al, 2005;Rubenson et al, 2012), generating a significant amount of positive power at push-off (Winter, 1990;Meinders et al, 1998). Elastic energy storage and recovery in the Achilles tendon helps to reduce plantarflexor muscle work (Roberts et al, 1997;Ishikawa et al, 2005).…”

Tendon elastic strain energy in the human ankle plantar-flexors and its role with increased running speed

“…Previous studies investigating the behavior of the lateral gastrocnemius in the turkey and the wallaby found similar nearisometric muscle fiber contractions, irrespective of locomotion speed (Taylor, 1994;Roberts et al, 1997;Biewener et al, 1998;Gabaldón et al, 2008). Muscle fiber length change for the human ankle plantar-flexors has also been observed to be small during running in experimental studies involving dynamic ultrasound recordings (Lichtwark et al, 2007;Farris and Sawicki, 2012;Rubenson et al, 2012;Cronin and Finni, 2013) as well as in a recent musculoskeletal modeling study (Arnold et al, 2013). The small muscle fiber length change noted in these studies (and in the present study) implies that the soleus and gastrocnemius muscle fibers operate under favorable contractile conditions on their force-velocity (F-V) relationship, allowing the development of larger muscle forces than would otherwise be possible.…”

Contribution of elastic tissues to the mechanics and energetics of muscle function during movement

“…Passive forces are not developed in muscle typically until after the length at which peak active muscle force is produced. In cases where we have measurements of muscle operating length during locomotion, most force production appears to occur at lengths less than that at which passive force is developed Rubenson et al, 2012). If non-cross-bridge elements are stiffened in the presence of Ca 2+ , the fiber lengths at which they can contribute force may be shorter than suggested by the passive force-length curve.…”