How muscle fiber lengths and velocities affect muscle force generation as humans walk and run at different speeds

Abstract

SUMMARYThe lengths and velocities of muscle fibers have a dramatic effect on muscle force generation. It is unknown, however, whether the lengths and velocities of lower limb muscle fibers substantially affect the ability of muscles to generate force during walking and running. We examined this issue by developing simulations of muscle-tendon dynamics to calculate the lengths and velocities of muscle fibers from electromyographic recordings of 11 lower limb muscles and kinematic measurements of the hip, knee and ankle made as five subjects walked at speeds of 1.0-1.75ms-1 and ran at speeds of 2.0-5.0ms. We analyzed the simulated fiber lengths, fiber velocities and forces to evaluate the influence of force-length and force-velocity properties on force generation at different walking and running speeds. The simulations revealed that force generation ability (i.e. the force generated per unit of activation) of eight of the 11 muscles was significantly affected by walking or running speed. Soleus force generation ability decreased with increasing walking speed, but the transition from walking to running increased the force generation ability by reducing fiber velocities. Our results demonstrate the influence of soleus muscle architecture on the walk-to-run transition and the effects of muscle-tendon compliance on the plantarflexorsʼ ability to generate ankle moment and power. The study presents data that permit lower limb muscles to be studied in unprecedented detail by relating muscle fiber dynamics and force generation to the mechanical demands of walking and running.Supplementary material available online at

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.…”

“…The combined stiffness of the two tendons was assumed to be 200 N mm −1 , which is within the range of values (145-390 N mm −1 ) reported in previous experimental studies (Rosager et al, 2002;Hansen et al, 2003;Lichtwark and Wilson, 2005;Muraoka et al, 2005). A similar value of Achilles tendon compliance was used recently (see Arnold et al, 2013) in simulations of walking and running. Tendon stiffness was calculated as the product of the tendon elastic modulus and crosssectional area divided by tendon slack length (Zajac, 1989).…”

“…Third, the predicted muscle fiber behavior for the soleus and gastrocnemius is likely sensitive to the tendon mechanical properties and muscle-tendon architecture assumed in the model. Arnold et al (Arnold et al, 2013) found that estimates of muscle fiber behavior with a less compliant tendon do not agree well with in vivo measurements at corresponding locomotion speeds. Yet, tendon stiffness for the human ankle plantar-flexors has been reported to vary between 145 and 390 N mm −1 (Lichtwark and Wilson, 2005;Muraoka et al, 2005).…”

Locomotion as an emergent property of muscle contractile dynamics

“…Even though in vivo experimental data do not exist for horse digital flexor muscles, the extreme architecture of these distal MTUs demonstrates a design for limited work output, but economical force generation and recovery of elastic energy from long tendons (Biewener, 1998a;Wilson et al, 2001). Experimental studies of human MG during walking and running based on ultrasound imaging in relation to joint moment patterns (Lichtwark et al, 2007) and recent musculoskeletal modeling analysis (Arnold et al, 2013) reinforce this pattern: proximal human muscles contract over larger lengths and perform the majority of lower extremity work compared with distal MTUs that contract with more limited length change, favoring economical force generation and tendon energy recovery.…”

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

“…Elastic energy storage and recovery in the Achilles tendon helps to reduce plantarflexor muscle work (Roberts et al, 1997;Ishikawa et al, 2005). Furthermore, the stiffness of the Achilles tendon, in conjunction with the resting length of the plantarflexor muscle fibers, has been shown to maximize plantarflexor muscle efficiency during walking and running by allowing the muscle fibers to operate at favorable lengths and velocities during positive fiber work production (Roberts et al, 1997;Roberts, 2002;Lichtwark and Wilson, 2007;Taylor, 2007;Lichtwark and Wilson, 2008;Lichtwark and Barclay, 2010;Arnold et al, 2013). Any change to the stiffness of the Achilles tendon can affect the mechanics of the plantarflexor muscle fibers and consequently alter muscle energy consumption (Lichtwark and Wilson, 2007).…”