In vivo behavior of the human soleus muscle with increasing walking and running speeds

Abstract

The interaction between the muscle fascicle and tendon components of the human soleus (SO) muscle influences the capacity of the muscle to generate force and mechanical work during walking and running. In the present study, ultrasound-based measurements of in vivo SO muscle fascicle behavior were combined with an inverse dynamics analysis to investigate the interaction between the muscle fascicle and tendon components over a broad range of steady-state walking and running speeds: slow-paced walking (0.7 m/s) through to moderate-paced running (5.0 m/s). Irrespective of a change in locomotion mode (i.e., walking vs. running) or an increase in steady-state speed, SO muscle fascicles were found to exhibit minimal shortening compared with the muscle-tendon unit (MTU) throughout stance. During walking and running, the muscle fascicles contributed only 35 and 20% of the overall MTU length change and shortening velocity, respectively. Greater levels of muscle activity resulted in increasingly shorter SO muscle fascicles as locomotion speed increased, both of which facilitated greater tendon stretch and recoil. Thus the elastic tendon contributed the majority of the MTU length change during walking and running. When transitioning from walking to running near the preferred transition speed (2.0 m/s), greater, more economical ankle torque development is likely explained by the SO muscle fascicles shortening more slowly and operating on a more favorable portion (i.e., closer to the plateau) of the force-length curve.

Muscle structural assembly and functional consequences

“…In vivo measurements of the gastrocnemius medialis tendon and fascicles performed during the gait cycle in humans show that when the muscle is active during the single support phase, the gastrocnemius medialis fascicles operate quasi-isometrically, enabling the tendon to be stretched and store elastic energy, which is then released during the push-off phase (Fukunaga et al, 2001). A similar effect has recently been observed in the soleus muscle (Lai et al, 2015). Quasi-isometricity in leg muscle behaviour has also previously been reported during terrestrial locomotion in non-human species Roberts et al, 1997).…”

Human ankle plantar flexor muscle–tendon mechanics and energetics during maximum acceleration sprinting

“…MTU, muscle fascicle and tendon lengths were normalized, respectively, to resting MTU length (l To test whether the model-based predictions were physiologically reasonable, we compared the model-based muscle fascicle lengths for the ankle plantar flexors against previously reported ultrasound measurements. For one representative participant, we collected additional data for running at a steady-state speed of 3.5 m s 21 in order to directly compare model-based fascicle lengths to ultrasound-measured fascicle lengths for the SO and MG [10,40,41].…”

“…The calibrated capture volume was approximately 8 m in length. Retro-reflective markers (14 mm diameter) were placed at predefined locations on the upper and lower limbs (see Lai et al [9,10] for full details). A fourth-order, low-pass Butterworth filter with a cut-off frequency of 15 Hz was used to filter the marker trajectories.…”

“…The ankle plantar flexors comprise short, highly pennated muscle fascicles connected to a long, elastic Achilles tendon, a configuration that allows tendon elasticity to significantly influence muscle fascicle behaviour (lengths and velocities) and energetics [4][5][6]. For instance, when running at a steady-state speed, these muscles store and recover a substantial amount of tendon elastic strain energy, which contributes to the required muscle-tendon unit (MTU) positive work and often exceeds the work done by the muscle fascicles [7][8][9][10]. Moreover, the muscle fascicles in the ankle plantar flexors maintain a relatively low shortening velocity compared with that of the MTU allowing them to operate in more favourable regions of the force -velocity (F-V) and force -length (F-L) relationships [10,11].…”

Additional in-series compliance reduces muscle force summation and alters the time course of force relaxation during fixed-end contractions

“…Energy stored in the stretched tendon can then be returned to the skeletal system when the tendon recoils during limb propulsion (Alexander and Vernon, 1975;Roberts et al, 1997). Strut-like muscle behaviour and cycling of elastic energy have been demonstrated clearly in the gastrocnemius and plantaris of tammar wallabies during hopping (Biewener et al, 1998), the gastrocnemius of turkeys during running (Roberts et al, 1997), and the gastrocnemius (Lichtwark et al, 2007;Farris and Sawicki, 2012) and soleus (Lai et al, 2015) of humans during walking and running. However, muscles with high series compliance are not confined to economic force production and elastic energy savings.…”