Author response: Muscle-specific economy of force generation and efficiency of work production during human running (original) (raw)

Muscle-specific economy of force generation and efficiency of work production during human running

bioRxiv (Cold Spring Harbor Laboratory), 2021

Human running features a spring-like interaction of body and ground, enabled by elastic tendons that store mechanical energy and facilitate muscle operating conditions to minimize the metabolic cost. By experimentally assessing the operating conditions of two important muscles for running, the soleus and vastus lateralis, we investigated physiological mechanisms of muscle energy production and muscle force generation. Results showed that the soleus continuously shortened throughout the stance phase, operating as energy generator under conditions that were found to be optimal for work production: high force-length potential and enthalpy efficiency. The vastus lateralis promoted tendon energy storage and contracted nearly isometrically close to optimal length, resulting in a high force-length-velocity potential beneficial for economical force generation. The favorable operating conditions of both muscles were a result of an effective length and velocity-decoupling of fascicles and muscle-tendon unit mostly due to tendon compliance and, in the soleus, marginally by fascicle rotation.

Enthalpy efficiency of the soleus muscle explains improvements in running economy

bioRxiv (Cold Spring Harbor Laboratory), 2020

During human running, the soleus, as the main plantar flexor muscle, generates the majority of the mechanical work through active shortening. The fraction of chemical energy that is converted into muscular work (i.e. the enthalpy efficiency) depends on the muscle shortening velocity. Here, we investigated the soleus muscle fascicle behavior during running with respect to the enthalpy efficiency as a mechanism that could explain previously reported improvements in running economy after exercise-induced increases of plantar flexor strength and Achilles tendon stiffness. Healthy amateur runners were randomly assigned to a control (n=10) or intervention group (n=13), which performed a specific 14-week muscle-tendon training. Significant increases in plantar flexor maximum strength (10%) and Achilles tendon stiffness (31%) yet reduced metabolic cost of running (4%) was found only in the intervention group (p<0.05). Following training, the soleus fascicle velocity profile throughout stance was altered, with the fascicles operating at a higher enthalpy efficiency during the phase of muscle-tendon unit lengthening (15%) and in average over stance (7%, p<0.05). These findings show that the improvements in energetic cost following increases in plantar flexor strength and Achilles tendon stiffness can be attributed to increased enthalpy efficiency of the operating soleus. This provides the first experimental evidence that the soleus enthalpy efficiency is a determinant of human running economy. Furthermore, the current results imply that the soleus energy production in the first part of the stance phase were the muscle-tendon unit is lengthening is crucial for the overall metabolic energy cost of running. .

Enthalpy efficiency of the soleus muscle contributes to improvements in running economy

Proceedings of the Royal Society B: Biological Sciences, 2021

Muscle work is biased toward energy generation over dissipation in non-level running

Journal of biomechanics, 2008

This study tested the hypothesis that skeletal muscles generate more mechanical energy in gait tasks that raise the center of mass compared to the mechanical energy they dissipate in gait tasks that lower the center of mass despite equivalent changes in total mechanical energy. Thirteen adults ran on a 10° decline and incline surface at a constant average velocity. Three-dimensional (3D) joint powers were calculated from ground force and 3D kinematic data using inverse dynamics. Joint work was calculated from the power curves and assumed to be due to skeletal muscle-tendon actuators. External work was calculated from the kinematics of the pelvis through the gait cycle. Incline vs. decline running was characterized with smaller ground forces that operated over longer lever arms causing larger joint torques and work from these torques. Total lower extremity joint work was 28% greater in incline vs. decline running (1.32 vs. −1.03 J/kg m, p<0.001). Total lower extremity joint work comprised 86% and 71% of the total external work in incline (1.53 J/kg m) and decline running (−1.45 J/kg m), which themselves were not significantly different (p<0.180). We conjectured that the larger ground forces in decline vs. incline running caused larger accelerations of all body tissues and initiated a greater energy-dissipating response in these tissues compared to their response in incline running. The runners actively lowered themselves less during decline stance and descended farther as projectiles than they lifted themselves during incline stance and ascended as projectiles. These data indicated that despite larger ground forces in decline running, the reduced displacement during downhill stance phases limited the work done by muscle contraction in decline compared to incline running.

Operating length and velocity of human vastus lateralis muscle during walking and running

Scientific Reports, 2018

According to the force-length-velocity relationships, the muscle force potential during locomotion is determined by the operating fibre length and velocity. We measured fascicle and muscle-tendon unit length and velocity as well as the activity of the human vastus lateralis muscle (VL) during walking and running. Furthermore, we determined the VL force-length relationship experimentally and calculated the force-length and force-velocity potentials (i.e. fraction of maximum force according to the forcelength-velocity curves) for both gaits. During the active state of the stance phase, fascicles showed significantly (p < 0.05) smaller length changes (walking: 9.2 ± 4.7% of optimal length (L 0); running: 9.0 ± 8.4%L 0) and lower velocities (0.46 ± 0.36 L 0 /s; 0.03 ± 0.83 L 0 /s) compared to the muscle-tendon unit (walking: 19.7 ± 5.3%L 0 , −0.94 ± 0.32 L 0 /s; running: 34.5 ± 5.8%L 0 , −2.59 ± 0.41 L 0 /s). The VL fascicles operated close to optimum length (L 0 = 9.4 ± 0.11 cm) in both walking (8.6 ± 0.14 cm) and running (10.1 ± 0.19 cm), resulting in high force-length (walking: 0.92 ± 0.08; running: 0.91 ± 0.14) and force-velocity (0.91 ± 0.08; 0.97 ± 0.13) potentials. For the first time we demonstrated that, in contrast to the current general conception, the VL fascicles operate almost isometrically and close to L 0 during the active state of the stance phase of walking and running. The findings further verify an important contribution of the series-elastic element to VL fascicle dynamics. A muscle's potential to generate force depends on intrinsic muscle properties as the force-length and force-velocity relationships 1,2. Consequently, the operating length and velocity of the muscle fibres during locomotion determine the force potential of the muscle, i.e. the fraction of maximum force according to the force-length and force-velocity curves. Roberts et al. 3 measured muscle fibre length and tendon force in the lateral gastrocnemius muscle of running turkeys in vivo and found that during the stance phase of running, where the muscle was active and generated force, the muscle fibres operated with almost constant length (i.e. maximum length change of 6.6% of the optimal length (L 0)) and close to L 0. The nearly isometric contraction of the muscle fibres was a result of a concomitant lengthening of the tendon that provided more than 60% of the work done by the muscle-tendon unit (MTU). Hence, the decoupling of muscle and tendon lengthening that enabled favourable muscle contraction conditions was concluded to be beneficial for economic force generation, since less muscle volume needs to be activated for a certain force output 3. In the past two decades, numerous studies investigated the fascicle behaviour of the human distal leg muscles, as for example soleus and gastrocnemius medialis, using the ultrasound methodology during walking and running in vivo 4-7. A decoupling of fascicle and tendon length changes during both gaits, which resulted in comparably smaller length changes at the fascicle level compared to the MTU, was consistently reported. However, for the human proximal leg muscles, as for example the vastus lateralis (VL), information regarding the fascicle behaviour during walking and running is scarce. It has been suggested that proximal muscles feature less compliant tendons and, therefore, MTU's length changes would be accompanied by major changes in fascicle length 8-10. In this regard, modelling studies predicted a stretch-shortening cycle of the VL muscle during the stance phase with notable fascicle length changes of up to ≈25% of optimal length during running 11 and ≈20% during walking 11,12 , covering a wide portion around the plateau of the force-length curve. However, experimental investigations demonstrated that the strain of the VL tendon-aponeurosis during a maximal isometric voluntary contraction in vivo is comparable to the strain of the gastrocnemius medialis' tendon aponeurosis 13,14 and evidently higher than the strain values used in the mentioned modelling studies (≈8.0% vs. 3.3% maximal strain). Consequently, the

Influence of the muscle-tendon unit's mechanical and morphological properties on running economy

Journal of Experimental Biology, 2006

SUMMARYThe purpose of this study was to test the hypothesis that runners having different running economies show differences in the mechanical and morphological properties of their muscle-tendon units (MTU) in the lower extremities. Twenty eight long-distance runners (body mass: 76.8±6.7 kg, height: 182±6 cm, age: 28.1±4.5 years) participated in the study. The subjects ran on a treadmill at three velocities (3.0, 3.5 and 4.0 m s-1) for 15 min each. The \batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \({\dot{V}}_{\mathrm{O}_{2}}\) \end{document}consumption was measured by spirometry. At all three examined velocities the kinematics of the left leg were captured whilst running on the treadmill using a high-speed digital video camera operating at 250 Hz. Furthermore the runners performed isometric maximal voluntary plantarflexion and knee extension contractions at eleven differen...

Muscle Contributions to Propulsion and Support During Running: 254

Medicine and Science in Sports and Exercise, 2009

Muscles actuate running by developing forces that propel the body forward while supporting the body's weight. To understand how muscles contribute to propulsion (i.e., forward acceleration of the mass center) and support (i.e., upward acceleration of the mass center) during running we developed a threedimensional muscle-actuated simulation of the running gait cycle. The simulation is driven by 92 musculotendon actuators of the lower extremities and torso and includes the dynamics of arm motion. We analyzed the simulation to determine how each muscle contributed to the acceleration of the body mass center. During the early part of the stance phase, the quadriceps muscle group was the largest contributor to braking (i.e., backward acceleration of the mass center) and support. During the second half of the stance phase, the soleus and gastrocnemius muscles were the greatest contributors to propulsion and support. The arms did not contribute substantially to either propulsion or support, generating less than 1% of the peak mass center acceleration. However, the arms effectively counterbalanced the vertical angular momentum of the lower extremities. Our analysis reveals that the quadriceps and plantarflexors are the major contributors to acceleration of the body mass center during running.

Changes in spring-mass behavior and muscle activity during an exhaustive run at V̇O2max

Journal of Biomechanics, 2013

The aim of this study was to evaluate concomitantly the changes in leg-spring behavior and the associated modifications in the lower limb muscular activity during a constant pace run to exhaustion at severe intensity. Methods: Twelve trained runners performed a running test at the velocity associated with V _ O2max (5.170.3 m s −1 ; mean time to exhaustion: 353769 s). Running step spatiotemporal parameters and spring-mass stiffness were calculated from vertical and horizontal components of ground reaction force measured by a 6.60 m long force platform system. The myoelectrical activity was measured by wireless surface electrodes on eight lower limb muscles. Results: The leg stiffness decreased significantly (−8.9%; P o 0.05) while the vertical stiffness did not change along the exhaustive exercise. Peak vertical force (−3.5%; P o 0.001) and aerial time (−9.7%; P o 0.001) decreased and contact time significantly increased (+4.6%; P o 0.05). The myoelectrical activity decreased significantly for triceps surae but neither vastus medialis nor vastus lateralis presented significant change. Both rectus and biceps femoris increased in the early phase of swing (+14.7%; P o 0.05) and during the pre-activation phase (+16.2%; P o 0.05). Conclusion: The decrease in leg spring-stiffness associated with the decrease in peak vertical ground reaction force was consistent with the decline in plantarflexor activity. The biarticular rectus femoris and biceps femoris seem to play a major role in the mechanical and spatiotemporal adjustments of stride pattern with the occurrence of fatigue during such exhaustive run.

Author response: Muscle-specific economy of force generation and efficiency of work production during human running (original) (raw)

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