Skeletal Muscle Shape Change in Relation to Varying Force Requirements Across Locomotor Conditions.

Nicolai Konow,Alexandra Collias,Andrew A Biewener

doi:10.3389/fphys.2020.00143

Nicolai Konow, Alexandra Collias + Show 1 more

Open Access

https://doi.org/10.3389/fphys.2020.00143

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Abstract

Contractions of skeletal muscles to generate in vivo movement involve dynamic changes in contractile and elastic tissue strains that likely interact to influence the force and work of a muscle. However, studies of the in vivo dynamics of skeletal muscle and tendon strains remain largely limited to bipedal animals, and rarely cover the broad spectra of movement requirements met by muscles that operate as motors, struts, or brakes across the various gaits that animals commonly use and conditions they encounter. Using high-speed bi-planar fluoromicrometry, we analyze in vivo strains within the rat medial gastrocnemius (MG) across a range of gait and slope conditions. These conditions require changes in muscle force ranging from decline walk (low) to incline gallop (high). Measurements are made from implanted (0.5–0.8 mm) tantalum spheres marking MG mid-belly width, mid-belly thickness, as well as strains of distal fascicles, the muscle belly, and the Achilles tendon. During stance, as the muscle contracts, muscle force increases linearly with respect to gait–slope combinations, and both shortening and lengthening fiber strains increase from approximately 5 to 15% resting length. Contractile change in muscle thickness (thickness strain) decreases (r2 = 0.86; p = 0.001); whereas, the change in muscle width (width strain) increases (r2 = 0.88; p = 0.001) and tendon strain increases (r2 = 0.77; p = 0.015). Our results demonstrate force-dependency of contractile and tendinous tissue strains with compensatory changes in shape for a key locomotor muscle in the hind limb of a small quadruped. These dynamic changes are linked to the ability of a muscle to tune its force and work output as requirements change with locomotor speed and environmental conditions.

Highlights

Skeletal muscle contractions that produce and control in vivo movement involve dynamic contractile and elastic tissue strains, as well as changes in muscle shape, that likely interact to influence the force and work production of a muscle
medial gastrocnemius (MG) fascicle strains measured via fluoromicrometry across slope and gait conditions exhibited generally consistent patterns when compared across slopes with respect to gaits (Figure 5A) but more complex patterns when compared across gaits with respect to slope (Figure 5B)
Our measurements of muscle shape change dynamics during unrestrained locomotion across differing gait–slope combinations based on 3D X-ray imaging and fluoromicrometry support the findings of past studies (Azizi et al, 2008; Holt et al, 2016) that have inferred muscle shape change based on in situ force–velocity measurements and how changes in force output affect fascicle rotation and the gearing of pennate muscles

Summary

Introduction

Skeletal muscle contractions that produce and control in vivo movement involve dynamic contractile and elastic tissue strains, as well as changes in muscle shape, that likely interact to influence the force and work production of a muscle. Distal limb muscles, for which direct in vivo measurements of mechanical work have been obtained, favor more economical force production with limited fascicle strain and work output (Roberts et al, 1997; Biewener and Roberts, 2000) The architecture of these distal muscle–tendon units (MTUs) favors elastic energy storage and return from their aponeuroses and tendons, with elastic energy savings that substantially reduces muscle work requirements for steady level locomotion (Biewener and Baudinette, 1995; Biewener et al, 1998; McGuigan et al, 2009)

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