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

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 (r 2 = 0.86; p = 0.001); whereas, the change in muscle width (width strain) increases (r 2 = 0.88; p = 0.001) and tendon strain increases (r 2 = 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.

Agonist-antagonist muscle strain in the residual limb preserves motor control and perception after amputation

“…More broadly, an exciting area of future research would be the development of residual limb architectures that enable direct computer control of mechanoneural transduction 49 . To this end, basic research advances are necessary in physiological actuators such as biocompatible synthetic actuators 57 , intramuscular sensors 58 – 60 , and stimulators that can be implanted in series with residual muscle end organs.…”

The Effect of Multidirectional Loading on Contractions of the M. Medial Gastrocnemius

“…It is possible that the decrease in both length and thickness is compensated by an increase in fascicle width, which was not measured during these experiments. Muscle measurements in the medial gastrocnemius of rats showed that widthwise strains were approximately twice that of thickness strains ( Konow et al, 2020 ). Raiteri et al (2016) showed significant differences between the changes in thickness and width of the tibialis anterior.…”

“…It has been hypothesized that there is anisotropy between the changes in thickness and width of a contracting muscle ( Azizi et al, 2008 ; Holt et al, 2016 ). Recent research has shown asymmetries in the bulging of muscle fascicles in humans ( Randhawa and Wakeling, 2018 ) and in whole muscles in humans ( Englund et al, 2011 ; Mazzoli et al, 2018 ) and rats ( Konow et al, 2020 ). These asymmetries in bulging could result from asymmetries in stress distribution across the muscle ( Wakeling et al, 2020 ).…”

Modern three-dimensional digital methods for studying locomotor biomechanics in tetrapods

“…Similarly, Arellano et al (2019) integrated XROMM skeletal kinematics with changes of M. gastrocnemius lateralis fibre length and aponeurosis length and width in wild turkeys during landing and jumping, showing that aponeurosis width had negative effects on aponeurosis stiffness in the longitudinal direction, and thereby how springlike the MTU was. Konow et al (2020) used fluoromicrometry of the M. gastrocnemius medialis in rats to show that, as slope and gait change during locomotion, muscle fibre and tendon lengths and muscle width increase, whilst muscle thickness decreases. XROMM with soft tissue implantations has also been used in veterinary contexts, such as the superficial digital flexor tendons in the forelimbs of ponies, revealing up to ∼6% strain in vivo during trotting ( Wagner et al, 2021 ).…”