The energy of muscle contraction. IV. Greater mass of larger muscles decreases contraction efficiency

Abstract

While skeletal muscle mass has been shown to decrease mass-specific mechanical work per cycle, it is not yet known how muscle mass alters contraction efficiency. In this study, we examined the effect of muscle mass on mass-specific metabolic cost and efficiency during cyclic contractions in simulated muscles of different sizes. We additionally explored how tendon and its stiffness alters the effects of muscle mass on mass-specific work, mass-specific metabolic cost and efficiency across different muscle sizes. To examine contraction efficiency, we estimated the metabolic cost of the cycles using established cost models. We found that for motor contractions in which the muscle was primarily active during shortening, greater muscle mass resulted in lower contraction efficiency, primarily due to lower mass-specific mechanical work per cycle. The addition of a tendon in series with the mass-enhanced muscle model improved the mass-specific work and efficiency per cycle with greater mass for motor contractions, particularly with a shorter excitation duty cycle, despite higher predicted metabolic cost. The results of this study indicate that muscle mass is an important determinant of whole muscle contraction efficiency.

Using physiologically-based models to predictin vivoskeletal muscle energetics

“…To better capture this aspect of muscle contraction, we could implement a three-dimensional model of muscle (eg. Blemker and Delp [2005], Dick and Wakeling [2018], Wakeling et al [2020]), which would allow us to account for not only the effects of architecture on the muscle fascicle shortening but also the energy required to deform the muscle itself [Wakeling et al, 2020, Ross et al, 2021, Ross and Wakeling, 2021]. Another aspect that has been simplified in the model is the use of a constant tendon stiffness.…”

Understanding Australia’s unique hopping species: a comparative review of the musculoskeletal system and locomotor biomechanics in Macropodoidea

“…Macropodoids also increase joint torque, to a lesser extent, with positive allometry of muscle moment arms (hip, ankle ∝ M 0.42 , knee ∝ M 0.40 ) (McGowan et al 2008b). The required muscle force scales with a higher exponent than the observed muscle PCSA across macropodoid species (∝M 1.00 vs ∝M 0.92 ), meaning that larger species will generate proportionally less force from their muscles than smaller macropods, particularly if we consider that muscle efficiency decreases as muscle mass increases (Ross and Wakeling 2021). However, when the scaling of the muscle moment arms is taken into account, the resulting joint moment capacity remains proportionate in larger macropodoids (McGowan et al 2008b).…”

Scaling of buccal mass growth and muscle activation determine the duration of feeding behaviors in the marine mollusc Aplysia californica

“…The MPS framework identifies the physical forces and mechanical constraints on behaviour, but behaviour is also shaped by physiological processes that show greater variation between species ( Sutton, et al, 2023 ). For example, muscle contraction shows substantial scale-dependent variation, including in muscle shortening velocity ( Hill, 1950 ; Medler, 2002 ; Marx et al, 2006 ), muscle deactivation rate ( Marsh, 1990 ), inertial resistance due to muscle mass ( Ross et al, 2020 ; Ross and Wakeling, 2021 ) and the time constants of muscle activation ( James et al, 1998 ; Van Wassenbergh et al, 2007 ; Ross et al, 2018 ). In legged or winged locomotion across taxa, maximum muscle velocity scales negatively with mass ( Medler, 2002 ), but no evidence was found for such a relationship in swimming or non-locomotory behaviours ( Medler, 2002 ).…”