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

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.

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The Energy of Muscle Contraction. III. Kinetic Energy During Cyclic Contractions

Frontiers in Physiology ◽

10.3389/fphys.2021.628819 ◽

2021 ◽

Vol 12 ◽

Author(s):

Stephanie A. Ross ◽

Sebastián Domínguez ◽

Nilima Nigam ◽

James M. Wakeling

Keyword(s):

Kinetic Energy ◽

Muscle Contraction ◽

Muscle Mass ◽

Mechanical Energy ◽

Specific Work ◽

External Work ◽

Fixed End ◽

Whole Muscle ◽

Work Loop

During muscle contraction, chemical energy is converted to mechanical energy when ATP is hydrolysed during cross-bridge cycling. This mechanical energy is then distributed and stored in the tissue as the muscle deforms or is used to perform external work. We previously showed how energy is distributed through contracting muscle during fixed-end contractions; however, it is not clear how the distribution of tissue energy is altered by the kinetic energy of muscle mass during dynamic contractions. In this study we conducted simulations of a 3D continuum muscle model that accounts for tissue mass, as well as force-velocity effects, in which the muscle underwent sinusoidal work-loop contractions coupled with bursts of excitation. We found that increasing muscle size, and therefore mass, increased the kinetic energy per unit volume of the muscle. In addition to greater relative kinetic energy per cycle, relatively more energy was also stored in the aponeurosis, and less was stored in the base material, which represented the intra and extracellular tissue components apart from the myofibrils. These energy changes in larger muscles due to greater mass were associated lower mass-specific mechanical work output per cycle, and this reduction in mass-specific work was greatest for smaller initial pennation angles. When we compared the effects of mass on the model tissue behaviour to that of in situ muscle with added mass during comparable work-loop trials, we found that greater mass led to lower maximum and higher minimum acceleration in the longitudinal (x) direction near the middle of the muscle compared to at the non-fixed end, which indicates that greater mass contributes to tissue non-uniformity in whole muscle. These comparable results for the simulated and in situ muscle also show that this modelling framework behaves in ways that are consistent with experimental muscle. Overall, the results of this study highlight that muscle mass is an important determinant of whole muscle behaviour.

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Added mass in rat plantaris muscle causes a reduction in mechanical work

Journal of Experimental Biology ◽

10.1242/jeb.224410 ◽

2020 ◽

Vol 223 (19) ◽

pp. jeb224410

Author(s):

Stephanie A. Ross ◽

Barbora Rimkus ◽

Nicolai Konow ◽

Andrew A. Biewener ◽

James M. Wakeling

Keyword(s):

Muscle Mass ◽

Maximum Velocity ◽

Length Change ◽

Added Mass ◽

Mechanical Work ◽

Type Model ◽

Plantaris Muscle ◽

Tissue Mass ◽

Cyclic Contractions ◽

Modelling Studies

ABSTRACTMost of what we know about whole muscle behaviour comes from experiments on single fibres or small muscles that are scaled up in size without considering the effects of the additional muscle mass. Previous modelling studies have shown that tissue inertia acts to slow the rate of force development and maximum velocity of muscle during shortening contractions and decreases the work and power per cycle during cyclic contractions; however, these results have not yet been confirmed by experiments on living tissue. Therefore, in this study we conducted in situ work-loop experiments on rat plantaris muscle to determine the effects of increasing the mass of muscle on mechanical work during cyclic contractions. We additionally simulated these experimental contractions using a mass-enhanced Hill-type model to validate our previous modelling work. We found that greater added mass resulted in lower mechanical work per cycle relative to the unloaded trials in which no mass was added to the muscle (P=0.041 for both 85 and 123% increases in muscle mass). We additionally found that greater strain resulted in lower work per cycle relative to unloaded trials at the same strain to control for length change and velocity effects on the work output, possibly due to greater accelerations of the muscle mass at higher strains. These results confirm that tissue mass reduces muscle mechanical work at larger muscle sizes, and that this effect is likely amplified for lower activations.

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Tail suspension is useful as a sarcopenia model in rats

Laboratory Animal Research ◽

10.1186/s42826-020-00083-9 ◽

2021 ◽

Vol 37 (1) ◽

Author(s):

Akira Nemoto ◽

Toru Goyagi

Keyword(s):

Skeletal Muscle ◽

Muscle Contraction ◽

Experimental Model ◽

Muscle Mass ◽

Muscle Atrophy ◽

Whole Body ◽

Skeletal Muscle Atrophy ◽

Enzyme Linked Immunosorbent Assay ◽

Control Group ◽

Simple Method

Abstract Background Sarcopenia promotes skeletal muscle atrophy and exhibits a high mortality rate. Its elucidation is of the highest clinical importance, but an animal experimental model remains controversial. In this study, we investigated a simple method for studying sarcopenia in rats. Results Muscle atrophy was investigated in 24-week-old, male, tail-suspended (TS), Sprague Dawley and spontaneously hypertensive rats (SHR). Age-matched SD rats were used as a control group. The skeletal muscle mass weight, muscle contraction, whole body tension (WBT), cross-sectional area (CSA), and Muscle RING finger-1 (MuRF-1) were assessed. Enzyme-linked immunosorbent assay was used to evaluate the MuRF-1 levels. Two muscles, the extensor digitorum longus and soleus muscles, were selected for representing fast and slow muscles, respectively. All data, except CSA, were analyzed by a one-way analysis of variance, whereas CSA was analyzed using the Kruskal-Wallis test. Muscle mass weight, muscle contraction, WBT, and CSA were significantly lower in the SHR (n = 7) and TS (n = 7) groups than in the control group, whereas MuRF-1 expression was dominant. Conclusions TS and SHR presented sarcopenic phenotypes in terms of muscle mass, muscle contraction and CSA. TS is a useful technique for providing muscle mass atrophy and weakness in an experimental model of sarcopenia in rats.

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Positional isomers of a non-nucleoside substrate differentially affect myosin function

10.1101/2019.12.17.879809 ◽

2019 ◽

Author(s):

M. Woodward ◽

E. Ostrander ◽

S.P. Jeong ◽

X. Liu ◽

B. Scott ◽

...

Keyword(s):

Energy Source ◽

Muscle Contraction ◽

Motor Function ◽

Molecular Motors ◽

Molecular Motor ◽

Vesicular Transport ◽

Gain Control ◽

Mechanical Work ◽

Chemical Energy ◽

Muscle Myosin

AbstractMolecular motors have evolved to transduce chemical energy from adenosine triphosphate into mechanical work to drive essential cellular processes, from muscle contraction to vesicular transport. Dysfunction of these motors is a root cause of many pathologies necessitating the need for intrinsic control over molecular motor function. Herein, we demonstrate that positional isomerism can be used as a simple and powerful tool to control the molecular motor of muscle, myosin. Using three isomers of a synthetic non-nucleoside triphosphate we demonstrate that myosin’s force and motion generating capacity can be dramatically altered at both the ensemble and single molecule levels. By correlating our experimental results with computation, we show that each isomer exerts intrinsic control by affecting distinct steps in myosin’s mechano-chemical cycle. Our studies demonstrate that subtle variations in the structure of an abiotic energy source can be used to control the force and motility of myosin without altering myosin’s structure.Statement of SignificanceMolecular motors transduce chemical energy from ATP into the mechanical work inside a cell, powering everything from muscle contraction to vesicular transport. While ATP is the preferred source of energy, there is growing interest in developing alternative sources of energy to gain control over molecular motors. We synthesized a series of synthetic compounds to serve as alternative energy sources for muscle myosin. Myosin was able to use this energy source to generate force and velocity. And by using different isomers of this compound we were able to modulate, and even inhibit, the activity of myosin. This suggests that changing the isomer of the substrate could provide a simple, yet powerful, approach to gain control over molecular motor function.

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Reduced prosthetic stiffness lowers the metabolic cost of running for athletes with bilateral transtibial amputations

Journal of Applied Physiology ◽

10.1152/japplphysiol.00587.2016 ◽

2017 ◽

Vol 122 (4) ◽

pp. 976-984 ◽

Cited By ~ 10

Author(s):

Owen N. Beck ◽

Paolo Taboga ◽

Alena M. Grabowski

Keyword(s):

Lower Limb ◽

Metabolic Cost ◽

Ground Reaction Forces ◽

Metabolic Rates ◽

Distance Running ◽

Cost Of Transport ◽

Leg Stiffness ◽

Metabolic Costs ◽

In Series ◽

Reaction Forces

Inspired by the springlike action of biological legs, running-specific prostheses are designed to enable athletes with lower-limb amputations to run. However, manufacturer’s recommendations for prosthetic stiffness and height may not optimize running performance. Therefore, we investigated the effects of using different prosthetic configurations on the metabolic cost and biomechanics of running. Five athletes with bilateral transtibial amputations each performed 15 trials on a force-measuring treadmill at 2.5 or 3.0 m/s. Athletes ran using each of 3 different prosthetic models (Freedom Innovations Catapult FX6, Össur Flex-Run, and Ottobock 1E90 Sprinter) with 5 combinations of stiffness categories (manufacturer’s recommended and ± 1) and heights (International Paralympic Committee’s maximum competition height and ± 2 cm) while we measured metabolic rates and ground reaction forces. Overall, prosthetic stiffness [fixed effect (β) = 0.036; P = 0.008] but not height ( P ≥ 0.089) affected the net metabolic cost of transport; less stiff prostheses reduced metabolic cost. While controlling for prosthetic stiffness (in kilonewtons per meter), using the Flex-Run (β = −0.139; P = 0.044) and 1E90 Sprinter prostheses (β = −0.176; P = 0.009) reduced net metabolic costs by 4.3–4.9% compared with using the Catapult prostheses. The metabolic cost of running improved when athletes used prosthetic configurations that decreased peak horizontal braking ground reaction forces (β = 2.786; P = 0.001), stride frequencies (β = 0.911; P < 0.001), and leg stiffness values (β = 0.053; P = 0.009). Remarkably, athletes did not maintain overall leg stiffness across prosthetic stiffness conditions. Rather, the in-series prosthetic stiffness governed overall leg stiffness. The metabolic cost of running in athletes with bilateral transtibial amputations is influenced by prosthetic model and stiffness but not height. NEW & NOTEWORTHY We measured the metabolic rates and biomechanics of five athletes with bilateral transtibial amputations while running with different prosthetic configurations. The metabolic cost of running for these athletes is minimized by using an optimal prosthetic model and reducing prosthetic stiffness. The metabolic cost of running was independent of prosthetic height, suggesting that longer legs are not advantageous for distance running. Moreover, the in-series prosthetic stiffness governs the leg stiffness of athletes with bilateral leg amputations.

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Rises in whole muscle passive tension of mammalian muscle after eccentric contractions at different lengths

Journal of Applied Physiology ◽

10.1152/japplphysiol.00163.2003 ◽

2003 ◽

Vol 95 (3) ◽

pp. 1224-1234 ◽

Cited By ~ 33

Author(s):

N. P. Whitehead ◽

D. L. Morgan ◽

J. E. Gregory ◽

U. Proske

Keyword(s):

Isometric Tension ◽

The Other ◽

Medial Gastrocnemius ◽

Eccentric Contractions ◽

Passive Tension ◽

Active Length ◽

Before And After ◽

Two Factors ◽

In Series ◽

Whole Muscle

This is a report of experiments carried out on the medial gastrocnemius muscle of the anesthetized cat, investigating the effects of eccentric contractions carried out at different muscle lengths on the passive and active length-tension relationships. In one series of experiments, the motor supply to the muscle was divided into three approximately equal parts; in the other, whole muscles were used. Fifty eccentric contractions were carried out over different regions of the active length-tension curve for each partial or whole muscle. Active and passive length-tension curves were measured before and after the eccentric contractions. When eccentric contractions were carried out at longer lengths, there was a larger shift of the optimum length for active tension in the direction of longer muscle lengths and a larger fall in peak isometric tension. Passive tension was higher immediately after the eccentric contractions, and if the muscle was left undisturbed for 40 min, it increased further to higher values, particularly after contractions at longer lengths. A series of 20 passive stretches of the same speed and amplitude and covering the same length range as the active stretches, reduced the passive tension which redeveloped over a subsequent 40-min period. It is hypothesized that there are two factors influencing the level of passive tension in a muscle after a series of eccentric contractions. One is injury contractures in damaged muscle fibers tending to raise passive tension; the other is the presence of disrupted sarcomeres in series with still-functioning sarcomeres tending to reduce it.

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The mechanics and energetics of human walking and running: a joint level perspective

Journal of The Royal Society Interface ◽

10.1098/rsif.2011.0182 ◽

2011 ◽

Vol 9 (66) ◽

pp. 110-118 ◽

Cited By ~ 172

Author(s):

Dominic James Farris ◽

Gregory S. Sawicki

Keyword(s):

Power Output ◽

Lower Limb ◽

Metabolic Cost ◽

Mechanical Work ◽

Total Power ◽

Joint Mechanics ◽

Metabolic Power ◽

Cost Of Transport ◽

Cost Of Locomotion ◽

Shed Light

Humans walk and run at a range of speeds. While steady locomotion at a given speed requires no net mechanical work, moving faster does demand both more positive and negative mechanical work per stride. Is this increased demand met by increasing power output at all lower limb joints or just some of them? Does running rely on different joints for power output than walking? How does this contribute to the metabolic cost of locomotion? This study examined the effects of walking and running speed on lower limb joint mechanics and metabolic cost of transport in humans. Kinematic and kinetic data for 10 participants were collected for a range of walking (0.75, 1.25, 1.75, 2.0 m s −1 ) and running (2.0, 2.25, 2.75, 3.25 m s −1 ) speeds. Net metabolic power was measured by indirect calorimetry. Within each gait, there was no difference in the proportion of power contributed by each joint (hip, knee, ankle) to total power across speeds. Changing from walking to running resulted in a significant ( p = 0.02) shift in power production from the hip to the ankle which may explain the higher efficiency of running at speeds above 2.0 m s −1 and shed light on a potential mechanism behind the walk–run transition.

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Modeling age-related changes in muscle-tendon dynamics during cyclical contractions in the rat gastrocnemius

Journal of Applied Physiology ◽

10.1152/japplphysiol.00396.2016 ◽

2016 ◽

Vol 121 (4) ◽

pp. 1004-1012 ◽

Cited By ~ 4

Author(s):

Nicole Danos ◽

Natalie C. Holt ◽

Gregory S. Sawicki ◽

Emanuel Azizi

Keyword(s):

Elastic Energy ◽

Metabolic Cost ◽

Medial Gastrocnemius ◽

Tissue Properties ◽

Age Related ◽

In Series ◽

Force Velocity ◽

Length Changes ◽

Metabolic Performance ◽

Age Related Changes

Efficient muscle-tendon performance during cyclical tasks is dependent on both active and passive mechanical tissue properties. Here we examine whether age-related changes in the properties of muscle-tendon units (MTUs) compromise their ability to do work and utilize elastic energy storage. We empirically quantified passive and active properties of the medial gastrocnemius muscle and material properties of the Achilles tendon in young (∼6 mo) and old (∼32 mo) rats. We then used these properties in computer simulations of a Hill-type muscle model operating in series with a Hookean spring. The modeled MTU was driven through sinusoidal length changes and activated at a phase that optimized muscle-tendon tuning to assess the relative contributions of active and passive elements to the force and work in each cycle. In physiologically realistic simulations where young and old MTUs started at similar passive forces and developed similar active forces, the capacity of old MTUs to store elastic energy and produce positive work was compromised. These results suggest that the observed increase in the metabolic cost of locomotion with aging may be in part due to the recruitment of additional muscles to compensate for the reduced work at the primary MTU. Furthermore, the age-related increases in passive stiffness coupled with a reduced active force capacity in the muscle can lead to shifts in the force-length and force-velocity operating range that may significantly impact mechanical and metabolic performance. Our study emphasizes the importance of the interplay between muscle and tendon mechanical properties in shaping MTU performance during cyclical contractions.

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