Power amplification in an isolated muscle-tendon is load dependent

Abstract

During rapid movements, tendons can act like springs, temporarily storing work done by muscles and then releasing it to power body movements. For some activities, such as frog jumping, energy is released from tendon much more rapidly than it is stored, thus amplifying muscle power output. The period during which energy is loaded into a tendon by muscle work may be aided by a catch mechanism that restricts motion, but theoretical studies indicate that power can be amplified in a muscle-tendon load system even in the absence of a catch. To explore the limits of power amplification with and without a catch, we studied the bullfrog plantaris muscle-tendon during in vitro contractions. A novel servomotor controller allowed us to measure muscle-tendon unit (MTU) mechanical behavior during contractions against a variety of simulated inertial-gravitational loads, ranging from zero to 1× the peak isometric force of the muscle. Power output of the MTU system was load dependent and power amplification occurred only at intermediate loads, reaching ∼1.3× the peak isotonic power output of the muscle. With a simulated anatomical catch mechanism in place, the highest power amplification occurred at the lowest loads, with a maximum amplification of more than 4× peak isotonic muscle power. At higher loads, the benefits of a catch for MTU performance diminished sharply, suggesting that power amplification >2.5× may come at the expense of net mechanical work delivered to the load.

Additional in-series compliance reduces muscle force summation and alters the time course of force relaxation during fixed-end contractions

“…This assertion is in agreement with models of muscle-tendon interaction, which predict that the force-length relationship should shift rightward and become skewed toward initial sarcomere lengths on the ascending limb as series elastic compliance increases (Lieber et al, 1992). The plantaris muscle of the bullfrog has a high fixed-end compliance (∼30%; Sawicki et al, 2015b), but avoids operating at fibre lengths on the ascending limb during the take-off phase of jumping by beginning at lengths on the descending limb. Force attenuation in this muscle is mitigated by actively shortening from lengths beyond optimum length onto the plateau region prior to take-off (Azizi and Roberts, 2010).…”

Effects of temperature and force requirements on muscle work and power output

“…In contractions of a muscle tendon unit with simulated loads, low loads relative to P 0 (∼17.5% P 0 ) tend to produce the greatest amount of muscle power amplification (Sawicki et al, 2015). These relatively low forces that maximize performance as measured by power amplification (Sawicki et al, 2015) also maximize thermal performance, as we have shown (Table 1, Fig.…”

“…Elastic systems in which relatively large muscles are moving small loads are optimized for power amplification, but not muscle work (Sawicki et al, 2015). In contractions of a muscle tendon unit with simulated loads, low loads relative to P 0 (∼17.5% P 0 ) tend to produce the greatest amount of muscle power amplification (Sawicki et al, 2015).…”

“…However, shortening with intermediate forces relative to P 0 (∼50% P 0 ) will increase performance measured as muscle work (Fig. 3) (Sawicki et al, 2015). Therefore, there is an High temp.…”

“…Many movements involved in feeding and locomotion require single muscle contractions, rather than a series of stretch-shortening cycles, and in these cases the work done by a muscle depends on the specific load being moved. Muscle contractions in simulated elastic-recoil mechanisms have revealed that work output is optimized when the muscle is shortening at intermediate loads (∼50% peak isometric tetanic force) (Sawicki et al, 2015). Therefore, the effects of temperature on muscle contraction in elastic-recoil mechanisms are most relevant under prescribed-load conditions, rather than cycles of imposed length changes and fluctuating load.…”