Evidence for multi-scale power amplification in skeletal muscle

Abstract

Many animals use a combination of skeletal muscle and elastic structures to amplify power output for fast motions. Among vertebrates, tendons in series with skeletal muscle are often implicated as the primary power-amplifying spring, but muscles contain elastic structures at all levels of organization, from the muscle tendon to the extracellular matrix to elastic proteins within sarcomeres. The present study used ex vivo muscle preparations in combination with high-speed video to quantify power output, as the product of force and velocity, at several levels of muscle organization to determine where power amplification occurs. Dynamic ramp-shortening contractions in isolated frog flexor digitorum superficialis brevis were compared with isotonic power output to identify power amplification within muscle fibers, the muscle belly, free tendon and elements external to the muscle tendon. Energy accounting revealed that artifacts from compliant structures outside of the muscle-tendon unit contributed significant peak instantaneous power. This compliance included deflection of clamped bone that stored and released energy contributing 195.22±33.19 W kg-1 (mean±s.e.m.) to the peak power output. In addition, we found that power detected from within the muscle fascicles for dynamic shortening ramps was 338.78±16.03 W kg-1, or approximately 1.75 times the maximum isotonic power output of 195.23±8.82 W kg-1. Measurements of muscle belly and muscle-tendon unit also demonstrated significant power amplification. These data suggest that intramuscular tissues, as well as bone, have the capacity to store and release energy to amplify whole-muscle power output.

Keywords: Lithobates catesbeianus; Elastic recoil; Frog; Locomotion; Power output.

Fig. 1.

Isolated muscle preparation schematic. (A) Schematic of the mounted muscle next to an enlarged image of the muscle belly illustrating pennation angle (θ) about a red muscle fascicle and a red dashed vertical axis. (B) Still image from a video recording, with segments labeled illustrating how length changes of the muscle–tendon unit (L_MTU), muscle belly (L_Belly) and muscle fascicles (L_Fasc), and instantaneous length changes about a single point along the distal bone (ΔL_Bone), were calculated.

Fig. 2.

The isotonic force, velocity and power relationship. Individual normalized force and velocity data (black) are well fit by a modified Hill equation (gray) (Marsh and Bennett, 1986). Results from each individual muscle are plotted as different shapes (n=6), and power (blue) was calculated from the modified Hill equation.

Fig. 3.

Contractile time series data. Data from a single representative individual (n=1) 60 mm s⁻¹ ramp shortening contraction is plotted against time in milliseconds. Length and power of each measured level of muscle organization are shown, along with force measured from the muscle motor (gray). The red horizontal line indicates the measured maximum isotonic power.

Fig. 4.

Power from potential springs at multiple levels of organization. (A) Power (W kg⁻¹) and power amplification (power relative to isotonic max.) are shown for a ramp shortening contraction of 160 mm s⁻¹. (B) An illustration highlights potential sources of elastic energy storage at multiple levels of organization. Opaque dashed boxes on the bar plot are estimates meant to highlight differences between bars potentially due to elastic elements at each level; elastic elements are named within these boxes as possible contributors (Apo, aponeurosis). The red horizontal line indicates the measured maximum isotonic power and the results are shown for the one-way repeated-measures ANOVA (*P<0.05, ***P<0.001; n=6).

Fig. 5.

Power output increases with increasing ramp shortening velocity. Power is plotted in W kg⁻¹ over the velocity of shortening ramps input from a control signal to the muscle motor. All four different shortening conditions are shown. Standard error of the mean is represented by the error bars (n=6). The red horizontal line indicates the measured maximum isotonic power.