Evidence for multi-scale power amplification in skeletal muscle

Abstract

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.