Muscles are composite structures. The protein filaments responsible for force production are bundled within fluid-filled cells, and these cells are wrapped in ordered sleeves of fibrous collagen. Recent models suggest that the mechanical interaction between intracellular fluid and extracellular collagen is essential to force production in passive skeletal muscle, ultimately allowing the material stiffness of extracellular collagen to contribute to passive muscle force at physiologically relevant muscle lengths. Such models lead to the prediction, tested here, that expansion of the fluid compartment within muscles should drive forceful shortening of muscle tissue, resulting in the production of mechanical work unassociated with contractile activity. We tested this prediction by experimentally increasing the fluid volumes of isolated bullfrog semimembranosus muscles via osmotically hypotonic bathing solutions. Over time, passive muscles bathed in hypotonic solution widened by 16.44 ± 3.66% as they took on fluid. At the same time, muscles shortened by 2.13 ± 0.75% (mean ± SD) along their line of action, displacing a force-regulated servomotor and doing measurable mechanical work. This behavior suggests a functional mechanism analogous to that of engineered pneumatic actuators and highlights the significance of three-dimensional processes of force transmission in skeletal muscle.

This data table contains the width and length data from figures 1a and 1b, as well as the strain data for all eight individuals in figure 2b. In figure 2b, strain is reported as a percentage, so the raw data must be multiplied by 100 to match the presentation in the main text.