The non‐linear elasticity of the muscle sarcomere and the compliance of myosin motors

Key points The force in the half‐sarcomere (hs), the functional unit of muscle, is due to the contributions of individual myosin motors arranged in parallel in the half‐myosin filament and pulling on the opposing actin filament. According to a linear hs model, during an isometric contraction the force rises to its maximal steady value ( T 0 ) in proportion to the number of actin‐attached motors, while the hs strain rises with a slope that depends on the compliance of the myofilaments. We measured the hs stiffness, superimposing small 4 kHz length oscillations on the development of isometric contraction, and found an elastic element in parallel to the myosin motors with a constant stiffness ∼1/20th that of the motor array at T 0 . The results support a structural model in which myosin motors are distributed in multiple substates, of which only the first ones are occupied during isometric force generation, causing a motor strain of ∼1.7 nm. Abstract Force in striated muscle is due to attachment of the heads of the myosin, the molecular motors extending from the myosin filament, to the actin filament in each half‐sarcomere, the functional unit where myosin motors act in parallel. Mechanical and X‐ray structural evidence indicates that at the plateau of isometric contraction (force T 0 ), less than half of the elastic strain of the half‐sarcomere is due to the strain in the array of myosin motors ( s ), with the remainder being accounted for by the compliance of filaments acting as linear elastic elements in series with the motor array. Early during the development of isometric force, however, the half‐sarcomere compliance has been found to be less than that expected from the linear elastic model assumed above, and this non‐linearity may affect the estimate of s . This question is investigated here by applying nanometre–microsecond‐resolution mechanics to single intact fibres from frog skeletal muscle at 4°C, to record the mechanical properties of the half‐sarcomere throughout the development of force in isometric contraction. The results are interpreted with mechanical models to estimate the compliance of the myosin motors. Our conclusions are as follows: (i) early during the development of an isometric tetanus, an elastic element is present in parallel with the myosin motors, with a compliance of ∼200 nm MPa −1 (∼20 times larger than the compliance of the motor array at T 0 ); and (ii) during isometric contraction, s is 1.66 ± 0.05 nm, which is not significantly different from the value estimated with the linear elastic model.