Aim: 

Skeletal muscle can act not only as a machine that converts metabolic energy into mechanical work but also as a brake generating a high resistive force at low energetic cost when the load is suddenly increased above the isometric force (Katz, J. Physiol. 96:45,1939). Recent X-ray diffraction experiments have shown that the braking action of muscle consists in the rapid binding of the second motor domain of the myosin molecules attached to the actin filament (Brunello et al., PNAS 104:20114, 2007).

Methods: 

The mechanism of stretch dependent motor recruitment is further investigated here by using fast sarcomere level mechanics in intact fibres from the skeletal muscle of the frog (Rana esculenta) to measure the changes in the half-sarcomere (hs) stiffness following step stretches of different amplitude (2–8 nm hs^-1). The results are interpreted with a mechanical model of the half-sarcomere that takes into account the contribution of the filament compliance to hs compliance.

Results: 

Additional motors are recruited already at the end of a 100 ms stretch and recruitment continues during the 2 ms of the quick force recovery following the stretch. When plotted against the axial distortion of the attached motors (Dz) produced by the stretch, the recruitment of new motors is the same for the same Dz, independently of the time elapsed after the stretch. On the contrary, the distortion at which motor recruitment saturates (Dz_c)depends on the phase of the force response to stretch: Dz_c is ~2 nm at the end of the stretch and ~4 nm 2 ms later.

Conclusions: 

The distortion of the attached motors is the only factor that drives the rapid recruitment of the partner motor. This mechanism allows the muscle to resist a stretch, rapidly redistributing the force excess amongst the motors, so that at 2 ms following the stretch the stress imposed on each motor is the same as that generated during the isometric contraction.

Supported by NIH (R01 AR049033) and MiUR (Italy)