Work Production and Work Absorption in Muscle Strips from Vertebrate Cardiac and Insect Flight Muscle Fibers

Abstract

Stretch activation, which underlies the ability of all striated muscles to do oscillatory work, is a prominent feature of both insect flight and vertebrate cardiac muscle. We have examined and compared work-producing and work-absorbing processes in skinned fibers of Drosophila flight muscle, mouse papillary muscle, and human ventricular strips. Using small amplitude sinusoidal length perturbation analysis, we distinguished viscoelastic properties attributable to crossbridge processes from those attributable to other structures of the sarcomere. Work-producing and work-absorbing processes were identified in Ca²⁺-activated fibers by deconvolving complex stiffness data. An ‘active’ work-producing process (“B”), attributed to crossbridge action, was identified, as were two work-absorbing processes, one attributable to crossbridge action (“C”) and the other primarily to viscoelastic properties of parallel passive structures (“A”). At maximal Ca²⁺-activation (pCa 5, 27°C), maximum net power output (processes A, B and C combined) occurs at a frequency of: 1.3 ± 0.1 Hz for human, 10.9 ± 2.2 Hz for mouse, and 226 ± 9 Hz for fly, comparable to the resting heart rate of the human (1 Hz, 37°C) and mouse (10 Hz, 37°C) and to the wing beat frequency of the fruit fly (200 Hz, 22°C). Process B maximal work production per myosin head is 7–11 x 10∼²¹ J per perturbation cycle, equivalent to approximately 2 kT of energy. Process C maximal work absorption is about the same magnitude. The equivalence suggests the possibility that a thermal ratchet type mechanism operates during small amplitude length perturbations. We speculate that there may be a survival advantage in having a mechanical energy dissipater (i.e., the C process) at work in muscles if they can be injuriously stretched by the system in which they operate.