The Mechanism of Spontaneous Oscillatory Contractions in Skeletal Muscle

• Published in: Biophysical journal Vol. 96; no. 9; pp. 3682 - 3691
• Main Authors: Smith, D.A., Stephenson, D.G.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 06.05.2009; Biophysical Society; The Biophysical Society
• Subjects: Actins - metabolism; Algorithms; Animals; Cells; Elasticity; Models, Biological; Muscle Contraction; Muscle Fibers, Fast-Twitch - physiology; Muscle Fibers, Slow-Twitch - physiology; Muscle, Molecular Motors and Cell Motility; Muscle, Skeletal - physiology; Musculoskeletal system; Myosins - metabolism; Periodicity; Proteins; Rats; Sarcomeres - physiology; Time Factors; Viscoelastic Substances; Viscoelasticity
• ISSN: 0006-3495; 1542-0086
• DOI: 10.1016/j.bpj.2009.01.039

Most striated muscles generate steady contractile tension when activated, but some preparations, notably cardiac myocytes and slow-twitch fibers, may show spontaneous oscillatory contractions (SPOC) at low levels of activation. We have provided what we believe is new evidence that SPOC is a property of the contractile system at low actin-myosin affinity, whether caused by a thin-filament regulatory system or by other means. We present a quantitative single-sarcomere model for isotonic SPOC in skeletal muscle with three basic ingredients: i), actin and myosin filaments initially in partial overlap, ii), stretch activation by length-dependent changes in the lattice spacing, and iii), viscoelastic passive tension. Modeling examples are given for slow-twitch and fast-twitch fibers, with periods of 10 s and 4 s respectively. Isotonic SPOC occurs in a narrow domain of parameter values, with small minimum and maximum values for actin-myosin affinity, a minimum amount of passive tension, and a maximum transient response rate that explains why SPOC is favored in slow–twitch fibers. The model also predicts the contractile, relaxed and SPOC phases as a function of phosphate and ADP levels. The single-sarcomere model can also be applied to a whole fiber under auxotonic and fixed-end conditions if the remaining sarcomeres are treated as a viscoelastic load. Here the model predicts an upper limit for the load stiffness that leads to SPOC; this limit lies above the equivalent loads expected from the rest of the fiber.