Theory and observation of spontaneous oscillatory contractions in skeletal myofibrils

At low levels of activation, an isometrically-held myofibrillar preparation on the descending limb may exhibit persistent oscillations of period 1-6 s in tension and sarcomere lengths. We propose a sarcomeric theory of spontaneous oscillatory contraction, based on the phenomena of force creep and delayed length activation. The time delay leads to oscillations and controls their period. A computer model using these ideas simulates spontaneous oscillatory contraction for fixed-end fibres only if isometric tension capacity varies slightly along the fibre. The form of this inhomogeneity controls a diversity of spontaneous oscillatory contraction behaviour: the tension waveform can vary from large and sinusoidal to small-amplitude pulses or chaotic behaviour, and these variations are observed in slow-twitch soleus fibres from the same animal (rat). The model predicts that oscillatory and quiescent regions coexist in the fibre, with large-amplitude sawtooth waveforms in sarcomere length in the former as observed. It can also generate travelling-wave structures, similar to those found by the Tokyo group, in oscillating regions when there is a spatial gradient in isometric tension capacity. Phase discontinuities in sarcomere length occur near the oscillatory-quiescent boundary. Predictions for the Ca2+ concentrations and sarcomere lengths in which spontaneous oscillatory contraction occurs and for differences in the spontaneous oscillatory contraction frequencies of fast- and slow-twitch fibres compare well with experiment. Spontaneous oscillatory contraction is also predicted under isotonic conditions.