Modulation of passive force in single skeletal muscle fibres

Abstract

In this study, we investigated the effects of activation and stretch on the passive force-sarcomere length relationship in skeletal muscle. Single fibres from the lumbrical muscle of frogs were placed at varying sarcomere lengths on the descending limb of the force-sarcomere length relationship, and tetanic contractions, active stretches and passive stretches (amplitudes of ca 10% of fibre length at a speed of 40% fibre length/s) were performed. The passive forces following stretch of an activated fibre were higher than the forces measured after isometric contractions or after stretches of a passive fibre at the corresponding sarcomere length. This effect was more pronounced at increased sarcomere lengths, and the passive force-sarcomere length relationship following active stretch was shifted upwards on the force axis compared with the corresponding relationship obtained following isometric contractions or passive stretches. These results provide strong evidence for an increase in passive force that is mediated by a length-dependent combination of stretch and activation, while activation or stretch alone does not produce this effect. Based on these results and recently published findings of the effects of Ca2+ on titin stiffness, we propose that the observed increase in passive force is caused by the molecular spring titin.

Figure 1

Force–time and sarcomere-length time histories of isometric contractions, active stretches and passive stretches in a typical experiment (a) in Ringer solution and (b) after adding 5 mM BDM. The inset shows isometric contractions performed at 2.0 μm at the beginning and at the end of one typical experiment. Note that the isometric force did not decrease throughout the experiment, suggesting that the quality of the fibres was preserved after stretches and BDM treatment. Act: active stretch; Pas: passive stretch. Iso: isometric contraction. Arrows show the times when passive forces were measured.

Figure 2

Passive force–sarcomere length relationship after isometric contractions, active stretches and passive stretches. All data were approximated with best-fitting second order polynomial equations. In panels (a) and (b), experiments from two representative fibres are shown, along with the best-fit lines and 95% confidence intervals. Note that the data points for the actively stretched fibres do not overlap with those recorded after isometric contractions or passive stretches. In panel (c), mean (±standard error) values are shown from data that were grouped into intervals of 0.2 μm (range: 2.2–3.2 μm). With the exception of a sarcomere length of 2.2 μm, there is a significant increase (p<0.05) in the passive force following active stretch compared with the passive force following isometric contraction and passive stretch.