Reinterpretation of the Tension Response of Muscle to Stretches and Releases

We have reexamined the experimental time courses of tension in frog muscle after rapid length steps. The early tension recoveries are biexponential. After 3 nm/hs stretches and releases, the rates of the immediate rapid tension changes are similar but the subsequent tension fall after a stretch is much slower than the rise after a release. After 1.5 nm/hs length steps, the entire tension responses are more nearly mirror images. To identify the underlying processes, we used a model of the muscle cross-bridge cycle with two tension-generating (tensing) steps. Analysis of the time course of the tension, the rates of the steps in the cycle, and their contributions to tension provided insights into previously puzzling features of the experimental response. After a stretch, the initial rapid tension fall in the model is caused principally by the reversal of the first tensing step, but after a few milliseconds the tensing step resumes its forward direction. We conclude that the remaining response should not be included in phase 2, the period of early tension recovery. With this exclusion, T₂, the tension at the end of this period, rises with an increase of stretch. The rate of early tension recovery also increases with stretch size, showing that the reversal of the first tensing step is strain sensitive. After small length steps, the fast and slow components of the early tension recovery are both caused mainly by the first tensing step. The fast component is triggered by the initial sliding of the filaments, and the slow component is due to further sliding that occurs as the tension recovers. With small length steps (<0.5 nm/hs), the time course of the response to a stretch is the reverse of that to a release.