Sarcomere dynamics and contraction-induced injury to maximally activated single muscle fibres from soleus muscles of rats.

1. The focal nature of contraction-induced injury to skeletal muscle fibres may arise from heterogeneities in sarcomere length that develop during contractions. We tested the hypothesis that when a maximally activated single permeabilized fibre segment is stretched and a deficit in maximum isometric force (force deficit) is produced, the regions of sarcomeres with the longest lengths of prior to the stretch contain the majority of the damaged sarcomeres when the fibre is returned to optimum length (Lo) after the stretch. 2. Single fibre segments (n = 16) were obtained from soleus muscles of rats. Average sarcomere length at five discrete positions along the length of each fibre was determined by lateral deflection of a diode laser spot. Diffraction patterns were obtained while fibres were relaxed and immediately before, during and after a single stretch of 40% strain relative to Lo. Following the stretch, the regions of each fibre that potentially contained damaged sarcomeres were identified by an increased scatter of the first-order diffraction patterns. The damage was confirmed by light and electron microscopy. 3. While single fibre segments were in relaxing solution, the mean value for all of the average sarcomere lengths sampled (n = 80) was 2.53 +/- 0.01 microns (range, 2.40-2.68 microns). During the maximum isometric contraction before each stretch, the mean sarcomere length decreased to 2.42 +/- 0.02 microns and the range increased to 2.12-3.01 microns. 4. During the stretch of 40% strain, all regions of sarcomeres were stretched onto the descending limb of the length-force curve, but sarcomere lengthening was non-uniform. After the stretch, when the maximally activated fibres were returned to Lo, the force deficit was 10 +/- 1%. Microscopic evaluation confirmed that the regions with the longest sarcomere lengths before the stretch contained the majority of the damaged sarcomeres after the stretch. We conclude that when heterogeneities in sarcomere length develop in single permeabilized fibre segments during a maximum isometric contraction, the sarcomeres in the regions with the longest lengths are the most susceptible to contraction-induced injury.