Lengthening Contractions Produce Strain-Dependent Regional Changes in the Passive Length-Tension Properties of Permeabilized Single Fibers

Abstract

During forced lengthening of an activated skeletal muscle fiber (a “lengthening contraction”), the applied strain is not distributed uniformly along the length of the fiber. Instead, regions having the longest sarcomere lengths (Ls) prior to the stretch are strained the most during the stretch (Panchangam et al. Biophys. J. 95:1890-1901, 2008). These differences in regional strain result in differences in strain history that could influence the subsequent resting Ls of the regions. We hypothesized that the change in resting Ls of a region following a lengthening contraction correlates positively with the strain of the region during the lengthening contraction. This hypothesis was tested on permeabilized fibers (n=15) obtained from soleus muscles of adult rats (8-9 mo, n=5). A laser diffraction technique was used to make rapid measurements (500 s−1) of the Ls in 20 contiguous regions of fibers before, during, and after a single lengthening contraction (strain, 27 %; strain rate, 54 % s−1; temperature, 15°C). During steady-state activation prior to lengthening, fibers produced an isometric stress of 133±29 kPa at a mean Ls of 2.54±0.16 μm. The lengthening contractions resulted in a 19±9 % loss in isometric stress. For each of the 20 contiguous regions, the difference between the resting Ls 5 min before and 10 min after the lengthening contraction was plotted as a function of the increase in Ls at the peak of the lengthening contraction. The increase in resting Ls correlated positively (r=0.71) with the increase in Ls during lengthening contractions. We conclude that lengthening contractions produce regional changes in the passive length-tension properties of permeabilized single fibers and that these changes can be attributed to the recent strain history of the fiber regions. Support: NIH AG-13283; AG-015434.