Increasing intramuscular fluid volume increases passive tension in mammalian skeletal muscle

Experimental work in amphibian skeletal muscle and modeling studies have demonstrated that intramuscular fluid volume is an important determinant of the passive force that develops during lengthening. However, this effect has yet to be investigated in mammalian skeletal muscle. Therefore, we exposed isolated mouse soleus and extensor digitorum longus (EDL) muscles to a graded series of hypotonic solutions to promote fluid uptake while measuring passive force development, muscle mass, and two-dimensional (2-D) projected muscle area. Normalized to the tension measured at 1.2 L₀ in isotonic Ringer's solution, the relative passive forces in the soleus were 1.14, 1.31, 1.52, and 1.92 in 70%, 60%, 55%, and 50% relative tonicity, respectively. Comparable values for the EDL were 1.13, 1.78, and 2.10 in 70%, 60%, and 55% relative tonicity, respectively. In both muscles, increases in passive force were accompanied by increases in mass and projected area. We also investigated the effect of muscle tension on fluid uptake. Soleus muscles left slack and allowed to shorten when exposed to a hypotonic solution gained much more mass compared with muscles held at the predicted length for maximal active force production, which suggests that at this length water uptake is limited by the buildup of hydrostatic pressure. Our findings support the hypothesis that in mammalian muscle, intramuscular fluid volume is an important determinant of passive force development. These results could have implications for human movement performance, where muscle volume change has been observed in vivo.NEW & NOTEWORTHY Our data suggest that intramuscular fluid volume is a determinant of passive force development in mammalian skeletal muscle. The amount of fluid a muscle takes up, and the associated passive force increase, may be fiber-type and muscle-dependent. In addition, we show that there may be an effect of hydrostatic pressure on fluid uptake, with muscles experiencing no tension taking up more fluid than muscles in tension. Together, these findings may have movement performance applications.