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 2D 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 in relative tonicities of 70%,
60%, and 55% were 1.13, 1.78, and 2.10, 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 to 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.