The active force–length relationship is invisible during extensive eccentric contractions in skinned skeletal muscle fibres

Abstract

In contrast to experimentally observed progressive forces in eccentric contractions, cross-bridge and sliding-filament theories of muscle contraction predict that varying myofilament overlap will lead to increases and decreases in active force during eccentric contractions. Non-cross-bridge contributions potentially explain the progressive total forces. However, it is not clear whether underlying abrupt changes in the slope of the nonlinear forcelength relationship are visible in long isokinetic stretches, and in which proportion cross-bridges and non-cross-bridges contribute to muscle force. Here, we show that maximally activated single skinned rat muscle fibres behave (almost across the entire working range) like linear springs. The force slope is about three times the maximum isometric force per optimal length. Cross-bridge and non-cross-bridge contributions to the muscle force were investigated using an actomyosin inhibitor. The experiments revealed a nonlinear progressive contribution of non-cross-bridge forces and suggest a nonlinear cross-bridge contribution similar to the active force-length relationship (though with increased optimal length and maximum isometric force). The linear muscle behaviour might significantly reduce the control effort. Moreover, the observed slight increase in slope with initial length is in accordance with current models attributing the non-cross-bridge force to titin.

A continuum-mechanical skeletal muscle model including actin-titin interaction predicts stable contractions on the descending limb of the force-length relation

“…Assuming homogeneous titin properties across sarcomeres, bound titin is stiffer in initially longer half-sarcomeres [31]. (This result of the titin model is in accordance with recent muscle fibre experiments [59]). Hence, in subsequent stretches, titin forces increase disproportionately in half-sarcomeres, which are initially longer.…”

“…Hence, actin—titin interaction might be particularly important for stable operation of muscles working on the descending limb of the force—length relation. Moreover, history- and activation-dependent actin—titin interactions can explain the phenomenon of force enhancement more completely than the sarcomere—length inhomogeneity theory [31] (especially forces exceeding the maximum isometric force by large amounts, e. g. [59, 72]).…”

Extensive eccentric contractions in intact cardiac trabeculae: revealing compelling differences in contractile behaviour compared to skeletal muscles

“…As demonstrated by previous investigations [2,4,57], the excised rat heart trabeculae featured a monotonically increasing FLR. This is in contrast with the typical slope change between the shallow and steep slope regions at the ascending limb of the FLR in striated skeletal muscles [5,56]. In cardiac muscle, the mean total stress was at 0.75 L 0 about 3% of the maximal isometric stress, P 0 , accompanied with zero passive stress (figure 1a, grey dotted line).…”

“…Comparing the mechanical response of skeletal [5] and cardiac muscle exposes differences in the underlying microstructure, in the force-producing mechanisms, and in the functioning of the respective muscles. Hence, the aim of our study was to investigate total force generation in intact cardiac trabeculae during extensive isokinetic eccentric contractions in order to examine a potential contribution of a calcium-dependent, adjustable spring element (i.e.…”

Biarticular muscles in light of template models, experiments and robotics: a review

“…Even molecular muscle mechanics help to simplify control (e.g. [42][43][44]). A more exhaustive discussion of such specific muscle properties can be found in [38,45].…”