Energy cost of isometric force production after active shortening in skinned muscle fibres

Abstract

The steady-state isometric force after active shortening of a skeletal muscle is lower than the purely isometric force at the corresponding length. This property of skeletal muscle is known as force depression. The purpose of this study was to investigate whether the energy cost of force production at the steady state after active shortening was reduced compared with the energy cost of force production for a purely isometric contraction performed at the corresponding length (same length, same activation). Experiments were performed in skinned fibres isolated from rabbit psoas muscle. Skinned fibres were actively shortened from an average sarcomere length of 3.0 µm to an average sarcomere length of 2.4 µm. Purely isometric reference contractions were performed at an average sarcomere length of 2.4 µm. Simultaneously with the force measurements, the ATP cost was measured during the last 30 s of isometric contractions using an enzyme-coupled assay. Stiffness was calculated during a quick stretch-release cycle of 0.2% fibre length performed once the steady state had been reached after active shortening and during the purely isometric reference contractions. Force and stiffness following active shortening were decreased by 10.0±1.8% and 11.0±2.2%, respectively, compared with the isometric reference contractions. Similarly, ATPase activity per second (not normalized to the force) showed a decrease of 15.6±3.0% in the force-depressed state compared with the purely isometric reference state. However, ATPase activity per second per unit of force was similar for the isometric contractions following active shortening (28.7± 2.4 mmol l −1 mN -1 s mm 3 ) and the corresponding purely isometric reference contraction (30.9±2.8 mmol l −1 mN −1 s mm 3 ). Furthermore, the reduction in absolute ATPase activity per second was significantly correlated with force depression and stiffness depression. These results are in accordance with the idea that force depression following active shortening is primarily caused by a decrease in the proportion of attached cross-bridges. Furthermore, these findings, along with previously reported results showing a decrease in ATP consumption per unit of force after active muscle stretching, suggest that the mechanisms involved in the steady-state force after active muscle shortening and active muscle lengthening are of distinctly different origin.

Force depression following a stretch-shortening cycle is independent of stretch peak force and work performed during shortening

“…Marechal and Plaghki (1979) proposed that FD is associated with a reduction of the proportion of attached cross-bridges because of a stress-induced deformation of the actin filaments entering the myofilament overlap zone in the shortening phase. This theory is consistent with the reduction in muscle stiffness observed in the FD state compared to purely isometric reference contractions 18 , and the maintenance of ATP consumption per unit of force in the FD state 19 .…”

The metabolic cost of in vivo constant muscle force production at zero net mechanical work

“…Reduction of metabolic cost was largest at fibre lengths that exceed optimum length. In contrast, force depression does not affect the metabolic cost of isometric force production (Joumaa et al, 2017). It is unclear to what extent these results can be generalized to prolonged in vivo contractions at fibre lengths below optimum length.…”

“…Recent in vitro studies have indicated that muscle history effects may reduce the metabolic cost of muscle fibre contractions (Joumaa and Herzog, 2013;Joumaa et al, 2017). Residual force enhancement in skinned fibres has been reported to decrease metabolic cost of isometric force production by 17.2±4.1% (mean± s.d.)…”

Dynamic multivoxel‐localized 31P MRS during plantar flexion exercise with variable knee angle

“…it crosses two joints in series and is therefore shortened in length with a flexed knee, while soleus is attached to the tibia and does not change in length by knee angulation. () Muscle shortening has been linked to a decrease in the number of available sites for cross‐bridge formation, which influences a muscle's force output and hence energy cost . Furthermore, the relation between sarcomere length and force output depends on the type of muscle .…”

“…15,16 Muscle shortening has been linked to a decrease in the number of available sites for cross-bridge formation, 19 which influences a muscle's force output 31 and hence energy cost. 32 Furthermore, the relation between sarcomere length and force output depends on the type of muscle. 31 This may contribute to the explanation of why PCr depletion in soleus did not increase to the same extent as the corresponding decrease in gastrocnemius.…”