Eccentric muscle contractions: from single muscle fibre to whole muscle mechanics

Abstract

Eccentric muscle loading encompasses several unique features compared to other types of contractions. These features include increased force, work, and performance at decreased oxygen consumption, reduced metabolic cost, improved energy efficiency, as well as decreased muscle activity. This review summarises explanatory approaches to long-standing questions in terms of muscular contraction dynamics and molecular and cellular mechanisms underlying eccentric muscle loading. Moreover, this article intends to underscore the functional link between sarcomeric components, emphasising the fundamental role of titin in skeletal muscle. The giant filament titin reveals versatile functions ranging from sarcomere organisation and maintenance, providing passive tension and elasticity, and operates as a mechanosensory and signalling platform. Structurally, titin consists of a viscoelastic spring segment that allows activation-dependent coupling to actin. This titin-actin interaction can explain linear force increases in active lengthening experiments in biological systems. A three-filament model of skeletal muscle force production (mediated by titin) is supposed to overcome significant deviations between experimental observations and predictions by the classic sliding-filament and cross-bridge theories. Taken together, this review intends to contribute to a more detailed understanding of overall muscle behaviour and force generation—from a microscopic sarcomere level to a macroscopic multi-joint muscle level—impacting muscle modelling, the understanding of muscle function, and disease.

Conserved mammalian muscle mechanics during eccentric contractions

“…Phase‐2 of the force development profile has been equally under‐investigated, despite it being routinely described in the literature (Josephson & Stokes, 1999; Joyce et al., 1969; Lombardi & Piazzesi, 1990; Stienen et al., 1992; Tomalka, 2023). Again, this is probably partly a result of the lack of standardised experimental approaches for muscle lengthening experimentation and quantification.…”

“…The physiological underpinning of the distinct biphasic force development response during eccentric lengthening is still a contentious topic. It is assumed that the initial rapid phase-1 profile is a response to elevated strain of attached cross-bridges, after which the detachment of myosin heads leads to the transition into a shallower phase-2 force response (Tomalka, 2023;Tomalka et al, 2020Tomalka et al, , 2021Weidner et al, 2022), whereas the phase-2 force response is assumed to be linked to increased strain of non-cross-bridge parallel elastic elements (Ramsey et al, 2010;Tomalka, 2023). To the best of our knowledge, this is the first comprehensive overview of eccentric muscle characteristics in mammalian muscle.…”

“…This complex phenomenon is thought to arise from two distinct mechanical processes. First, the initial rapid phase-1 response is hypothesised to arise from elevated strain of attached cross-bridges, after which the detachment of myosin heads leads to the transition into the shallower phase-2 force response (Tomalka, 2023;Tomalka et al, 2020Tomalka et al, , 2021Weidner et al, 2022). The phase-2 force response is assumed to be linked to increased strain of non-cross-bridge, parallel elastic elements (Ramsey et al, 2010;Tomalka, 2023).…”

“…Finally, as mentioned previously, the rapid phase-1 force development profile is assumed to be the response to elevated strain of attached cross-bridges (Tomalka, 2023;Tomalka et al, 2020Tomalka et al, , 2021Weidner et al, 2022), with the phase-2 force response assumed to be linked to increased strain of non-cross-bridge parallel elastic elements (De Ruiter et al, 2000;Ramsey et al, 2010;Tomalka, 2023). Recent work has shown that titin plays an important role in both passive and active muscle properties, contributing to force enhancement and depression during lengthening and shortening contractions (Tahir et al, 2020).…”

“…First, the initial rapid phase‐1 response is hypothesised to arise from elevated strain of attached cross‐bridges, after which the detachment of myosin heads leads to the transition into the shallower phase‐2 force response (Tomalka, 2023; Tomalka et al., 2020, 2021; Weidner et al., 2022). The phase‐2 force response is assumed to be linked to increased strain of non‐cross‐bridge, parallel elastic elements (Ramsey et al., 2010; Tomalka, 2023). Little is known about the rate of force development in these two phases in relation to lengthening velocity, or how or whether this relationship differs between muscles of distinctive phenotypes, or as a result of scaling in relation to body mass.…”