Trading force for speed: Why superfast crossbridge kinetics leads to superlow forces

Abstract

Superfast muscles power high-frequency motions such as sound production and visual tracking. As a class, these muscles also generate low forces. Using the toadfish swimbladder muscle, the fastest known vertebrate muscle, we examined the crossbridge kinetic rates responsible for high contraction rates and how these might affect force generation. Swimbladder fibers have evolved a 10-fold faster crossbridge detachment rate than fast-twitch locomotory fibers, but surprisingly the crossbridge attachment rate has remained unchanged. These kinetics result in very few crossbridges being attached during contraction of superfast fibers (only Ϸ1͞6 of that in locomotory fibers) and thus low force. This imbalance between attachment and detachment rates is likely to be a general mechanism that imposes a tradeoff of force for speed in all superfast fibers.The superfast fiber type is found where high-frequency contractions are required, such as in vertebrate eye muscles and in both vertebrate and invertebrate synchronous soundproducing muscles. These muscles have a series of modifications for speed, including a large volume of sarcoplasmic reticulum (SR) (1-7) to produce very rapid calcium transients (8) and low-affinity troponin to speed myofilament deactivation after [Ca 2ϩ

Is sexual dimorphism in singing behavior related to syringeal muscle composition?

“…Interestingly, the superfast fibers, which contract at rates reaching 250 Hz, are, in some cases, double the size of fast fibers. Perhaps this increased diameter compensates for otherwise low force production, which is likely to result from the trade-off between force and speed (Rome et al 1996, Rome and Linstedt 1998, Rome et al 1999, Rome 2006. Individual muscle size is limited by constraints of overall body size, but it is unclear whether the size of individual structures, such as the syrinx, also influences the maximal diameter of muscle fibers.…”

“…These fibers contract faster than typical vertebrate ''fast'' muscle and display a trade-off between force generation and speed (Rome 2006). In songbirds, superfast fibers have been shown to produce positive work up to 250 Hz in European Starlings and up to 200 Hz in male Zebra Finches (Elemans et al 2008), placing them among the fastest vertebrate skeletal muscles (e.g., Rome et al 1996, Rome et al 1999. Uchida et al (2010) described both superfast and fast fibers in the European Starling syrinx.…”

Range-based techniques for discovering optimality and analyzing scaling relationships in neuromechanical systems

“…Changes driven by muscular control may involve a robustness mechanism which provides a mechanism for adaptation that is semi-independent of the perturbation. Muscle fiber recruitment and protein expression in the cross bridges of the muscle fibers during contraction may allow for this robustness mechanism to compensate for morphological control and override neural control under certain conditions (Rome et al, 1999).…”

“…Another factor that determines performance is adaptation based on the interaction of neuromuscular behavior and adaptation. There are various regularities in the properties of muscle mass, muscle fiber composition, and mechanical advantage during function that is related in a linear fashion when compared across phenotypes of different sizes (Barry and Enoka, 2007;Rome, 1999). …”

Vocal production complexity correlates with neural instructions in the oyster toadfish (Opsanus tau)

“…2A). Because superfast muscles trade off force for speed (Rome et al, 1999) and energetic cost (Rome, 2006), the design for highfrequency contractions results in reduced muscle power output (Young and Rome, 2001) and lower acoustic power radiated. The acoustical power radiated as a function of stimulation frequency (Fig.…”