Fundamental constraints in synchronous muscle limit superfast motor control in vertebrates

Abstract

Superfast muscles (SFMs) are extremely fast synchronous muscles capable of contraction rates up to 250 Hz, enabling precise motor execution at the millisecond time scale. SFM phenotypes have been discovered in most major vertebrate lineages, but it remains unknown whether all SFMs share excitation-contraction coupling pathway adaptations for speed, and if SFMs arose once, or from independent evolutionary events. Here, we demonstrate that to achieve rapid actomyosin crossbridge kinetics bat and songbird SFM express myosin heavy chain genes that are evolutionarily and ontologically distinct. Furthermore, we show that all known SFMs share multiple functional adaptations that minimize excitation-contraction coupling transduction times. Our results suggest that SFM evolved independently in sound-producing organs in ray-finned fish, birds, and mammals, and that SFM phenotypes operate at a maximum operational speed set by fundamental constraints in synchronous muscle. Consequentially, these constraints set a fundamental limit to the maximum speed of fine motor control.

Vocal Motor Performance in Birdsong Requires Brain–Body Interaction

“…Most nuclei of the song system are smaller in females (Nixdorf-Bergweiler, 1996; Shaughnessy et al, 2019), females have a smaller motor nucleus projecting to the syrinx (Godsave et al, 2002; Wade et al, 2002), the syrinx itself is also smaller with a less developed skeleton (Düring et al, 2013), and syringeal muscles have less mass (Bleisch et al, 1984; Wade and Buhlman, 2000; Düring et al, 2013) and a lower contraction speed (Elemans et al, 2008), albeit still nearly two orders of magnitude faster than locomotory muscles. Moreover, syrinx muscles in females express less MYH13 than in males (Mead et al, 2017). The sexual dimorphic nature of these observations suggests that these traits are mediated by gonadal steroid hormones.…”

“…Because contractile muscle properties determine the forces that act on body and environment, they are critical traits for understanding the biomechanics of vocal production and thereby linking motor commands to behavioral output, i.e., song. It has recently been shown that over song learning, the superfast syringeal muscles controlling song double in isometric contraction speed and ultimately reach the maximal attainable speed possible in vertebrate synchronous muscle (Mead et al, 2017). The muscle speed increase was associated with a composition change of expressed heavy myosin chain gene isoforms ( MYH ) toward near-exclusive expression of MYH13 aka superfast myosin (Mead et al, 2017).…”

“…It has recently been shown that over song learning, the superfast syringeal muscles controlling song double in isometric contraction speed and ultimately reach the maximal attainable speed possible in vertebrate synchronous muscle (Mead et al, 2017). The muscle speed increase was associated with a composition change of expressed heavy myosin chain gene isoforms ( MYH ) toward near-exclusive expression of MYH13 aka superfast myosin (Mead et al, 2017). Concluding, over vocal development syringeal muscles exhibit changes in morphology as well as contractile properties.…”

Woodpecker drumming behavior is linked to the elevated expression of genes that encode calcium handling proteins in the neck musculature

“…Zhang et al, 1993). Other genes that encode essential proteins for muscle function may similarly evolve to support LC speed, including a variety of myosin and/or troponin isoforms (Mead et al, 2017;Tikunov et al, 2001).…”

Parasitic gut infection causes functional and molecular resemblance of Libellula pulchella dragonfly flight muscle to skeletal muscle of obese vertebrates

“…Sacktor 1975 in Candy and Kilby, 1975;Gilmour 1965), flight motor designs that are optimized for high mechanical performance and energy catabolism, will need equally fine-tuned, homeostatic interactions with digestive, energy anabolic and nutrient mobilization physiology. In a fashion similar to how a high-performance race car differs from a mini-van (Marden et al, 1999;Mead et al, 2017), flying insects may have lower built-in safety factors that protect against disturbances of these homeostatic interactions than non-flying insects, and show more pronounced effects of infections. Studies of the effects of parasitic infections on insect flight performance traits have focused mainly on mosquitos and honeybees (e.g.…”