Fundamental constraints in synchronous muscle limit superfast motor control in vertebrates

Andrew F Mead, Nerea Osinalde, Niels Ørtenblad, Joachim Nielsen, Jonathan Brewer, Michiel Vellema, Iris Adam, Constance Scharff, Yafeng Song, Ulrik Frandsen, Blagoy Blagoev, Irina Kratchmarova, Coen Ph Elemans

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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.

Original languageEnglish
Article numbere29425
JournaleLife
Volume6
Number of pages20
ISSN2050-084X
DOIs
Publication statusPublished - 2017

Keywords

  • Journal Article

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