RT Journal Article
SR Electronic
T1 Fundamental constraints in synchronous muscle limit superfast motor control in vertebrates
JF bioRxiv
FD Cold Spring Harbor Laboratory
SP 135343
DO 10.1101/135343
A1 AF Mead
A1 N. Osinalde
A1 N. Ørtenblad
A1 J. Nielsen
A1 J. Brewer
A1 M. Vellema
A1 I. Adam
A1 C. Scharff
A1 Y. Song
A1 U. Frandsen
A1 B. Blagoev
A1 I. Kratchmarova
A1 CPH Elemans
YR 2017
UL http://biorxiv.org/content/early/2017/06/06/135343.abstract
AB Superfast muscles (SFM) are extremely fast synchronous muscles capable of contraction rates up to 250 Hz, enabling precise motor execution at the millisecond time scale. To allow such speed, the archetypal SFM, found in the toadfish swimbladder, has hallmark structural and kinetic adaptations at each step of the conserved excitation-contraction coupling (ECC) pathway. More recently SFM phenotypes have been discovered in most major vertebrate lineages, but it remains unknown whether all SFM share ECC adaptations for speed, and if SFM arose once, or from independent evolutionary events. Here we use genomic analysis to identify the myosin heavy chain genes expressed in bat and songbird SFM to achieve rapid actomyosin crossbridge kinetics and demonstrate that these are evolutionarily and ontologically distinct. Furthermore, by quantifying cellular morphometry and calcium signal transduction combined with force measurements we show that all known SFM share multiple functional adaptations that minimize ECC 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.