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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Resumé

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.

OriginalsprogEngelsk
Artikelnummere29425
TidsskrifteLife
Vol/bind6
Antal sider20
ISSN2050-084X
DOI
StatusUdgivet - 2017

Fingeraftryk

Muscle
Vertebrates
Muscles
Skates (Fish)
Actomyosin
Myosin Heavy Chains
Mammals
Birds
Fish
Genes
Acoustic waves
Kinetics

Citer dette

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title = "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.",
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author = "Mead, {Andrew F} and Nerea Osinalde and Niels {\O}rtenblad and Joachim Nielsen and Jonathan Brewer and Michiel Vellema and Iris Adam and Constance Scharff and Yafeng Song and Ulrik Frandsen and Blagoy Blagoev and Irina Kratchmarova and Elemans, {Coen Ph}",
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Fundamental constraints in synchronous muscle limit superfast motor control in vertebrates. / Mead, Andrew F; Osinalde, Nerea; Ørtenblad, Niels; Nielsen, Joachim; Brewer, Jonathan; Vellema, Michiel; Adam, Iris; Scharff, Constance; Song, Yafeng; Frandsen, Ulrik; Blagoev, Blagoy; Kratchmarova, Irina; Elemans, Coen Ph.

I: eLife, Bind 6, e29425, 2017.

Publikation: Bidrag til tidsskriftTidsskriftartikelForskningpeer review

TY - JOUR

T1 - Fundamental constraints in synchronous muscle limit superfast motor control in vertebrates

AU - Mead, Andrew F

AU - Osinalde, Nerea

AU - Ørtenblad, Niels

AU - Nielsen, Joachim

AU - Brewer, Jonathan

AU - Vellema, Michiel

AU - Adam, Iris

AU - Scharff, Constance

AU - Song, Yafeng

AU - Frandsen, Ulrik

AU - Blagoev, Blagoy

AU - Kratchmarova, Irina

AU - Elemans, Coen Ph

PY - 2017

Y1 - 2017

N2 - 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.

AB - 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.

KW - Journal Article

U2 - 10.7554/eLife.29425

DO - 10.7554/eLife.29425

M3 - Journal article

C2 - 29165242

VL - 6

JO - eLife

JF - eLife

SN - 2050-084X

M1 - e29425

ER -