Fundamental constraints in synchronous muscle limit superfast motor control in vertebrates

Mead, Andrew; Osinalde, Nerea; Ørtenblad, Niels; Nielsen, Joachim; Brewer, Jonathan R.; Vellema, Michael; Adam, Iris; Scharff, Constance; Song, Yafeng; Blagoev, Blagoy; Kratchmarova, Irina; Elemans, Coen P. H.

doi:10.1101/135343

Cited by 14 publications

(26 citation statements)

References 68 publications

(136 reference statements)

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“…We further compared expression of the three fast-twitch fiber myosin heavy chains (Myh1/2/4) that differ in their fiber shortening velocity, which decreases in the order: Myh4 > Myh1 > Myh2 [29]. We found that Myh4 makes up 90% of the myosin heavy chain expression in the anterior cricothyroid muscle, consistent with the need for fast contraction and consistent with a recent study [42]. In contrast, Myh4 has the lowest expression in breast muscle, where the expression order of Myh4 > Myh2 > Myh1 observed in the anterior cricothyroid muscle is reversed.…”

Section: Resultssupporting

confidence: 88%

Molecular parallelism in fast-twitch muscle proteins in echolocating mammals

Lee

Lewis

Moural

et al. 2018

Preprint

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Detecting associations between genomic changes and phenotypic differences is fundamental to understanding how phenotypes evolved. By developing a method to systematically screen for parallel amino acid substitutions, we discovered that echolocating bats and dolphins exhibit more parallel substitutions than expected in fast-twitch but in not slow-twitch muscle fiber proteins. Both bats and dolphins rely on specialized superfast muscles to produce an extremely rapid call rate when homing in on their prey. We show that these genes with parallel substitutions are expressed in the superfast call-producing muscle of bats and demonstrate that the calcium storage protein calsequestrin 1 of bats and dolphins form calcium-sequestering polymers at lower calcium concentrations, consistent with adaptations to rapid calcium transients required for superfast muscle physiology. Our results provide molecular insights into the convergent evolution of vocalization in echolocating mammals and demonstrate the potential of systematic screens to uncover associations between genomic changes and phenotypic differences.

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Section: Resultssupporting

confidence: 88%

Molecular parallelism in fast-twitch muscle proteins in echolocating mammals

Lee

Lewis

Moural

et al. 2018

Preprint

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“…These larval myotomal muscles in certain ways resemble the ‘superfast’ vertebrate muscles, found exclusively in sound-producing organ systems, which work at cycling frequencies between 100 and 200 Hz (27, 46-48). The physiologic adaptations that enable superfast muscle to cycle at such high frequencies come at the expense of force production.…”

Section: Discussionmentioning

confidence: 99%

Mechanical characteristics of ultrafast zebrafish larval swimming muscles

Mead

Kennedy

Palmer

et al. 2020

Preprint

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13Zebrafish (Danio rerio) swim within days of fertilization, powered by muscles of the axial myotomes. 14 Forces generated by these muscles can be measured rapidly in whole, intact larval tails by adapting 15 protocols developed for ex vivo muscle mechanics. But it is not known how well these measurements 16 reflect the function of the underlying muscle fibers and sarcomeres. Here we consider the anatomy of 17 the 5-day-old, wild-type larval tail, and implement technical modifications to measuring muscle 18 physiology in intact tails. Specifically, we quantify fundamental relationships between force, length, and 19 shortening velocity, and capture the extreme contractile speeds required to swim with tail-beat 20 frequencies of 80-100 Hz. Therefore, we analyze 1000 frames/second movies to track the movement of 21 structures, visible in the transparent tail, which correlate with sarcomere length. We also characterize 22 the passive viscoelastic properties of the preparation to isolate forces contributed by non-muscle 23 structures within the tail. Myotomal muscles generate more than 95% of their maximum isometric 24 stress (76±3 mN/mm 2 ) over the range of muscle lengths used in vivo. They have rapid twitch kinetics 25 (full width at half-maximum stress: 11±1 msec) and a high twitch to tetanus ratio (0.91±0.05), indicating 26 adaptations for fast excitation-contraction coupling. Although contractile stress is relatively low, 27 myotomal muscles develop high net power (134±20 W/kg at 80 Hz) in cyclical work loop experiments 28 designed to simulate the in vivo dynamics of muscle fibers during swimming. When shortening at a 29 constant speed of 7±1 muscle lengths/second, muscles develop 86±2% of isometric stress, while peak 30 instantaneous power during 100Hz work loops occurs at 18±2 muscle lengths/second. These approaches 31 can improve the usefulness of zebrafish as a model system for muscle research by providing a rapid and 32 sensitive functional readout for experimental interventions. 34Statement of significance 36The zebrafish (Danio rerio) may prove a uniquely efficient model system for characterizing vertebrate 37 muscle physiology. Transparent, drug-permeable larva -each, in essence, a fully functional muscle -can 38 be generated rapidly, inexpensively, and in large numbers. Critically, the zebrafish genome contains 39 homologs of major muscle genes and is highly amenable to manipulation. To reach its potential, reliable 40 (and preferably rapid) means are needed to observe the effects of experimental interventions on larval 41 muscle function. In the present study we show how mechanical measurements made on whole, intact 42 larval tails can provide a readout of fundamental muscle-mechanical properties. Additionally, we show 43 that these muscles are among the fastest ever measured, and therefore worthy of study in their own 44 right.45 82 contractile conditions, using a modified work loop approach. Our results suggest that the tail muscle 83 fibers generate their maximum force at the in vivo resting length ...

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“…Stress ranges from the peak stress during the all-or-none twitch contraction (Ptw) caused by a single motor neuron spike, up to the maximum stress 130 during tetanic contraction (Po) caused by spike trains of the motor neuron. Because syringeal muscles are superfast muscles that can power movement up to 200 -250 Hz [26], they trade force for speed as a fundamental architectural trait [27,28] and are expected to have low Po. Indeed, pigeon syringeal muscles generate a Po as low as 18 -50 mN/mm 2 [29], 5 -10 times lower as regular skeletal muscle fibers (~150 -300 mN/mm 2 ) [30, 31] ( Fig 135 2), but the Po of songbird syringeal muscles is unknown.…”

Section: Songbird Syringeal Muscles Generate the Lowest Stressmentioning

confidence: 99%

“…From a motor control perspective, this suggests a strong selection for small force steps, which can be achieved by small MU sizes combined with low specific force. As a result of the selection on muscle speed, muscle specific force reduces significantly due to architectural constraints of skeletal muscles [27]. Thus, if the force per 215…”

Section: Behavioral Selection On Resolution Drove Small Mus 205mentioning

confidence: 99%

“…MU innervation numbers below 10 are on the extremely low end of MU sizes in 220 vertebrates, and have so far only been reported for laryngeal [19,47], extraocular [20,24] and ear muscles [25]. Interestingly, all those muscles belong to the craniofacial lineage [27] suggesting that their developmental origin might predispose them or even provide unique access to low MU sizes. Thus, developmental origin may in part explain the ability to achieve fine force gradation through small MUs.…”

Section: Behavioral Selection On Resolution Drove Small Mus 205mentioning

confidence: 99%

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One-to-one innervation of vocal muscles allows precise control of birdsong

Adam

Maxwell

Rößler

et al. 2020

Preprint

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15SummaryThe motor control resolution of any animal behavior is limited to the minimal force step available when activating muscles, which is set by the number and size distribution of motor units (MUs) and muscle specific force [1,2]. Birdsong is an excellent model system for understanding sequence learning of complex fine motor skills [3], but we know surprisingly 20 little how the motor pool controlling the syrinx is organized [4] and how MU recruitment drives changes in vocal output [5]. Here we combine measurements of syringeal muscle innervation ratios with muscle stress and an in vitro syrinx preparation to estimate MU size distribution and the control resolution of fundamental frequency (fo), a key vocal parameter, in zebra finches. We show that syringeal muscles have extremely small MUs, with 50% 25innervating ≤ 3, and 13 -17% innervating a single muscle fiber. Combined with the lowest specific stress (5 mN/mm 2 ) known to skeletal vertebrate muscle, small force steps by the major fo controlling muscle provide control of 50 mHz to 4.2 Hz steps per MU. We show that the song system has the highest motor control resolution possible in the vertebrate nervous system and suggest this evolved due to strong selection on fine gradation of vocal output. 30Furthermore, we propose that high-resolution motor control was a key feature contributing to the radiation of songbirds that allowed diversification of song and speciation by vocal space expansion. Results & DiscussionVocal communication is of paramount importance for reproduction and survival of songbirds and even drives speciation. This is clearly exemplified by sympatric species that are 40 morphologically indistinguishable, but nevertheless fully separated solely by song [6, 7]. The potential to acoustically separate depends on the number of distinct sounds -or vocal space -that can be produced and perceived. The vocal space is set both by the range available to vary an acoustic feature, and in what steps, or resolution, the feature can be controlled within this range. Thus, both resolution and range expand the vocal space and may form a rich 45 substrate for species diversification [8,9]. While the range of an acoustic feature, for example fo, is typically limited by intrinsic constraints of the vocal organ [10-12], the ability 65 ( Fig 1A, B, Table S1, See Methods). The average total number of muscle fibers was 6995 ± 789 (n = 4), corroborating earlier reported ~6730 [17]. The left side had significantly less muscle fibers (3234 ± 232, range: 2992 -3503, n = 4) than right (3794 ± 334, range 3586 -4286, n = 4) (Welch t-test: t = -2.8, df = 5.4, p-value = 0.04). The number of axons in the tracheosyringeal branch of the hypoglossal nerve (NXIIts), assumed to represent the 70 number of MUs (See Methods), was not significantly different between left (820 ± 187, range: 602 -1162, n = 8) and right (790 ± 148, range: 677 -1045, n = 5) (Welch t-test: t = 0.32, df = 10.2, p-value = 0.76) and lower but within range of the 1026 ± 126 (n = 6) reported earlier [18]. The ...

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Fundamental constraints in synchronous muscle limit superfast motor control in vertebrates

Cited by 14 publications

References 68 publications

Molecular parallelism in fast-twitch muscle proteins in echolocating mammals

Molecular parallelism in fast-twitch muscle proteins in echolocating mammals

Mechanical characteristics of ultrafast zebrafish larval swimming muscles

One-to-one innervation of vocal muscles allows precise control of birdsong

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