Shortening deactivation: quantifying a critical component of cyclical muscle contraction

2021 ◽  
Author(s):  
Amy K. Loya ◽  
Sarah K. Van Houten ◽  
Bernadette M. Glasheen ◽  
Douglas M. Swank
Keyword(s):  
Power Output ◽  
Muscle Activation ◽  
Muscle Relaxation ◽  
Length Change ◽  
Isometric Tension ◽  
Energetic Cost ◽  
Muscle Shortening ◽  
Shortening Deactivation ◽  
Muscle Types ◽  
Flight Muscles

A muscle undergoing cyclical contractions requires fast and efficient muscle activation and relaxation to generate high power with relatively low energetic cost. To enhance activation and increase force levels during shortening, some muscle types have evolved stretch activation (SA), a delayed increased in force following rapid muscle lengthening. SA's complementary phenomenon is shortening deactivation (SD), a delayed decrease in force following muscle shortening. SD increases muscle relaxation, which decreases resistance to subsequent muscle lengthening. While it might be just as important to cyclical power output, SD has received less investigation than SA. To enable mechanistic investigations into SD and quantitatively compare it to SA, we developed a protocol to elicit SA and SD from Drosophila and Lethocerus indirect flight muscles (IFM) and Drosophila jump muscle. When normalized to isometric tension, Drosophila IFM exhibited a 118% SD tension decrease, Lethocerus IFM dropped by 97%, and Drosophila jump muscle decreased by 37%. The same order was found for normalized SA tension: Drosophila IFM increased by 233%, Lethocerus IFM by 76%, and Drosophila jump muscle by only 11%. SD occurred slightly earlier than SA, relative to the respective length change, for both IFMs; but SD was exceedingly earlier than SA for jump muscle. Our results suggest SA and SD evolved to enable highly efficient IFM cyclical power generation and may be caused by the same mechanism. However, jump muscle SA and SD mechanisms are likely different, and may have evolved for a role other than to increase the power output of cyclical contractions.

Use of a new index to study relaxation in a vascular model of anaphylactic shock

1993 ◽  
Vol 74 (6) ◽  
pp. 2621-2626 ◽  
Author(s):  
X. Liu ◽  
H. Jiang ◽  
N. L. Stephens
Keyword(s):  
Saphenous Vein ◽  
Anaphylactic Shock ◽  
Muscle Activation ◽  
Muscle Relaxation ◽  
Contractile Element ◽  
Time Index ◽  
Muscle Shortening ◽  
Cross Bridges ◽  
And Control ◽  
Relaxation Index

We have reported increased smooth muscle shortening ability in ragweed pollen-sensitized saphenous vein (SSV). This may account for the vascular hyperreactivity of anaphylactic shock. We have now investigated relaxation in SSV. Because isotonic relaxation is load and initial contractile element length dependent, we developed an adjusted half-relaxation time index, which was independent of these variables. Muscle activation state was monitored by measuring maximum unloaded velocity. The relaxation index showed no difference between SSV and control saphenous vein after 2.5, 10, and 15 s of electrical stimulation; however, after 1 s of stimulation it was prolonged significantly in SSV. We concluded that the cross bridges activating early in contraction demonstrated prolonged relaxation. Activation state during muscle relaxation spontaneously increased toward the end of relaxation, coincident with a slowing in isotonic re-elongation rate. This was seen only in muscles relaxing from 15 s of stimulation. Our results indicate that 1) the relaxation properties of early cycling (1 s) cross bridges are altered after sensitization; and 2) toward the end of isotonic relaxation, cross-bridge cycling rate increases spontaneously, a phenomenon not previously reported. We speculate that the rapid re-elongation in late relaxation may reactivate muscle.

The influence of temperature on power production during swimming. I. In vivo length change and stimulation pattern

2000 ◽  
Vol 203 (2) ◽  
pp. 321-331 ◽  
Author(s):  
D.M. Swank ◽  
L.C. Rome
Keyword(s):  
Power Generation ◽  
Low Temperature ◽  
Power Output ◽  
Low Temperatures ◽  
Muscle Relaxation ◽  
Length Change ◽  
Significant Finding ◽  
Red Muscle ◽  
Effects Of Temperature

Ectothermal animals are able to locomote effectively over a wide range of temperatures despite low temperature reducing the power output of their muscles. It has been suggested that animals recruit more muscle fibres and faster fibre types to compensate for the reduced power output at low temperature, but it is not known how much low temperature actually reduces power output in vivo. ‘Optimized’ work-loop measurements, which are thought to approximate muscle function in vivo, give a Q(10) of approximately 2.3 for power output of scup (Stenotomus chrysops) red muscle between 10 degrees C and 20 degrees C. However, because of the slower muscle relaxation rate at low temperatures, ‘optimizing’ work loops requires stimulation duration to be reduced and oscillation frequency to be decreased to obtain maximal power output. Previous fish swimming experiments suggest that similar optimization may not occur in vivo, and this may have substantial consequences in terms of muscle power generation and swimming at low temperatures. To assess more precisely the effects of temperature on muscle performance and swimming, in the present study, we measured the length change, stimulation duration and stimulus phase of red muscle at various positions along scup swimming at several speeds at 10 degrees C and 20 degrees C. In a companion study, we determined the effects of temperature on in vivo power generation by driving muscle fibre bundles through these in vivo length changes and stimulation conditions, and measuring the resulting power output. The most significant finding from the present study is that, despite large differences in the in vivo parameters along the length of the fish (a decrease in stimulus duration, an increase in strain and a negative shift in phase) moving posteriorly, these parameters do not change with temperature. Thus, although the nervous system of fish could, in theory, compensate for slow muscle relaxation by greatly reducing muscle stimulation duration at low temperatures, it does not. This lack of compensation to low temperatures might reflect a potential limitation in neural control.

In vivo pectoralis muscle force-length behavior during level flight in pigeons (Columba livia)

1998 ◽  
Vol 201 (24) ◽  
pp. 3293-3307 ◽  
Author(s):  
A. A. Biewener ◽  
W. R. Corning ◽  
B. W. Tobalske
Keyword(s):  
Power Output ◽  
Muscle Length ◽  
Columba Livia ◽  
Length Change ◽  
Pectoralis Muscle ◽  
Fascicle Length ◽  
Force Development ◽  
Mechanical Power Output ◽  
Muscle Shortening

For the first time, we report in vivo measurements of pectoralis muscle length change obtained using sonomicrometry combined with measurements of its force development via deltopectoral crest strain recordings of a bird in free flight. These measurements allow us to characterize the contractile behavior and mechanical power output of the pectoralis under dynamic conditions of slow level flight in pigeons Columba livia. Our recordings confirm that the pigeon pectoralis generates in vivo work loops that begin with the rapid development of force as the muscle is being stretched or remains nearly isometric near the end of the upstroke. The pectoralis then shortens by a total of 32 % of its resting length during the downstroke,generating an average of 10.33.6 J kg-1 muscle (mean s.d.) of work per cycle for the anterior and posterior sites recorded among the five animals. In contrast to previous kinematic estimates of muscle length change relative to force development, the sonomicrometry measurements of fascicle length change show that force declines during muscle shortening. Simultaneous measurements of fascicle length change at anterior and posterior sites within the same muscle show significant (P<0.001, three of four animals) differences in fractional length (strain) change that averaged 1912 %, despite exhibiting similar work loop shape. Length changes at both anterior and posterior sites were nearly synchronous and had an asymmetrical pattern, with shortening occupying 63 % of the cycle. This nearly 2:1 phase ratio of shortening to lengthening probably favors the ability of the muscle to do work. Mean muscle shortening velocity was 5.381.33 and 4.881.27 lengths s-1 at the anterior and posterior sites respectively. Length excursions of the muscle were more variable at the end of the downstroke (maximum shortening), particularly when the birds landed,compared with highly uniform length excursions at the end of the upstroke(maximum lengthening). When averaged for the muscle as a whole, our in vivo work measurements yield a mass-specific net mechanical power output of 70. 2 W kg-1 for the muscle when the birds flew at 5-6 m s-1, with a wingbeat frequency of 8.7 Hz. This is 38 % greater than the value that we obtained previously for wild-type pigeons, but still 24-50 % less than that predicted by theory.

scholarly journals Determinants of metabolic cost during submaximal cycling

2002 ◽  
Vol 93 (3) ◽  
pp. 823-828 ◽  
Author(s):  
J. McDaniel ◽  
J. L. Durstine ◽  
G. A. Hand ◽  
J. C. Martin
Keyword(s):  
Power Output ◽  
Muscle Activation ◽  
Metabolic Cost ◽  
Mechanical Power ◽  
Shortening Velocity ◽  
Mechanical Power Output ◽  
Muscle Shortening ◽  
Main Determinants ◽  
Power Outputs ◽  
Pedaling Rate

The metabolic cost of producing submaximal cycling power has been reported to vary with pedaling rate. Pedaling rate, however, governs two physiological phenomena known to influence metabolic cost and efficiency: muscle shortening velocity and the frequency of muscle activation and relaxation. The purpose of this investigation was to determine the relative influence of those two phenomena on metabolic cost during submaximal cycling. Nine trained male cyclists performed submaximal cycling at power outputs intended to elicit 30, 60, and 90% of their individual lactate threshold at four pedaling rates (40, 60, 80, 100 rpm) with three different crank lengths (145, 170, and 195 mm). The combination of four pedaling rates and three crank lengths produced 12 pedal speeds ranging from 0.61 to 2.04 m/s. Metabolic cost was determined by indirect calorimetery, and power output and pedaling rate were recorded. A stepwise multiple linear regression procedure selected mechanical power output, pedal speed, and pedal speed squared as the main determinants of metabolic cost ( R 2 = 0.99 ± 0.01). Neither pedaling rate nor crank length significantly contributed to the regression model. The cost of unloaded cycling and delta efficiency were 150 metabolic watts and 24.7%, respectively, when data from all crank lengths and pedal speeds were included in a regression. Those values increased with increasing pedal speed and ranged from a low of 73 ± 7 metabolic watts and 22.1 ± 0.3% (145-mm cranks, 40 rpm) to a high of 297 ± 23 metabolic watts and 26.6 ± 0.7% (195-mm cranks, 100 rpm). These results suggest that mechanical power output and pedal speed, a marker for muscle shortening velocity, are the main determinants of metabolic cost during submaximal cycling, whereas pedaling rate (i.e., activation-relaxation rate) does not significantly contribute to metabolic cost.

scholarly journals Flightin maintains myofilament lattice organization required for optimal flight power and courtship song quality in Drosophila

2017 ◽  
Vol 284 (1854) ◽  
pp. 20170431 ◽  
Author(s):  
Samya Chakravorty ◽  
Bertrand C. W. Tanner ◽  
Veronica Lee Foelber ◽  
Hien Vu ◽  
Matthew Rosenthal ◽  
...  
Keyword(s):  
Power Output ◽  
Lattice Structure ◽  
Courtship Song ◽  
Fine Tuning ◽  
Male Reproductive Success ◽  
Supporting Evidence ◽  
Force Transmission ◽  
Wingbeat Frequency ◽  
Terminal Domain ◽  
Flight Muscles

The indirect flight muscles (IFMs) of Drosophila and other insects with asynchronous flight muscles are characterized by a crystalline myofilament lattice structure. The high-order lattice regularity is considered an adaptation for enhanced power output, but supporting evidence for this claim is lacking. We show that IFMs from transgenic flies expressing flightin with a deletion of its poorly conserved N-terminal domain ( fln ΔN62 ) have reduced inter-thick filament spacing and a less regular lattice. This resulted in a decrease in flight ability by 33% and in skinned fibre oscillatory power output by 57%, but had no effect on wingbeat frequency or frequency of maximum power output, suggesting that the underlying actomyosin kinetics is not affected and that the flight impairment arises from deficits in force transmission. Moreover, we show that fln ΔN62 males produced an abnormal courtship song characterized by a higher sine song frequency and a pulse song with longer pulses and longer inter-pulse intervals (IPIs), the latter implicated in male reproductive success. When presented with a choice, wild-type females chose control males over mutant males in 92% of the competition events. These results demonstrate that flightin N-terminal domain is required for optimal myofilament lattice regularity and IFM activity, enabling powered flight and courtship song production. As the courtship song is subject to female choice, we propose that the low amino acid sequence conservation of the N-terminal domain reflects its role in fine-tuning species-specific courtship songs.

scholarly journals The Drosophila indirect flight muscle myosin heavy chain isoform is insufficient to transform the jump muscle into a highly stretch-activated muscle type

2017 ◽  
Vol 312 (2) ◽  
pp. C111-C118 ◽  
Author(s):  
Cuiping Zhao ◽  
Douglas M. Swank
Keyword(s):  
Power Generation ◽  
Myosin Heavy Chain ◽  
Heavy Chain ◽  
Flight Muscle ◽  
Fold Increase ◽  
Isometric Tension ◽  
Indirect Flight Muscle ◽  
Muscle Type ◽  
Myosin Heavy Chain Isoform ◽  
Muscle Types

Stretch activation (SA) is a delayed increase in force that enables high power and efficiency from a cyclically contracting muscle. SA exists in various degrees in almost all muscle types. In Drosophila, the indirect flight muscle (IFM) displays exceptionally high SA force production ( FSA), whereas the jump muscle produces only minimal FSA. We previously found that expressing an embryonic (EMB) myosin heavy chain (MHC) isoform in the jump muscle transforms it into a moderately SA muscle type and enables positive cyclical power generation. To investigate whether variation in MHC isoforms is sufficient to produce even higher FSA, we substituted the IFM MHC isoform (IFI) into the jump muscle. Surprisingly, we found that IFI only caused a 1.7-fold increase in FSA, less than half the increase previously observed with EMB, and only at a high Pi concentration, 16 mM. This IFI-induced FSA is much less than what occurs in IFM, relative to isometric tension, and did not enable positive cyclical power generation by the jump muscle. Both isometric tension and FSA of control fibers decreased with increasing Pi concentration. However, for IFI-expressing fibers, only isometric tension decreased. The rate of FSA generation was ~1.5-fold faster for IFI fibers than control fibers, and both rates were Pi dependent. We conclude that MHC isoforms can alter FSA and hence cyclical power generation but that isoforms can only endow a muscle type with moderate FSA. Highly SA muscle types, such as IFM, likely use a different or additional mechanism.

Climbing Performance of Harris' Hawks (Parabuteo Unicinctus) with Added Load: Implications for Muscle Mechanics and for Radiotracking

1989 ◽  
Vol 142 (1) ◽  
pp. 17-29 ◽  
Author(s):  
C. J. PENNYCUICK ◽  
M. R. FULLER ◽  
LYNNE McALLISTER
Keyword(s):  
Body Mass ◽  
Power Output ◽  
Muscle Power ◽  
Muscle Mechanics ◽  
The Body ◽  
Power Product ◽  
Horizontal Flight ◽  
Flight Muscles ◽  
Food Load ◽  
Parabuteo Unicinctus

Two Harris' hawks were trained to fly along horizontal and climbing flight paths, while carrying loads of various masses, to provide data for estimating available muscle power during short flights. The body mass of both hawks was about 920 g, and they were able to carry loads up to 630 g in horizontal flight. The rate of climb decreased with increasing all-up mass, as also did the climbing power (product of weight and rate of climb). Various assumptions about the aerodynamic power in low-speed climbs led to estimates of the maximum power output of the flight muscles ranging from 41 to 46 W. This, in turn, would imply a stress during shortening of around 210 kPa. The effects of a radio package on a bird that is raising young should be considered in relation to the food load that the forager can normally carry, rather than in relation to its body mass.

Relationship between Shear Wave Velocity and Muscle Activation is Inconsistent Across Different Muscle Types

2021 ◽  
Author(s):  
Michel Bernabei ◽  
Daniel Ludvig ◽  
Thomas G. Sandercock ◽  
Eric J. Perreault ◽  
Sabrina SM Lee
Keyword(s):  
Shear Wave ◽  
Wave Velocity ◽  
Shear Wave Velocity ◽  
Muscle Activation ◽  
Muscle Types

Asynchronous muscle: a primer

2000 ◽  
Vol 203 (18) ◽  
pp. 2713-2722 ◽  
Author(s):  
R.K. Josephson ◽  
J.G. Malamud ◽  
D.R. Stokes
Keyword(s):  
Time Course ◽  
Flight Muscle ◽  
Isometric Force ◽  
Length Change ◽  
Mechanical Activity ◽  
Stretch Activation ◽  
Passive Stiffness ◽  
Schistocerca Americana ◽  
Slow Time ◽  
Shortening Deactivation

The asynchronous muscles of insects are characterized by asynchrony between muscle electrical and mechanical activity, a fibrillar organization with poorly developed sarcoplasmic reticulum, a slow time course of isometric contraction, low isometric force, high passive stiffness and delayed stretch activation and shortening deactivation. These properties are illustrated by comparing an asynchronous muscle, the basalar flight muscle of the beetle Cotinus mutabilis, with synchronous wing muscles from the locust, Schistocerca americana. Because of delayed stretch activation and shortening deactivation, a tetanically stimulated beetle muscle can do work when subjected to repetitive lengthening and shortening. The synchronous locust muscle, subjected to similar stimulation and length change, absorbs rather than produces work.

In vivo loads on airway smooth muscle: the role of noncontractile airway structures

1992 ◽  
Vol 70 (4) ◽  
pp. 602-606 ◽  
Author(s):  
Philip Robinson ◽  
Mitsushi Okazawa ◽  
Tony Bai ◽  
Peter Paré
Keyword(s):  
Smooth Muscle ◽  
Airway Smooth Muscle ◽  
Muscle Activation ◽  
Muscle Length ◽  
Tracheal Cartilage ◽  
Elastic Load ◽  
Muscle Shortening ◽  
Trachealis Muscle

The degree of airway smooth muscle contraction and shortening that occurs in vivo is modified by many factors, including those that influence the degree of muscle activation, the resting muscle length, and the loads against which the muscle contracts. Canine trachealis muscle will shorten up to 70% of starting length from optimal length in vitro but will only shorten by around 30% in vivo. This limitation of shortening may be a result of the muscle shortening against an elastic load such as could be applied by tracheal cartilage. Limitation of airway smooth muscle shortening in smaller airways may be the result of contraction against an elastic load, such as could be applied by lung parenchymal recoil. Measurement of the elastic loads applied by the tracheal cartilage to the trachealis muscle and by lung parenchymal recoil to smooth muscle of smaller airways were performed in canine preparations. In both experiments the calculated elastic loads applied by the cartilage and the parenchymal recoil explained in part the limitation of maximal active shortening and airway narrowing observed. We conclude that the elastic loads provided by surrounding structures are important in determining the degree of airway smooth muscle shortening and the resultant airway narrowing.Key words: elastic loads, tracheal cartilage, airway smooth muscle shortening.

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