PECTORALIS MUSCLE FORCE AND POWER OUTPUT DURING FLIGHT IN THE STARLING

1992 ◽  
Vol 164 (1) ◽  
pp. 1-18 ◽  
Author(s):  
ANDREW A. BIEWENER ◽  
KENNETH P. DIAL ◽  
G. E. GOSLOW

Force recordings of the pectoralis muscle of European starlings have been made in vivo during level flight in a wind tunnel, based on bone strain recordings at the muscle's attachment site on the humerus (deltopectoral crest). This represents the first direct measurement of muscle force during activity in a live animal based on calibrated bone strain recordings. Our force measurements confirm earlier electromyographic data and show that the pectoralis begins to develop force during the final one-third of the upstroke, reaches a maximal level halfway through the downstroke, and sustains force throughout the downstroke. Peak forces generated by the pectoralis during level flight at a speed estimated to be 13.7ms−1 averaged 6.4N (28% of maximal isometric force), generating a mean mass-specific muscle power output of 104 W kg−1. Combining our data for the power output of the pectoralis muscle with data for the metabolic power of starlings flying at a similar speed yields an overall flight efficiency of 13 %. The force recordings and length changes of the muscle, based on angular displacements of the humerus, indicate that the pectoralis muscle undergoes a lengthening--shortening contraction sequence during its activation and that, in addition to lift and thrust generation, overcoming wing inertia is probably an important function of this muscle in flapping flight.

1993 ◽  
Vol 176 (1) ◽  
pp. 31-54 ◽  
Author(s):  
K. P. Dial ◽  
A. A. Biewener

In vivo measurements of pectoralis muscle force during different modes of free flight (takeoff, level flapping, landing, vertical ascending and near vertical descending flight) were obtained using a strain gauge attached to the dorsal surface of the delto-pectoral crest (DPC) of the humerus in four trained pigeons (Columba livia). In one bird, a rosette strain gauge was attached to the DPC to determine the principal axis of strain produced by tension of the pectoralis. Strain signals recorded during flight were calibrated to force based on in situ measurements of tetanic force and on direct tension applied to the muscle's insertion at the DPC. Rosette strain recordings showed that at maximal force the orientation of tensile principal strain was −15° (proximo-anterior) to the perpendicular axis of the DPC (or +75° to the longitudinal axis of the humerus), ranging from +15 to −25° to the DPC axis during the downstroke. The consistency of tensile principal strain orientation in the DPC confirms the more general use of single-element strain gauges as being a reliable method for determining in vivo pectoralis force generation. Our strain recordings show that the pectoralis begins to develop force as it is being lengthened, during the final one-third of the upstroke, and attains maximum force output while shortening during the first one-third of the downstroke. Force is sustained throughout the entire downstroke, even after the onset of the upstroke for certain flight conditions. Mean peak forces developed by the pectoralis based on measurements from 40 wingbeats for each bird (160 total) were: 24.9+/−3.1 N during takeoff, 19.7+/−2.0 N during level flight (at speeds of about 6–9 m s-1 and a wingbeat frequency of 8.6+/−0.3 Hz), 18.7+/−2.5 N during landing, 23.7+/−2.7 N during near-vertical descent, and 26.0+/−1.8 N during vertical ascending flight. These forces are considerably lower than the maximum isometric force (67 N, P0) of the muscle, ranging from 28 % (landing) to 39 % (vertical ascending) of P0. Based on estimates of muscle fiber length change determined from high- speed (200 frames s-1) light cine films taken of the animals, we calculate the mass-specific power output of the pigeon pectoralis to be 51 W kg-1 during level flight (approximately 8 m s-1), and 119 W kg-1 during takeoff from the ground. When the birds were harnessed with weighted backpacks (50 % and 100 % of body weight), the forces generated by the pectoralis did not significantly exceed those observed in unloaded birds executing vertical ascending flight. These data suggest that the range of force production by the pectoralis under these differing conditions is constrained by the force- velocity properties of the muscle operating at fairly rapid rates of shortening (4.4 fiber lengths s-1 during level flight and 6.7 fiber lengths s-1 during takeoff).


1983 ◽  
Vol 55 (3) ◽  
pp. 759-769 ◽  
Author(s):  
S. J. Gunst

Strips of tonically contracted canine tracheal and bronchial airway smooth muscles (AWSM) were studied in vitro to compare dynamic muscle force during stretch-retraction cycles with static isometric muscle force at various length points within the cycling range. At any particular rate, a characteristic force-length loop was obtained by cycling over a given range of lengths. Dynamic muscle force dropped well below static isometric muscle force at lengths short of the peak length at all rates of cycling. When stretch or retraction of the muscle was stopped at any point along either path of the cycle, muscle force rose to approach the isometric force at that length. Dynamic force at the peak length of the cycle remained close to, or slightly greater than, the static isometric force. The results suggest that the velocity of shortening of tonically contracted AWSM is very slow relative to the rates of cycling employed. A slow rate of shortening of AWSM relative to the rate of change in airway caliber during breathing could account for well-known effects of volume history on airway tone.


2021 ◽  
Vol 12 ◽  
Author(s):  
Anthony L. Hessel ◽  
Jenna A. Monroy ◽  
Kiisa C. Nishikawa

The sliding filament–swinging cross bridge theory of skeletal muscle contraction provides a reasonable description of muscle properties during isometric contractions at or near maximum isometric force. However, it fails to predict muscle force during dynamic length changes, implying that the model is not complete. Mounting evidence suggests that, along with cross bridges, a Ca2+-sensitive viscoelastic element, likely the titin protein, contributes to muscle force and work. The purpose of this study was to develop a multi-level approach deploying stretch-shortening cycles (SSCs) to test the hypothesis that, along with cross bridges, Ca2+-sensitive viscoelastic elements in sarcomeres contribute to force and work. Using whole soleus muscles from wild type and mdm mice, which carry a small deletion in the N2A region of titin, we measured the activation- and phase-dependence of enhanced force and work during SSCs with and without doublet stimuli. In wild type muscles, a doublet stimulus led to an increase in peak force and work per cycle, with the largest effects occurring for stimulation during the lengthening phase of SSCs. In contrast, mdm muscles showed neither doublet potentiation features, nor phase-dependence of activation. To further distinguish the contributions of cross bridge and non-cross bridge elements, we performed SSCs on permeabilized psoas fiber bundles activated to different levels using either [Ca2+] or [Ca2+] plus the myosin inhibitor 2,3-butanedione monoxime (BDM). Across activation levels ranging from 15 to 100% of maximum isometric force, peak force, and work per cycle were enhanced for fibers in [Ca2+] plus BDM compared to [Ca2+] alone at a corresponding activation level, suggesting a contribution from Ca2+-sensitive, non-cross bridge, viscoelastic elements. Taken together, our results suggest that a tunable viscoelastic element such as titin contributes to: (1) persistence of force at low [Ca2+] in doublet potentiation; (2) phase- and length-dependence of doublet potentiation observed in wild type muscles and the absence of these effects in mdm muscles; and (3) increased peak force and work per cycle in SSCs. We conclude that non-cross bridge viscoelastic elements, likely titin, contribute substantially to muscle force and work, as well as the phase-dependence of these quantities, during dynamic length changes.


1990 ◽  
Vol 148 (1) ◽  
pp. 395-402 ◽  
Author(s):  
JOHN D. ALTRINGHAM ◽  
IAN A. JOHNSTON

Intact, electrically excitable fibre bundles were isolated from the fast and slow myotomal muscle of the bullrout (Myoxocephalus scorpius L.). Power output was measured under conditions simulating their activity in a fish swimming at different speeds. Preparations were subjected to sinusoidal length changes of ±5% of resting length, and stimulated briefly during each cycle. The number and timing of stimuli were adjusted at each cycle frequency to maximise power output. Maximum power was produced at 5–7 Hz for fast fibres (25–35 W kg−1) and 2 Hz for slow fibres (5–8 Wkg−1). Under these conditions, pre-stretch of active muscle provides an important mechanism for storing potential energy for release during the shortening part of the cycle.


2001 ◽  
Vol 204 (3) ◽  
pp. 495-507 ◽  
Author(s):  
M.R. Williamson ◽  
K.P. Dial ◽  
A.A. Biewener

In vivo measurements of pectoralis muscle length change and force production were obtained using sonomicrometry and delto-pectoral bone strain recordings during ascending and slow level flight in mallards (Anas platyrhynchos). These measurements provide a description of the force/length properties of the pectoralis under dynamic conditions during two discrete flight behaviors and allow an examination of the effects of differences in body size and morphology on pectoralis performance by comparing the results with those of a recent similar study of slow level flight in pigeons (Columbia livia). In the present study, the mallard pectoralis showed a distinct pattern of active lengthening during the upstroke. This probably enhances the rate of force generation and the magnitude of the force generated and, thus, the amount of work and power produced during the downstroke. The power output of the pectoralis averaged 17.0 W kg(−)(1)body mass (131 W kg(−)(1)muscle mass) during slow level flight (3 m s(−)(1)) and 23.3 W kg(−)(1)body mass (174 W kg(−)(1)muscle mass) during ascending flight. This increase in power was achieved principally via an increase in muscle strain (29 % versus 36 %), rather than an increase in peak force (107 N versus 113 N) or cycle frequency (8.4 Hz versus 8.9 Hz). Body-mass-specific power output of mallards during slow level flight (17.0 W kg(−)(1)), measured in terms of pectoralis mechanical power, was similar to that measured recently in pigeons (16.1 W kg(−)(1)). Mallards compensate for their greater body mass and proportionately smaller wing area and pectoralis muscle volume by operating with a high myofibrillar stress to elevate mechanical power output.


1997 ◽  
Vol 200 (22) ◽  
pp. 2861-2870 ◽  
Author(s):  
M M Peplowski ◽  
R L Marsh

It has been suggested that small frogs use a catapult mechanism to amplify muscle power production during the takeoff phase of jumping. This conclusion was based on an apparent discrepancy between the power available from the hindlimb muscles and that required during takeoff. The present study provides integrated data on muscle contractile properties, morphology and jumping performance that support this conclusion. We show here that the predicted power output during takeoff in Cuban tree frogs Osteopilus septentrionalis exceeds that available from the muscles by at least sevenfold. We consider the sartorius muscle as representative of the bulk of the hindlimb muscles of these animals, because this muscle has properties typical of other hindlimb muscles of small frogs. At 25 degrees C, this muscle has a maximum shortening velocity (Vmax) of 8.77 +/- 0.62 L0 s-1 (where L0 is the muscle length yielding maximum isometric force), a maximum isometric force (P0) of 24.1 +/- 2.3 N cm-2 and a maximum isotonic power output of 230 +/- 9.2 W kg-1 of muscle (mean +/- S.E.M.). In contrast, the power required to accelerate the animal in the longest jumps measured (approximately 1.4 m) is more than 800 W kg-1 of total hindlimb muscle. The peak instantaneous power is expected to be twice this value. These estimates are probably conservative because the muscles that probably power jumping make up only 85% of the total hindlimb muscle mass. The total mechanical work required of the muscles is high (up to 60 J kg-1), but is within the work capacities predicted for vertebrate skeletal muscle. Clearly, a substantial portion of this work must be performed and stored prior to takeoff to account for the high power output during jumping. Interestingly, muscle work output during jumping is temperature-dependent, with greater work being produced at higher temperatures. The thermal dependence of work does not follow from simple muscle properties and instead must reflect the interaction between these properties and the other components of the skeletomuscular system during the propulsive phase of the jump.


1993 ◽  
Vol 174 (1) ◽  
pp. 199-213 ◽  
Author(s):  
T. P. Johnson ◽  
S. J. Swoap ◽  
A. F. Bennett ◽  
R. K. Josephson

The power output of fast-glycolytic (FG) muscle fibres isolated from the iliofibularis (IF) muscle of desert iguanas (Dipsosaurus dorsalis) was measured at 35 sC using the oscillatory work-loop technique. To simulate cyclical muscle length changes during running, isolated fibre bundles were subjected to sinusoidal length changes and phasic stimulation during the strain cycle. At constant strain (12 %), the duration and timing (phase) of stimulation were adjusted to maximise power output. Using both hatchlings (4–8 g) and adults of varying sizes (15–70 g), the intraspecific allometries of IF length and contractile properties were described by regression analysis. The muscle length at which isometric force was maximum (L0, mm) increased geometrically with body mass (M, g) (L0=5.7M0.33). Maximum power output and the force produced during shortening showed no significant relationship to body size; work output per cycle (Wopt, J kg-1) under conditions required to maximise power did increase with body size (Wopt=3.7M0.24). Twitch duration (Td, ms), measured from the onset of force generation to 50 % relaxation, increased allometrically with body mass (Td=12.4M0.18). Limb cycling frequency during burst running (f, reported in the literature) and the frequency required to maximise power output in vitro (fopt) decreased with body size, both being proportional to body mass raised to the power 0.24. These findings suggest that limb cycling frequency may be limited by twitch contraction kinetics. However, despite corresponding proportionality to body size, limb cycling frequencies during burst running are about 20 % lower than the cycling frequencies required to maximise power output. Differences in the contractile performance of the IF in vitro and in vivo are discussed in relation to constraints imposed by gravitational forces and the design of muscular, nervous and skeletal systems.


1998 ◽  
Vol 201 (7) ◽  
pp. 913-923 ◽  
Author(s):  
R James ◽  
I A Johnston

Fast-starts associated with escape responses were studied in short-horn sculpin (Myoxocephalus scorpius L.), ranging from 5.5 to 32 cm in total length (L). Electromyography and sonomicrometry were used simultaneously to measure muscle activation and length changes, respectively, in the superficial layers of fast muscle in rostral myotomes. Escape responses consisted of a half tailbeat to bend the body into a C-shape (C-bend), another half tailbeat (contralateral contraction), followed by one or two more tailbeats and/or a gliding phase. The scaling relationships for both muscle strain and shortening duration differed between the C-bend and the contralateral contraction. As a result, relative muscle shortening velocity (V/V0) scaled as -1.18L1.06 for the C-bend and as 1.23L-0. 66 for the contralateral contraction. Therefore, the scaling relationships for muscle shortening velocity varied throughout the time course of the escape response. Muscle power output was determined by using the work-loop technique to subject isolated muscle fibres to in vivo strain and stimulation patterns. Plots of the instantaneous muscle forces and velocities achieved during the contralateral contraction were found to deviate from the steady-state force-velocity relationship. Maximum instantaneous muscle power output was independent of body size, with mean maximum values of 307 and 222 W kg-1 wet muscle mass for the C-bend and the contralateral contraction, respectively. <P>


2012 ◽  
Vol 112 (12) ◽  
pp. 1975-1983 ◽  
Author(s):  
Maarten F. Bobbert

Force-velocity relationships reported in the literature for functional tasks involving a combination of joint rotations tend to be quasi-linear. The purpose of this study was to explain why they are not hyperbolic, like Hill's relationship. For this purpose, a leg press task was simulated with a musculoskeletal model of the human leg, which had stimulation of knee extensor muscles as only independent input. In the task the ankles moved linearly, away from the hips, against an imposed external force that was reduced over contractions from 95 to 5% of the maximum isometric value. Contractions started at 70% of leg length, and force and velocity values were extracted when 80% of leg length was reached. It was shown that the relationship between leg extension velocity and external force was quasi-linear, while the relationship between leg extension velocity and muscle force was hyperbolic. The discrepancy was explained by the fact that segmental dynamics canceled more and more of the muscle force as the external force was further reduced and velocity became higher. External power output peaked when the imposed external force was ∼50% of maximum, while muscle power output peaked when the imposed force was only ∼15% of maximum; in the latter case ∼70% of muscle power was buffered by the leg segments. According to the results of this study, there is no need to appeal to neural mechanisms to explain why, in leg press tasks, the force-velocity relationship is quasi-linear rather than hyperbolic.


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