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

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.

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).


2001 ◽  
Vol 204 (21) ◽  
pp. 3587-3600 ◽  
Author(s):  
Graham N. Askew ◽  
Richard L. Marsh

SUMMARYSonomicrometry and electromyographic (EMG) recordings were made for the pectoralis muscle of blue-breasted quail (Coturnix chinensis) during take-off and horizontal flight. In both modes of flight, the pectoralis strain trajectory was asymmetrical, with 70 % of the total cycle time spent shortening. EMG activity was found to start just before mid-upstroke and continued into the downstroke. The wingbeat frequency was 23 Hz, and the total strain was 23 % of the mean resting length.Bundles of fibres were dissected from the pectoralis and subjected in vitro to the in vivo length and activity patterns, whilst measuring force. The net power output was only 80 W kg–1 because of a large artefact in the force record during lengthening. For more realistic estimates of the pectoralis power output, we ignored the power absorbed by the muscle bundles during lengthening. The net power output during shortening averaged over the entire cycle was approximately 350 W kg–1, and in several preparations over 400 W kg–1. Sawtooth cycles were also examined for comparison with the simulation cycles, which were identical in all respects apart from the velocity profile. The power output during these cycles was found to be 14 % lower than during the in vivo strain trajectory. This difference was due to a higher velocity of stretch, which resulted in greater activation and higher power output throughout the later part of shortening, and the increase in shortening velocity towards the end of shortening, which facilitated deactivation.The muscle was found to operate at a mean length shorter than the plateau of the length/force relationship, which resulted in the isometric stress measured at the mean resting length being lower than is typically reported for striated muscle.


1994 ◽  
Vol 197 (1) ◽  
pp. 143-164
Author(s):  
D A Syme

Mechanical power and oxygen consumption (VO2) were measured simultaneously from isolated segments of trabecular muscle from the frog (Rana pipiens) ventricle. Power was measured using the work-loop technique, in which bundles of trabeculae were subjected to cyclic, sinusoidal length change and phasic stimulation. VO2 was measured using a polarographic O2 electrode. Both mechanical power and VO2 increased with increasing cycle frequency (0.4-0.9 Hz), with increasing muscle length and with increasing strain (= shortening, range 0-25% of resting length). Net efficiency, defined as the ratio of mechanical power output to the energy equivalent of the increase in VO2 above resting level, was independent of cycle frequency and increased from 8.1 to 13.0% with increasing muscle length, and from 0 to 13% with increasing strain, in the ranges examined. Delta efficiency, defined as the slope of the line relating mechanical power output to the energy equivalent of VO2, was 24-43%, similar to that reported from studies using intact hearts. The cost of increasing power output was greater if power was increased by increasing cycle frequency or muscle length than if it was increased by increasing strain. The results suggest that the observation that pressure-loading is more costly than volume-loading is inherent to these muscle fibres and that frog cardiac muscle is, if anything, less efficient than most skeletal muscles studied thus far.


Author(s):  
Amy K. Loya ◽  
Sarah K. Van Houten ◽  
Bernadette M. Glasheen ◽  
Douglas M. Swank

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.


2000 ◽  
Vol 203 (17) ◽  
pp. 2667-2689 ◽  
Author(s):  
R.K. Josephson ◽  
J.G. Malamud ◽  
D.R. Stokes

The basalar muscle of the beetle Cotinus mutabilis is a large, fibrillar flight muscle composed of approximately 90 fibers. The paired basalars together make up approximately one-third of the mass of the power muscles of flight. Changes in twitch force with changing stimulus intensity indicated that a basalar muscle is innervated by at least five excitatory axons and at least one inhibitory axon. The muscle is an asynchronous muscle; during normal oscillatory operation there is not a 1:1 relationship between muscle action potentials and contractions. During tethered flight, the wing-stroke frequency was approximately 80 Hz, and the action potential frequency in individual motor units was approximately 20 Hz. As in other asynchronous muscles that have been examined, the basalar is characterized by high passive tension, low tetanic force and long twitch duration. Mechanical power output from the basalar muscle during imposed, sinusoidal strain was measured by the work-loop technique. Work output varied with strain amplitude, strain frequency, the muscle length upon which the strain was superimposed, muscle temperature and stimulation frequency. When other variables were at optimal values, the optimal strain for work per cycle was approximately 5%, the optimal frequency for work per cycle approximately 50 Hz and the optimal frequency for mechanical power output 60–80 Hz. Optimal strain decreased with increasing cycle frequency and increased with muscle temperature. The curve relating work output and strain was narrow. At frequencies approximating those of flight, the width of the work versus strain curve, measured at half-maximal work, was 5% of the resting muscle length. The optimal muscle length for work output was shorter than that at which twitch and tetanic tension were maximal. Optimal muscle length decreased with increasing strain. The curve relating work output and muscle length, like that for work versus strain, was narrow, with a half-width of approximately 3 % at the normal flight frequency. Increasing the frequency with which the muscle was stimulated increased power output up to a plateau, reached at approximately 100 Hz stimulation frequency (at 35 degrees C). The low lift generated by animals during tethered flight is consistent with the low frequency of muscle action potentials in motor units of the wing muscles. The optimal oscillatory frequency for work per cycle increased with muscle temperature over the temperature range tested (25–40 degrees C). When cycle frequency was held constant, the work per cycle rose to an optimum with increasing temperature and then declined. We propose that there is a temperature optimum for work output because increasing temperature increases the shortening velocity of the muscle, which increases the rate of positive work output during shortening, but also decreases the durations of the stretch activation and shortening deactivation that underlie positive work output, the effect of temperature on shortening velocity being dominant at lower temperatures and the effect of temperature on the time course of activation and deactivation being dominant at higher temperatures. The average wing-stroke frequency during free flight was 94 Hz, and the thoracic temperature was 35 degrees C. The mechanical power output at the measured values of wing-stroke frequency and thoracic temperature during flight, and at optimal muscle length and strain, averaged 127 W kg(−1)muscle, with a maximum value of 200 W kg(−1). The power output from this asynchronous flight muscle was approximately twice that measured with similar techniques from synchronous flight muscle of insects, supporting the hypothesis that asynchronous operation has been favored by evolution in flight systems of different insect groups because it allows greater power output at the high contraction frequencies of flight.


1992 ◽  
Vol 70 (4) ◽  
pp. 602-606 ◽  
Author(s):  
Philip Robinson ◽  
Mitsushi Okazawa ◽  
Tony Bai ◽  
Peter Paré

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.


PeerJ ◽  
2016 ◽  
Vol 4 ◽  
pp. e2260 ◽  
Author(s):  
Brent J. Raiteri ◽  
Andrew G. Cresswell ◽  
Glen A. Lichtwark

Background.Muscles not only shorten during contraction to perform mechanical work, but they also bulge radially because of the isovolumetric constraint on muscle fibres. Muscle bulging may have important implications for muscle performance, however quantifying three-dimensional (3D) muscle shape changes in human muscle is problematic because of difficulties with sustaining contractions for the duration of anin vivoscan. Although two-dimensional ultrasound imaging is useful for measuring local muscle deformations, assumptions must be made about global muscle shape changes, which could lead to errors in fully understanding the mechanical behaviour of muscle and its surrounding connective tissues, such as aponeurosis. Therefore, the aims of this investigation were (a) to determine the intra-session reliability of a novel 3D ultrasound (3DUS) imaging method for measuringin vivohuman muscle and aponeurosis deformations and (b) to examine how contraction intensity influencesin vivohuman muscle and aponeurosis strains during isometric contractions.Methods.Participants (n= 12) were seated in a reclined position with their left knee extended and ankle at 90° and performed isometric dorsiflexion contractions up to 50% of maximal voluntary contraction. 3DUS scans of the tibialis anterior (TA) muscle belly were performed during the contractions and at rest to assess muscle volume, muscle length, muscle cross-sectional area, muscle thickness and width, fascicle length and pennation angle, and central aponeurosis width and length. The 3DUS scan involved synchronous B-mode ultrasound imaging and 3D motion capture of the position and orientation of the ultrasound transducer, while successive cross-sectional slices were captured by sweeping the transducer along the muscle.Results.3DUS was shown to be highly reliable across measures of muscle volume, muscle length, fascicle length and central aponeurosis length (ICC ≥ 0.98, CV < 1%). The TA remained isovolumetric across contraction conditions and progressively shortened along its line of action as contraction intensity increased. This caused the muscle to bulge centrally, predominantly in thickness, while muscle fascicles shortened and pennation angle increased as a function of contraction intensity. This resulted in central aponeurosis strains in both the transverse and longitudinal directions increasing with contraction intensity.Discussion.3DUS is a reliable and viable method for quantifying multidirectional muscle and aponeurosis strains during isometric contractions within the same session. Contracting muscle fibres do work in directions along and orthogonal to the muscle’s line of action and central aponeurosis length and width appear to be a function of muscle fascicle shortening and transverse expansion of the muscle fibres, which is dependent on contraction intensity. How factors other than muscle force change the elastic mechanical behaviour of the aponeurosis requires further investigation.


1985 ◽  
Vol 115 (1) ◽  
pp. 239-251 ◽  
Author(s):  
I. A. Johnston

The kinds of muscle fibre that are recruited for sustained force production by different vertebrates are described. Although aerobic metabolism always accounts for a significant proportion of their ATP turnover, no single characteristic such as colour, number and form of motor endplates, membrane properties, myosin isotype or contraction speed is diagnostic of such muscles. As mechanical power output increases, there is a tendency for a decrease in fatigue resistance with repetitive usage and an increase in both aerobic capacity and the fraction of energy requirements derived from glycolysis.


2021 ◽  
Author(s):  
Luis G. Rosa ◽  
Jonathan S. Zia ◽  
Omer T. Inan ◽  
Gregory S. Sawicki

AbstractBackground and objectiveDynamic muscle fascicle length measurements through B-mode ultrasound have become popular for the non-invasive physiological insights they provide regarding musculoskeletal structure-function. However, current practices typically require time consuming post-processing to track muscle length changes from B-mode images. A real-time measurement tool would not only save processing time but would also help pave the way toward closed-loop applications based on feedback signals driven by in vivo muscle length change patterns. In this paper, we benchmark an approach that combines traditional machine learning (ML) models with B-mode ultrasound recordings to obtain muscle fascicle length changes in real-time. To gauge the utility of this framework for ‘in-the-loop’ applications, we evaluate accuracy of the extracted muscle length change signals against time-series’ derived from a standard, post-hoc automated tracking algorithm.MethodsWe collected B-mode ultrasound data from the soleus muscle of six participants performing five defined ankle motion tasks: (a) seated, constrained ankle plantarflexion, (b) seated, free ankle dorsi/plantarflexion, (c) weight-bearing, calf raises (d) walking, and then a (e) mix. We trained machine learning (ML) models by pairing muscle fascicle lengths obtained from standardized automated tracking software (UltraTrack) with the respective B-mode ultrasound image input to the tracker, frame-by-frame. Then we conducted hyperparameter optimizations for five different ML models using a grid search to find the best performing parameters for a combination of high correlation and low RMSE between ML and UltraTrack processed muscle fascicle length trajectories. Finally, using the global best model/hyperparameter settings, we comprehensively evaluated training-testing outcomes within subject (i.e., train and test on same subject), cross subject (i.e., train on one subject, test on another) and within/direct cross task (i.e., train and test on same subject, but different task).ResultsSupport vector machine (SVM) was the best performing model with an average r = 0.70 ±0.34 and average RMSE = 2.86 ±2.55 mm across all direct training conditions and average r = 0.65 ±0.35 and average RMSE = 3.28 ±2.64 mm when optimized for all cross-participant conditions. Comparisons between ML vs. UltraTrack (i.e., ground truth) tracked muscle fascicle length versus time data indicated that ML tracked images reliably capture the salient qualitative features in ground truth length change data, even when correlation values are on the lower end. Furthermore, in the direct training, calf raises condition, which is most comparable to previous studies validating automated tracking performance during isolated contractions on a dynamometer, our ML approach yielded 0.90 average correlation, in line with other accepted tracking methods in the field.ConclusionsBy combining B-mode ultrasound and classical ML models, we demonstrate it is possible to achieve real-time tracking of human soleus muscle fascicles across a number of functionally relevant contractile conditions. This novel sensing modality paves the way for muscle physiology in-the-loop applications that could be used to modify gait via biofeedback or unlock novel wearable device control techniques that could enable restored or augmented locomotion performance.


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