Showing papers by "Andrew A. Biewener published in 2008"

Functional diversification within and between muscle synergists during locomotion

Abstract: Locomotion arises from the complex and coordinated function of limb muscles. Yet muscle function is dynamic over the course of a single stride and between strides for animals moving at different sp...

Hind limb scaling of kangaroos and wallabies (superfamily Macropodoidea): implications for hopping performance, safety factor and elastic savings

Abstract: The aim of this study was to examine hind limb scaling of the musculoskeletal system in the Macropodoidea, the superfamily containing wallabies and kangaroos, to re-examine the effect of size on the locomotor mechanics and physiology of marsupial hopping. Morphometric musculoskeletal analyses were conducted of 15 species and skeletal specimens of 21 species spanning a size range from 0.8 to 80 kg that included representatives of 12 of the 16 extant genera of macropodoids. We found that unlike other groups, macropodoids are able to match force demands associated with increasing body size primarily through a combination of positive allometry in muscle area and muscle moment arms. Isometric scaling of primary hind limb bones suggests, however, that larger species experience relatively greater bone stresses. Muscle to tendon area ratios of the ankle extensors scale with strong positive allometry, indicating that peak tendon stresses also increase with increasing body size but to a lesser degree than previously reported. Consistent with previous morphological and experimental studies, large macropodoids are therefore better suited for elastic strain energy recovery but operate at lower safety factors, which likely poses an upper limit to body size. Scaling patterns for extant macropodoids suggest that extinct giant kangaroos (~250 kg) were likely limited in locomotor capacity.

Contractile properties of the pigeon supracoracoideus during different modes of flight

Abstract: The supracoracoideus (SUPRA) is the primary upstroke muscle for avian flight and is the antagonist to the downstroke muscle, the pectoralis (PECT). We studied in vivo contractile properties and mechanical power output of both muscles during take-off, level and landing flight. We measured muscle length change and activation using sonomicrometry and electromyography, and muscle force development using strain recordings on the humerus. Our results support a hypothesis that the primary role of the SUPRA is to supinate the humerus. Antagonistic forces exerted by the SUPRA and PECT overlap during portions of the wingbeat cycle, thereby offering a potential mechanism for enhancing control of the wing. Among flight modes, muscle strain was approximately the same in the SUPRA (33-40%) and the PECT (35-42%), whereas peak muscle stress was higher in the SUPRA (85-126 N m(-2)) than in the PECT (50-58 N m(-2)). The SUPRA mainly shortened relative to resting length and the PECT mainly lengthened. We estimated that elastic energy storage in the tendon of the SUPRA contributed between 28 and 60% of the net work of the SUPRA and 6-10% of the total net mechanical work of both muscles. Mechanical power output in the SUPRA was congruent with the estimated inertial power required for upstroke, but power output from the PECT was only 42-46% of the estimated aerodynamic power requirements for flight. There was a significant effect of flight mode upon aspects of the contractile behavior of both muscles including strain, strain rate, peak stress, work and power.

Compliance, actuation, and work characteristics of the goat foreleg and hindleg during level, uphill, and downhill running

Abstract: We model the action of muscle-tendon system(s) about a given joint as a serial actuator and spring. By this technique, the experimental joint moment is imposed while the combined angular deflection of the actuator and spring are constrained to match the experimental joint angle throughout the stance duration. The same technique is applied to the radial leg (i.e., shoulder/hip-to-foot). The spring constant that minimizes total actuator work is considered optimal, and this minimum work is expressed as a fraction of total joint/radial leg work, yielding an actuation ratio (AR; 1 = pure actuation and 0 = pure compliance). To address work modulation, we determined the specific net work (SNW), the absolute value of net divided by total work. This ratio is unity when only positive or negative work is done and zero when equal energy is absorbed and returned. Our proximodistal predictions of joint function are supported during level and 15° grade running. The greatest AR and SNW are found in the proximal leg joints (elbow and knee). The ankle joint is the principal spring of the hindleg and shows no significant change in SNW with grade, reflecting the true compliance of the common calcaneal tendon. The principal foreleg spring is the metacarpophalangeal joint. The observed pattern of proximal actuation and distal compliance, as well as the substantial SNW at proximal joints, minimal SNW at intermediate joints, and variable energy absorption at distal joints, may emerge as general principles in quadruped limb mechanics and help to inform the leg designs of highly capable running robots.

Kinematics and power requirements of ascending and descending flight in the pigeon (Columba livia).

Abstract: Ascending or descending locomotion involves a change in potential energy (PE) and a corresponding change in power requirement. We sought to test whether the mechanical power required for steady ascending or descending flight is a simple sum of the power required for level flight and the power necessary for potential energy change. Pigeons (Columba livia) were trained to fly at varying angles of ascent and descent (60 degrees , 30 degrees , 0 degrees , -30 degrees , -60 degrees ), and were recorded using high-speed video. Detailed three-dimensional kinematics were obtained from the recordings, allowing analysis of wing movement. Aerodynamic forces and power requirements were then estimated from kinematic data. As expected, ;PE flight power' increased significantly with angle of flight (0.234 W deg.(-1)), though there appeared to be a limit on the amount of PE that the birds could gain or dissipate per wingbeat. We found that the total power output for flight at various angles was not different from the sum of power required for level flight and the PE rate of change for a given angle, except for the steep -60 degrees descent. The total power for steep descent was higher than this sum because of a higher induced power due to the bird's deceleration and slower flight velocity. Aerodynamic force estimates during mid-downstroke did not differ significantly in magnitude or orientation among flight angles. Pigeons flew fastest during -30 degrees flights (4.9+/-0.1 m s(-1)) and slowest at 60 degrees (2.9+/-0.1 m s(-1)). Although wingbeat frequency ranged from 6.1 to 9.6 Hz across trials, the variation was not significant across flight angles. Stroke plane angle was more horizontal, and the wing more protracted, for both +60 degrees and -60 degrees flights, compared with other flight path angles.

Integration within and between muscles during terrestrial locomotion: effects of incline and speed.

Abstract: Animals must continually adapt to varying locomotor demands when moving in their natural habitat. Despite the dynamic nature of locomotion, little is known about how multiple muscles, and different parts of a muscle, are functionally integrated as demand changes. In order to determine the extent to which synergist muscles are functionally heterogeneous, and whether this heterogeneity is altered with changes in demand, we examined the in vivo function of the lateral (LG) and medial (MG) gastrocnemius muscles of helmeted guinea fowl (Numida meleagris) during locomotion on different inclines (level and uphill at 14 degrees ) and at different speeds (0.5 and 2.0 m s(-1)). We also quantified function in the proximal (pMG) and distal (dMG) regions of the MG to examine the extent to which a single muscle is heterogeneous. We used electromyography, sonomicrometry and tendon force buckles to quantify activation, length change and force patterns of both muscles, respectively. We show that the LG and MG exhibited an increase in force and stress with a change in gait and an increase in locomotor speed, but not with changes in incline. While the LG and MG exhibited similar levels of stress when walking at 0.5 m s(-1), stress in the LG was 1.8 times greater than in the MG when running at 2.0 m s(-1). Fascicle shortening increased with an increase in speed on both inclines for the LG, but only on the level for the pMG. Positive work performed by the LG exceeded that of the pMG and dMG for all conditions, and this difference was magnified when locomotor speed increased. Within the MG, the pMG shortened more, and at a faster rate than the dMG, resulting in a greater amount of positive work performed by the pMG. Mean spike amplitude of the electromyogram (EMG) bursts increased for all muscle locations with an increase in speed, but changes with incline were more variable. The functional differences between the LG and MG are likely due to the different moments each exerts at the knee, as well as differences in motor unit recruitment. The differences within the MG are likely due to motor unit recruitment differences, but also differences in architecture. Fascicles within the dMG insert into an extensive aponeurosis, which results in a higher apparent dynamic stiffness relative to fascicles operating within the pMG. On the level surface, the greater compliance of the pMG leads to increased stretch of its fascicles at the onset of force, further enhancing force production. Our results demonstrate the capacity for functional diversity between and within muscle synergists, which occur with changes in gait, speed and grade.

Tendons and Ligaments: Structure, Mechanical Behavior and Biological Function

Abstract: The non-linear viscoelasticity of tendons and ligaments, for which much of their mechanical behavior reflects the properties of their collagen I fibrils, is well suited to absorbing and returning energy associated with the transmission of tensile forces across joints of the body. The high resilience of tendon means that it can serve as an effective biological spring. At the same time, the flexibility of tendons and ligaments allows them to accommodate a wide range of joint movement (or, in the case of ligaments, to restrict movement within a certain range). The high strength of tendons and ligaments also provides considerable weight savings, but this is traded off against the ability to control position and movements of the musculoskeletal system. Tendon and ligament compliance allows elastic energy to be stored and returned to offset energy fluctuations of the body’s center of mass during locomotion, conserving muscle work and reducing the metabolic energy cost of locomotor movement. Tendon architecture greatly affects the storage and recovery of elastic strain energy, with long, thin tendons favoring greater strain energy/volume (and weight) of the tendon. It is likely that other elastic elements, such as muscle aponeuroses, also contribute significant energy savings. Tendon compliance may also reduce the cost of muscle contraction, by reducing a muscle’s contractile velocity and length change for a given movement, as well as increasing the power output of muscle–tendon units that is key to rapid acceleration and jumping performance. This power enhancement requires a temporal decoupling of muscle work to stretch the tendon from the subsequent more rapid release of elastic strain energy from the tendon. This decoupling may be achieved by changes in inertia and mechanical advantage in vertebrates, but is facilitated by catch mechanisms in invertebrate jumpers. Although it is critical that tendons and ligaments have sufficient strength and an adequate safety factor to limit the risk of failure, tendons are likely subject to damage during their use, which favors a greater safety factor. In addition, because tendon compliance impedes position control, the thickness of many tendons suggests that having sufficient stiffness, rather than strength, is a key structural requirement. Indeed, the majority of tendons that have been studied to date appear to operate at lower stresses and strains, have larger safety factors, and are stiffer, compared with “high-stress” tendons of animals specialized for elastic energy savings.

Differential design for hopping in two species of wallabies

Abstract: Hindlimb musculoskeletal anatomy and steady speed over ground hopping mechanics were compared in two species of macropod marsupials, tammar wallabies and yellow-footed rock wallabies (YFRW). These two species are relatively closely related and are of similar size and general body plan, yet they inhabit different environments with presumably different musculoskeletal demands. Tammar wallabies live in relatively flat, open habitat whereas yellow-footed rock wallabies inhabit steep cliff faces. The goal of this study was to explore musculoskeletal differences between tammar wallabies and yellow-footed rock wallabies and determine how these differences influence each species' hopping mechanics. We found the cross-sectional area of the combined ankle extensor tendons of yellow-footed rock wallabies was 13% greater than that of tammar wallabies. Both species experienced similar ankle joint moments during steady-speed hopping, however due to a lower mechanical advantage at this joint, tammar wallabies produced 26% more muscle force. Thus, during moderate speed hopping, yellow-footed rock wallabies operated with 38% higher tendon safety factors, while tammar wallabies were able to store 73% more elastic strain energy (2.18 J per leg vs. 1.26 J in YFRW). This likely reflects the differing demands of the environments inhabited by these two species, where selection for non-steady locomotor performance in rocky terrain likely requires trade-offs in locomotor economy.

Differential muscle function between muscle synergists: long and lateral heads of the triceps in jumping and landing goats (Capra hircus)

Abstract: We investigate how the biarticular long head and monoarticular lateral head of the triceps brachii function in goats (Capra hircus) during jumping and landing. Elbow moment and work were measured from high-speed video and ground reaction force (GRF) recordings. Muscle activation and strain were measured via electromyography and sonomicrometry, and muscle stress was estimated from elbow moment and by partitioning stress based on its relative strain rate. Elbow joint and muscle function were compared among three types of limb usage: jump take-off (lead limb), the step prior to jump take-off (lag limb), and landing. We predicted that the strain and work patterns in the monoarticular lateral head would follow the kinematics and work of the elbow more closely than would those of the biarticular long head. In general this prediction was supported. For instance, the lateral head stretched (5 +/- 2%; mean +/- SE) in the lead and lag limbs to absorb work during elbow flexion and joint work absorption, while the long head shortened (-7 +/- 1%) to produce work. During elbow extension, both muscles shortened by similar amounts (-10 +/- 2% long; -13 +/- 4% lateral) in the lead limb to produce work. Both triceps heads functioned similarly in landing, stretching (13 +/- 3% in the long head and 19 +/- 5% in the lateral) to absorb energy. In general, the long head functioned to produce power at the shoulder and elbow, while the lateral head functioned to resist elbow flexion and absorb work, demonstrating that functional diversification can arise between mono- and biarticular muscle agonists operating at the same joint.

Variability in forelimb bone strains during non-steady locomotor activities in goats

Abstract: The purpose of this study was to investigate the effects of non-steady locomotor activities on load predictability in two goat forelimb bones and to explore the degree to which bone curvature influences load predictability. We measured in vivo bone strains in the radius and metacarpus of juvenile goats performing a variety of natural behaviors in an outdoor arena and compared these strain magnitudes and loading patterns with those measured during steady-state treadmill locomotion. We sought to test two hypotheses: our first hypothesis expects an increase in the variability of strain magnitude and pattern during outdoor non-steady behavior when compared to treadmill locomotion. Our second hypothesis was that the curved radius experiences higher peak strains but less variability during non-steady activities than the straighter metacarpus. We found that unsteady, outdoor locomotion generally caused more variable strain patterns (consistent with the first hypothesis), but not more variable strain magnitudes, than treadmill locomotion in both bones. During outdoor locomotion, higher magnitude strain events in the radius showed more constrained loading patterns than in the metacarpus (consistent with the second hypothesis). In addition to the radius experiencing significantly greater bending strains compared to the straighter metacarpus, these results support the idea of a trade-off between increased predictability of loading pattern and increased bending-induced strain. Strain magnitudes recorded during both outdoor and treadmill locomotion showed a lognormal frequency distribution, but the outdoor bone strain distributions had a greater range because they included high magnitude loading events that did not occur during steady treadmill locomotion.

Biomechanics of swimming and flight

Abstract: This special issue on Biomechanics of Swimming and Flight underpins the importance of biomechanics as one of the core disciplines of The Journal of Experimental Biology . It was inspired by a two-day symposium on swimming and flying at the 5th World Congress of Biomechanics 2006 in Munich, Germany.