Publications

2019
Lai A, Biewener AA, Wakeling JM. Muscle-specific indices to characterise the functional behavior of human lower-limb muscles during locomotion . Journal of Biomechanics [Internet]. 2019;89 :134-138. Publisher's Version
McHorse BK, Biewener AA, Pierce SE. The evolution of a single toe in horses: causes, consequences, and the way forward. Integrative & Compartive Biology [Internet]. 2019;icz050 (10.1093) :1-18. Publisher's Version
Kessler SE, Rainbow MJ, Lichtwark GA, Cresswell AG, D'Andrea SE, Konow N, Kelly LA. A Direct Comparison of Biplanar Videoradiography and Optical Motion Capture for Foot and Ankle Kinematics. Frontiers in Bioengineering and Biotechnology [Internet]. 2019;7 (199) :1-10. Publisher's VersionAbstract
Measuring motion of the human foot presents a unique challenge due to the large number of closely packed bones with congruent articulating surfaces. Optical motion capture (OMC) and multi-segment models can be used to infer foot motion, but might be affected by soft tissue artifact (STA). Biplanar videoradiography (BVR) is a relatively new tool that allows direct, non-invasive measurement of bone motion using high-speed, dynamic x-ray images to track individual bones. It is unknown whether OMC and BVR can be used interchangeably to analyse multi-segment foot motion. Therefore, the aim of this study was to determine the agreement in kinematic measures of dynamic activities. Nine healthy participants performed three walking and three running trials while BVR was recorded with synchronous OMC. Bone position and orientation was determined through manual scientific-rotoscoping. The OMC and BVR kinematics were co-registered to the same coordinate system, and BVR tracking was used to create virtual markers for comparison to OMC during dynamic trials. Root mean square (RMS) differences in marker positions and joint angles as well as a linear fit method (LFM) was used to compare the outputs of both methods. When comparing BVR and OMC, sagittal plane angles were in good agreement (ankle: R2 = 0.947, 0.939; Medial Longitudinal Arch (MLA) Angle: R2 = 0.713, 0.703, walking and running, respectively). When examining the ankle, there was a moderate agreement between the systems in the frontal plane (R2 = 0.322, 0.452, walking and running, respectively), with a weak to moderate correlation for the transverse plane (R2 = 0.178, 0.326, walking and running, respectively). However, root mean squared error (RMSE) showed angular errors ranging from 1.06 to 8.31° across the planes (frontal: 3.57°, 3.67°, transverse: 4.28°, 4.70°, sagittal: 2.45°, 2.67°, walking and running, respectively). Root mean square (RMS) differences between OMC and BVR marker trajectories were task dependent with the largest differences in the shank (6.0 ± 2.01 mm) for running, and metatarsals (3.97 ± 0.81 mm) for walking. Based on the results, we suggest BVR and OMC provide comparable solutions to foot motion in the sagittal plane, however, interpretations of out-of-plane movement should be made carefully.
Witzmann F, Brainerd EL, Konow N. Eye Movements in Frogs and Salamanders—Testing the Palatal Buccal Pump Hypothesis. Integrative Organismal Biology [Internet]. 2019;1 (1). Publisher's VersionAbstract
In frogs and salamanders, movements of the eyeballs in association with an open palate have often been proposed to play a functional role in lung breathing. In this “palatal buccal pump,” the eyeballs are elevated during the lowering of the buccal floor to suck air in through the nares, and the eyeballs are lowered during elevation of the buccal floor to help press air into the lungs. Here, we used X-Ray Reconstruction of Moving Morphology to investigate eye movements during lung breathing and feeding in bullfrogs and axolotls. Our data do not show eye movements that would be in accordance with the palatal buccal pump. On the contrary, there is a small passive elevation of the eyeballs when the buccal floor is raised. Inward drawing of the eyeballs occurs only during body motion and for prey transport in bullfrogs, but this was not observed in axolotls. Each eye movement in bullfrogs has a vertical, a mediolateral, and an anteroposterior component. Considering the surprisingly weak posterior motion component of the eyeballs, their main role in prey transport might be fixing the prey by pressing it against the buccal floor. The retraction of the buccal floor would then contribute to the posterior push of the prey. Because our study provides no evidence for a palatal buccal pump in frogs and salamanders, there is also no experimental support for the idea of a palatal buccal pump in extinct temnospondyl amphibians, in contrast to earlier suggestions.
Arellano C, Konow N, Gidmark N, Roberts TJ. Evidence of a tunable biological spring: Elastic energy storage in aponeuroses varies with transverse strain in vivo. Proceedings of Royal Society Series B [Internet]. 2019;286 (1900) :20182764. Publisher's Version
Lin Y, Konow N, Dumont ER. How moles destroy your lawn: the forelimb kinematics of Eastern moles in loose and compact substrates. Journal of Experimental Biology [Internet]. 2019;222. Publisher's Version
Heiss E, Schwartz D, Konow N. Chewing or not? Intraoral food processing in a salamandrid newt. Journal of Experimental Biology [Internet]. 2019;222. Publisher's Version
Clites TR, Arnold AS, Singh NM, H.Chen, Tugman C, Billadeau B, Biewener AA, Herr HM. Goats decrease hindlimb stiffness when walking over compliant surfaces. Journal of Experimental Biology [Internet]. 2019;222. Publisher's Version
Lai A, Biewener AA, Wakeling JM. Muscle-specific indices to characterise the functional behaviours of human lower limb muscles during locomotion. Journal of Biomechanics. 2019;89 :134-138.
2018
Biewener AA. Animal Locomotion: Near-Ground Low-Cost Flights. Curr. Biol. [Internet]. 2018;28 (23) :R1348-R1349. Publisher's Version
Lai A, Biewener AA, Wakeling JM. Metabolic cost underlies task-dependent variations in motor unit recruitment. J. Roy. Soc. Interface [Internet]. 2018;15 (148). Publisher's Version
Clifton GT, Biewener AA. Foot-propelled swimming kinematics and turning strategies in common loons. J. exp. Biol. [Internet]. 2018;221 :1-11. Publisher's Version
Ahn AN, Konow N, Tijs C, Biewener AA. Different segments within vertebrate muscles can operate on different regions of their force-length relationships. Int. Comp. Biol. [Internet]. 2018;58 :219-231. Publisher's Version
Biewener AA. Evolutionary race as predators hunt prey. Nature [Internet]. 2018;554 :176-178. Publisher's Version
Lai PH, Biewener AA, Pierce SE. Three‐dimensional mobility and muscle attachments in the pectoral limb of the Triassic cynodont Massetognathus pascuali (Romer, 1967). Journal of Anatomy [Internet]. 2018;232 (3) :383-406. Publisher's VersionAbstract
The musculoskeletal configuration of the mammalian pectoral limb has been heralded as a key anatomical feature leading to the adaptive radiation of mammals, but limb function in the non‐mammaliaform cynodont outgroup remains unresolved. Conflicting reconstructions of abducted and adducted posture are based on mutually incompatible interpretations of ambiguous osteology. We reconstruct the pectoral limb of the Triassic non‐mammaliaform cynodont Massetognathus pascuali in three dimensions, by combining skeletal morphology from micro‐computed tomography with muscle anatomy from an extended extant phylogenetic bracket. Conservative tests of maximum range of motion suggest a degree of girdle mobility, as well as substantial freedom at the shoulder and the elbow joints. The glenoid fossa supports a neutral pose in which the distal end of the humerus points 45° posterolaterally from the body wall, intermediate between classically ‘sprawling’ and ‘parasagittal’ limb postures. Massetognathus pascuali is reconstructed as having a near‐mammalian complement of shoulder muscles, including an incipient rotator cuff (m. subscapularis, m. infraspinatus, m. supraspinatus, and m. teres minor). Based on close inspection of the morphology of the glenoid fossa, we hypothesize a posture‐driven scenario for the evolution of the therian ball‐and‐socket shoulder joint. The musculoskeletal reconstruction presented here provides the anatomical scaffolding for more detailed examination of locomotor evolution in the precursors to mammals.
Lai A, Arnold A, Biewener AA, Dick T, Wakeling JM. Does a two-element muscle model offer advantages when estimating ankle plantar flexor forces during human cycling?. Journal of Biomechanics [Internet]. 2018;68 :6-13. Publisher's VersionAbstract
Traditional Hill-type muscle models, parameterized using high-quality experimental data, are often “too weak” to reproduce the joint torques generated by healthy adults during rapid, high force tasks. This study investigated whether the failure of these models to account for different types of motor units contributes to this apparent weakness; if so, muscle-driven simulations may rely on excessively high muscle excitations to generate a given force. We ran a series of forward simulations that reproduced measured ankle mechanics during cycling at five cadences ranging from 60 to 140 RPM. We generated both “nominal” simulations, in which an abstract ankle model was actuated by a 1-element Hill-type plantar flexor with a single contractile element (CE), and “test” simulations, in which the same model was actuated by a 2-element plantar flexor with two CEs that accounted for the force-generating properties of slower and faster motor units. We varied the total excitation applied to the 2-element plantar flexor between 60 and 105% of the excitation from each nominal simulation, and we varied the amount distributed to each CE between 0 and 100% of the total. Within this test space, we identified the excitation level and distribution, at each cadence, that best reproduced the plantar flexor forces generated in the nominal simulations. Our comparisons revealed that the 2-element model required substantially less total excitation than the 1-element model to generate comparable forces, especially at higher cadences. For instance, at 140 RPM, the required excitation was reduced by 23%. These results suggest that a 2-element model, in which contractile properties are “tuned” to represent slower and faster motor units, can increase the apparent strength and perhaps improve the fidelity of simulations of tasks with varying mechanical demands.
2017
Lai AKM, Arnold AS, Wakeling JM. Why are antagonist muscles co-activated in my simulation? A musculoskeletal model for analyzing human locomotor tasks. Annals of Biomedical Engineering [Internet]. 2017;45 (12) :2762-2774. Publisher's VersionAbstract
Existing "off-the-shelf" musculoskeletal models are problematic when simulating movements that involve substantial hip and knee flexion, such as the upstroke of pedalling, because they tend to generate excessive passive fibre force. The goal of this study was to develop a refined musculoskeletal model capable of simulating pedalling and fast running, in addition to walking, which predicts the activation patterns of muscles better than existing models. Specifically, we tested whether the anomalous co-activation of antagonist muscles, commonly observed in simulations, could be resolved if the passive forces generated by the underlying model were diminished. We refined the OpenSim™ model published by Rajagopal et al. (IEEE Trans Biomed Eng 63:1-1, 2016) by increasing the model's range of knee flexion, updating the paths of the knee muscles, and modifying the force-generating properties of eleven muscles. Simulations of pedalling, running and walking based on this model reproduced measured EMG activity better than simulations based on the existing model-even when both models tracked the same subject-specific kinematics. Improvements in the predicted activations were associated with decreases in the net passive moments; for example, the net passive knee moment during the upstroke of pedalling decreased from 36.9 N m (existing model) to 6.3 N m (refined model), resulting in a dramatic decrease in the co-activation of knee flexors. The refined model is available from SimTK.org and is suitable for analysing movements with up to 120° of hip flexion and 140° of knee flexion.
Kambic RE, Biewener AA, Pierce SE. Experimental determination of three-dimensional cervical joint mobility in the avian neck. Frontiers in Zoology. 2017;14 (37) :1-15.Abstract

Background

Birds have highly mobile necks, but neither the details of how they realize complex poses nor the evolution of this complex musculoskeletal system is well-understood. Most previous work on avian neck function has focused on dorsoventral flexion, with few studies quantifying lateroflexion or axial rotation. Such data are critical for understanding joint function, as musculoskeletal movements incorporate motion around multiple degrees of freedom simultaneously. Here we use biplanar X-rays on wild turkeys to quantify three-dimensional cervical joint range of motion in an avian neck to determine patterns of mobility along the cranial-caudal axis.

Results

Range of motion can be generalized to a three-region model: cranial joints are ventroflexed with high axial and lateral mobility, caudal joints are dorsiflexed with little axial rotation but high lateroflexion, and middle joints show varying amounts axial rotation and a low degree of lateroflexion. Nonetheless, variation within and between regions is high. To attain complex poses, substantial axial rotation can occur at joints caudal to the atlas/axis complex and zygapophyseal joints can reduce their overlap almost to osteological disarticulation. Degrees of freedom interact at cervical joints; maximum lateroflexion occurs at different dorsoventral flexion angles at different joints, and axial rotation and lateroflexion are strongly coupled. Further, patterns of joint mobility are strongly predicted by cervical morphology.

Conclusion

Birds attain complex neck poses through a combination of mobile intervertebral joints, coupled rotations, and highly flexible zygapophyseal joints. Cranial-caudal patterns of joint mobility are tightly linked to cervical morphology, such that function can be predicted by form. The technique employed here provides a repeatable protocol for studying neck function in a broad array of taxa that will be directly comparable. It also serves as a foundation for future work on the evolution of neck mobility along the line from non-avian theropod dinosaurs to birds.

Electronic supplementary material

The online version of this article (doi:10.1186/s12983-017-0223-z) contains supplementary material, which is available to authorized users.

Keywords: Function, Mobility, XROMM, Avian, Bird, Anatomy, Cervical, Neck, X-ray, Motion, Morphology
Deetjen ME, Biewener AA, Lentink D. High-speed surface reconstruction of a flying bird using structured-light. J. Exp. Biol. 2017;220 :1956-1961.Abstract
Birds fly effectively and maneuver nimbly by dynamically changing the shape of their wings during each wingbeat. These shape changes have yet to be quantified automatically at high temporal and spatial resolution. Therefore, we developed a custom 3D surface reconstruction method, which uses a high-speed camera to identify spatially encoded binary striped patterns that are projected on a flying bird. This non-invasive structured-light method allows automated 3D reconstruction of each stand-alone frame and can be extended to multiple views. We demonstrate this new technique by automatically reconstructing the dorsal surface of a parrotlet wing at 3200 fps during flapping flight. From this shape we analyze key parameters such as wing twist and angle of attack distribution. While our binary ‘single-shot’ algorithm is demonstrated by quantifying dynamic shape changes of a flying bird, it is generally applicable to moving animals, plants and deforming objects.
McHorse BK, Biewener AA, Pierce SE. Mechanics of evolutionary digit reduction in fossil horses . Proc. Roy. Soc. B. 2017;284 (20171174) :1-8.Abstract
Digit reduction is a major trend that characterizes horse evolution, but its causes and consequences have rarely been quantitatively tested. Using beam analysis on fossilized centre metapodials, we tested how locomotor bone stresses changed with digit reduction and increasing body size across the horse lineage. Internal bone geometry was captured from 13 fossil horse genera that covered the breadth of the equid phylogeny and the spectrum of digit reduction and body sizes, from Hyracotherium to Equus. To account for the load-bearing role of side digits, a novel, continuous measure of digit reduction was also established—toe reduction index (TRI). Our results show that without accounting for side digits, three-toed horses as late as Parahippus would have experienced physiologically untenable bone stresses. Conversely, when side digits are modelled as load-bearing, species at the base of the horse radiation through Equus probably maintained a similar safety factor to fracture stress. We conclude that the centre metapodial compensated for evolutionary digit reduction and body mass increases by becoming more resistant to bending through substantial positive allometry in internal geometry. These results lend support to two historical hypotheses: that increasing body mass selected for a single, robust metapodial rather than several smaller ones; and that, as horse limbs became elongated, the cost of inertia from the side toes outweighed their utility for stabilization or load-bearing.

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