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Musculoskeletal modelling of an ostrich (Struthio camelus) pelvic limb: influence of limb orientation on muscular capacity during locomotion.

Hutchinson JR, Rankin JW, Rubenson J, Rosenbluth KH, Siston RA, Delp SL - PeerJ (2015)

Bottom Line: Our two hypotheses relate to the control priorities that a large bipedal animal might evolve under biomechanical constraints to achieve more effective static weight support.However, some conspicuous areas of disagreement in our results illustrate some cautionary principles.Such a framework could remove obstacles impeding the analysis of muscle function in extinct taxa.

View Article: PubMed Central - HTML - PubMed

Affiliation: Structure and Motion Laboratory, Department of Comparative Biomedical Sciences, The Royal Veterinary College, University of London , Hatfield, Hertfordshire , United Kingdom ; Bioengineering Department, Stanford University , Stanford, CA , USA.

ABSTRACT
We developed a three-dimensional, biomechanical computer model of the 36 major pelvic limb muscle groups in an ostrich (Struthio camelus) to investigate muscle function in this, the largest of extant birds and model organism for many studies of locomotor mechanics, body size, anatomy and evolution. Combined with experimental data, we use this model to test two main hypotheses. We first query whether ostriches use limb orientations (joint angles) that optimize the moment-generating capacities of their muscles during walking or running. Next, we test whether ostriches use limb orientations at mid-stance that keep their extensor muscles near maximal, and flexor muscles near minimal, moment arms. Our two hypotheses relate to the control priorities that a large bipedal animal might evolve under biomechanical constraints to achieve more effective static weight support. We find that ostriches do not use limb orientations to optimize the moment-generating capacities or moment arms of their muscles. We infer that dynamic properties of muscles or tendons might be better candidates for locomotor optimization. Regardless, general principles explaining why species choose particular joint orientations during locomotion are lacking, raising the question of whether such general principles exist or if clades evolve different patterns (e.g., weighting of muscle force-length or force-velocity properties in selecting postures). This leaves theoretical studies of muscle moment arms estimated for extinct animals at an impasse until studies of extant taxa answer these questions. Finally, we compare our model's results against those of two prior studies of ostrich limb muscle moment arms, finding general agreement for many muscles. Some flexor and extensor muscles exhibit self-stabilization patterns (posture-dependent switches between flexor/extensor action) that ostriches may use to coordinate their locomotion. However, some conspicuous areas of disagreement in our results illustrate some cautionary principles. Importantly, tendon-travel empirical measurements of muscle moment arms must be carefully designed to preserve 3D muscle geometry lest their accuracy suffer relative to that of anatomically realistic models. The dearth of accurate experimental measurements of 3D moment arms of muscles in birds leaves uncertainty regarding the relative accuracy of different modelling or experimental datasets such as in ostriches. Our model, however, provides a comprehensive set of 3D estimates of muscle actions in ostriches for the first time, emphasizing that avian limb mechanics are highly three-dimensional and complex, and how no muscles act purely in the sagittal plane. A comparative synthesis of experiments and models such as ours could provide powerful synthesis into how anatomy, mechanics and control interact during locomotion and how these interactions evolve. Such a framework could remove obstacles impeding the analysis of muscle function in extinct taxa.

No MeSH data available.


Related in: MedlinePlus

Hip flexor/extensor moment arms plotted against joint angle for key proximal thigh muscles.See captions for Figs. 9 and 10.
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fig-11: Hip flexor/extensor moment arms plotted against joint angle for key proximal thigh muscles.See captions for Figs. 9 and 10.

Mentions: Figures 9–11 show our results for hip flexion/extension moment arms of ostrich muscles, with comparable data from Smith et al. (2007) and Bates & Schachner (2012) also plotted if available (abbreviated in this section as S.E.A. and B.A.S. respectively). Here we focus on the major findings. The two AMB muscles (Fig. 9) compare reasonably well among all three studies, showing a decrease of hip flexion moment arms at strongly flexed limb poses and in some cases (our AMB1,2 and the AMB of B.A.S.) a switch from flexor to extensor action with flexion (∼30–90°). The IC muscles likewise have reasonably comparable results, but only our IC muscle switches action at extreme flexion. Our model agrees well with the data of S.E.A. and especially B.A.S. for the IL muscle, including its decreasing hip extensor moment arm with increasing hip flexion and a switch from hip extensor to flexor action at typical in vivo positions (∼40–70°). We have similar findings for the ILFB muscle, although no switch to hip flexor moment arms is observed in either of the two parts of this muscle in our model (S.E.A. and B.A.S. represented it as one part) (Fig. 9).


Musculoskeletal modelling of an ostrich (Struthio camelus) pelvic limb: influence of limb orientation on muscular capacity during locomotion.

Hutchinson JR, Rankin JW, Rubenson J, Rosenbluth KH, Siston RA, Delp SL - PeerJ (2015)

Hip flexor/extensor moment arms plotted against joint angle for key proximal thigh muscles.See captions for Figs. 9 and 10.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4465956&req=5

fig-11: Hip flexor/extensor moment arms plotted against joint angle for key proximal thigh muscles.See captions for Figs. 9 and 10.
Mentions: Figures 9–11 show our results for hip flexion/extension moment arms of ostrich muscles, with comparable data from Smith et al. (2007) and Bates & Schachner (2012) also plotted if available (abbreviated in this section as S.E.A. and B.A.S. respectively). Here we focus on the major findings. The two AMB muscles (Fig. 9) compare reasonably well among all three studies, showing a decrease of hip flexion moment arms at strongly flexed limb poses and in some cases (our AMB1,2 and the AMB of B.A.S.) a switch from flexor to extensor action with flexion (∼30–90°). The IC muscles likewise have reasonably comparable results, but only our IC muscle switches action at extreme flexion. Our model agrees well with the data of S.E.A. and especially B.A.S. for the IL muscle, including its decreasing hip extensor moment arm with increasing hip flexion and a switch from hip extensor to flexor action at typical in vivo positions (∼40–70°). We have similar findings for the ILFB muscle, although no switch to hip flexor moment arms is observed in either of the two parts of this muscle in our model (S.E.A. and B.A.S. represented it as one part) (Fig. 9).

Bottom Line: Our two hypotheses relate to the control priorities that a large bipedal animal might evolve under biomechanical constraints to achieve more effective static weight support.However, some conspicuous areas of disagreement in our results illustrate some cautionary principles.Such a framework could remove obstacles impeding the analysis of muscle function in extinct taxa.

View Article: PubMed Central - HTML - PubMed

Affiliation: Structure and Motion Laboratory, Department of Comparative Biomedical Sciences, The Royal Veterinary College, University of London , Hatfield, Hertfordshire , United Kingdom ; Bioengineering Department, Stanford University , Stanford, CA , USA.

ABSTRACT
We developed a three-dimensional, biomechanical computer model of the 36 major pelvic limb muscle groups in an ostrich (Struthio camelus) to investigate muscle function in this, the largest of extant birds and model organism for many studies of locomotor mechanics, body size, anatomy and evolution. Combined with experimental data, we use this model to test two main hypotheses. We first query whether ostriches use limb orientations (joint angles) that optimize the moment-generating capacities of their muscles during walking or running. Next, we test whether ostriches use limb orientations at mid-stance that keep their extensor muscles near maximal, and flexor muscles near minimal, moment arms. Our two hypotheses relate to the control priorities that a large bipedal animal might evolve under biomechanical constraints to achieve more effective static weight support. We find that ostriches do not use limb orientations to optimize the moment-generating capacities or moment arms of their muscles. We infer that dynamic properties of muscles or tendons might be better candidates for locomotor optimization. Regardless, general principles explaining why species choose particular joint orientations during locomotion are lacking, raising the question of whether such general principles exist or if clades evolve different patterns (e.g., weighting of muscle force-length or force-velocity properties in selecting postures). This leaves theoretical studies of muscle moment arms estimated for extinct animals at an impasse until studies of extant taxa answer these questions. Finally, we compare our model's results against those of two prior studies of ostrich limb muscle moment arms, finding general agreement for many muscles. Some flexor and extensor muscles exhibit self-stabilization patterns (posture-dependent switches between flexor/extensor action) that ostriches may use to coordinate their locomotion. However, some conspicuous areas of disagreement in our results illustrate some cautionary principles. Importantly, tendon-travel empirical measurements of muscle moment arms must be carefully designed to preserve 3D muscle geometry lest their accuracy suffer relative to that of anatomically realistic models. The dearth of accurate experimental measurements of 3D moment arms of muscles in birds leaves uncertainty regarding the relative accuracy of different modelling or experimental datasets such as in ostriches. Our model, however, provides a comprehensive set of 3D estimates of muscle actions in ostriches for the first time, emphasizing that avian limb mechanics are highly three-dimensional and complex, and how no muscles act purely in the sagittal plane. A comparative synthesis of experiments and models such as ours could provide powerful synthesis into how anatomy, mechanics and control interact during locomotion and how these interactions evolve. Such a framework could remove obstacles impeding the analysis of muscle function in extinct taxa.

No MeSH data available.


Related in: MedlinePlus