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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: We find that ostriches do not use limb orientations to optimize the moment-generating capacities or moment arms of their muscles.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

Ostrich musculoskeletal model: wrapping surface examples.See Table 2 for muscle abbreviations. Lateral (A), craniolateral (B), and caudolateral (C) views of eight muscle wrapping objects (in blue), as half and whole cylinders, ellipses and a torus. The PIFML and ILFB wrapping surfaces are shown as meshes, for added clarity.
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fig-5: Ostrich musculoskeletal model: wrapping surface examples.See Table 2 for muscle abbreviations. Lateral (A), craniolateral (B), and caudolateral (C) views of eight muscle wrapping objects (in blue), as half and whole cylinders, ellipses and a torus. The PIFML and ILFB wrapping surfaces are shown as meshes, for added clarity.

Mentions: We used these anatomical data and bone images to construct a 3D musculoskeletal computer model of the right pelvic limb using SIMM software (Musculographics, Inc., Chicago, Illinois, USA; Delp et al., 1990; Delp & Zajac, 1992; Delp & Loan, 1995; Delp & Loan, 2000). The right limb was mirrored as a left limb. The digitized muscle paths were used as a template for developing the muscle paths in the final model (Figs. 3 and 4). Paths were represented using a combination of “via points” (i.e., static points fixed relative to a segment) and “wrapping surfaces” that prevented translation of points outside of a predefined area (see Delp & Loan, 1995; Delp & Loan, 2000 for details; also Hutchinson et al., 2005, for a similar procedure we used for Tyrannosaurus rex). Table 2 presents the muscles modelled, with abbreviations used throughout the paper. Table 3 describes all the muscle wrapping surfaces assumed in the model and Fig. 5 displays examples.


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)

Ostrich musculoskeletal model: wrapping surface examples.See Table 2 for muscle abbreviations. Lateral (A), craniolateral (B), and caudolateral (C) views of eight muscle wrapping objects (in blue), as half and whole cylinders, ellipses and a torus. The PIFML and ILFB wrapping surfaces are shown as meshes, for added clarity.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

fig-5: Ostrich musculoskeletal model: wrapping surface examples.See Table 2 for muscle abbreviations. Lateral (A), craniolateral (B), and caudolateral (C) views of eight muscle wrapping objects (in blue), as half and whole cylinders, ellipses and a torus. The PIFML and ILFB wrapping surfaces are shown as meshes, for added clarity.
Mentions: We used these anatomical data and bone images to construct a 3D musculoskeletal computer model of the right pelvic limb using SIMM software (Musculographics, Inc., Chicago, Illinois, USA; Delp et al., 1990; Delp & Zajac, 1992; Delp & Loan, 1995; Delp & Loan, 2000). The right limb was mirrored as a left limb. The digitized muscle paths were used as a template for developing the muscle paths in the final model (Figs. 3 and 4). Paths were represented using a combination of “via points” (i.e., static points fixed relative to a segment) and “wrapping surfaces” that prevented translation of points outside of a predefined area (see Delp & Loan, 1995; Delp & Loan, 2000 for details; also Hutchinson et al., 2005, for a similar procedure we used for Tyrannosaurus rex). Table 2 presents the muscles modelled, with abbreviations used throughout the paper. Table 3 describes all the muscle wrapping surfaces assumed in the model and Fig. 5 displays examples.

Bottom Line: We find that ostriches do not use limb orientations to optimize the moment-generating capacities or moment arms of their muscles.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