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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

Maximal muscle moments about distal limb joints (ankle and metatarsophalangeal MTP), for representative walking and running trials (see ‘Methods’).See caption for Fig. 6.
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fig-7: Maximal muscle moments about distal limb joints (ankle and metatarsophalangeal MTP), for representative walking and running trials (see ‘Methods’).See caption for Fig. 6.

Mentions: Our 3D ostrich limb model predicted how the maximal capacity to generate muscle moments should vary with limb orientation during walking and running (Figs. 6 and 7). Maximal flexor moments increase if force–length properties are ignored (treating all muscles as isometric). This indicates that most muscles in the model are at disadvantageously short fibre lengths during locomotion, with walking having a generally greater capacity for flexor moment generation (especially about the hip) than running. These curves do not change much across the gait cycle. The pattern for extensor moments is more complex. Peak capacity tends to be in late swing phase (reasonably consistent across all joints). Force-length properties here provide an advantage, presumably because the muscles are lengthened. Data during the stance phase do not support the hypothesis, regardless of assumptions about muscle-force length states, that postures used around mid-stance of walking or running optimize the moment-generating capacity of pelvic limb muscles in ostriches: the maximal moments early or late in stance phase, and late in swing phase, are of similar or greater magnitudes. The relatively flattened shapes of most moment curves without force–length properties enforced (“Fmax”; dotted lines in Figs. 6 and 7) indicate that muscle moment arm variation across postures used in vivo during locomotion is a smaller contributor to moment generation than force–length properties (“F–L”; solid lines) in Struthio.


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)

Maximal muscle moments about distal limb joints (ankle and metatarsophalangeal MTP), for representative walking and running trials (see ‘Methods’).See caption for Fig. 6.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

fig-7: Maximal muscle moments about distal limb joints (ankle and metatarsophalangeal MTP), for representative walking and running trials (see ‘Methods’).See caption for Fig. 6.
Mentions: Our 3D ostrich limb model predicted how the maximal capacity to generate muscle moments should vary with limb orientation during walking and running (Figs. 6 and 7). Maximal flexor moments increase if force–length properties are ignored (treating all muscles as isometric). This indicates that most muscles in the model are at disadvantageously short fibre lengths during locomotion, with walking having a generally greater capacity for flexor moment generation (especially about the hip) than running. These curves do not change much across the gait cycle. The pattern for extensor moments is more complex. Peak capacity tends to be in late swing phase (reasonably consistent across all joints). Force-length properties here provide an advantage, presumably because the muscles are lengthened. Data during the stance phase do not support the hypothesis, regardless of assumptions about muscle-force length states, that postures used around mid-stance of walking or running optimize the moment-generating capacity of pelvic limb muscles in ostriches: the maximal moments early or late in stance phase, and late in swing phase, are of similar or greater magnitudes. The relatively flattened shapes of most moment curves without force–length properties enforced (“Fmax”; dotted lines in Figs. 6 and 7) indicate that muscle moment arm variation across postures used in vivo during locomotion is a smaller contributor to moment generation than force–length properties (“F–L”; solid lines) in Struthio.

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