|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online June 29, 2007
Journal of Experimental Biology 210, 2548-2562 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02792
Running in ostriches (Struthio camelus): three-dimensional joint axes alignment and joint kinematics
1 School of Human Movement and Exercise Science, The University of Western
Australia, Crawley, WA, 6009, Australia,
2 Department of Orthopaedics, Stanford University, 341 Galvez St, Stanford,
CA 94305, USA
3 Fauna Technology, PO Box 558, Gosnells, WA, 6990, Australia
* Author for correspondence (e-mail: jrubenson{at}csupomona.edu)
Accepted 16 May 2007
 |
Summary |
|---|
 TOP Summary IntroductionMaterials and methodsResultsDiscussionAppendixReferences |
|---|
3.3 m
s–1) in the largest avian biped, the ostrich. Our analysis
revealed that the majority of the segment motion during running in the ostrich
occurs in flexion/extension. Importantly, however, the alignment of the
average flexion/extension helical axes of the knee and ankle are rotated
externally to the direction of travel (37° and 21°, respectively) so
that pure flexion and extension at the knee will act to adduct and adbuct the
tibiotarsus relative to the plane of movement, and pure flexion and extension
at the ankle will act to abduct and adduct the tarsometatarsus relative to the
plane of movement. This feature of the limb anatomy appears to provide the
major lateral (non-sagittal) displacement of the lower limb necessary for
steering the swinging limb clear of the stance limb and replaces what would
otherwise require greater adduction/abduction and/or internal/external
rotation, allowing for less complex joints, musculoskeletal geometry and
neuromuscular control. Significant rotation about the joints'
non-flexion/extension axes nevertheless occurs over the running stride. In
particular, hip abduction and knee internal/external and varus/valgus motion
may further facilitate limb clearance during the swing phase, and substantial
non-flexion/extension movement at the knee is also observed during stance.
Measurement of 3-D segment and joint motion in birds will be aided by the use
of functionally determined axes of rotation rather than assumed axes, proving
important when interpreting the biomechanics and motor control of avian
bipedalism.
Key words: kinematics, ostrich, bird, three-dimensional, locomotion, joint
|
Introduction |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionAppendixReferences |
|---|
;
Verstappen et al., 2000),
muscle function (Clark and Alexander,
1975; Roberts and Scales,
2004), neural and motor control
(Johnston and Bekoff, 1992;
Johnston and Bekoff, 1996;
Verstappen and Aerts, 2000),
ontogeny of locomotion (Muir et al.,
1996) and locomotor energetics
(Fedak et al., 1982;
Roberts et al., 1998;
Roberts and Scales, 2004;
Rubenson et al., 2004).
Hind-limb kinematics of birds has also been used to explore the evolution of
avian bipedalism and archosaur locomotion in general
(Gatesy and Biewener, 1991;
Gatesy, 1999;
Hutchinson and Gatesy, 2000),
and has been used to aid predictions of the locomotor abilities of extinct
bipedal taxa (Hutchinson,
2004).
A significant limitation of past kinematic studies, however, is the general
reliance on two-dimensional (2-D) planar analyses. Analyses in 2-D have been
found to be insufficient for understanding the movement of many terrestrial
species. This is particularly apparent in those animals with sprawled
postures, whose limb segments are not aligned in the sagittal plane [e.g.
lizards and crocodylians (Gatesy,
1991; Reilly and Elias,
1998; Irschick and Jayne,
1999; Jayne and Irschick,
1999]. The importance of incorporating three-dimensional (3-D)
kinematics is not restricted to sprawling gaits. Indeed, 3-D kinematics are
necessary for revealing fundamental aspects of human locomotion, many of which
have direct clinical application (Whittle,
1995), and some studies indicate that 3-D limb motions also occur
in running birds (Cracraft,
1971; Gatesy,
1999), although no comprehensive joint analyses during locomotion
have been undertaken.
Examination of human kinematics has revealed that not only limb posture,
but also the alignment of the joint axes, play an important role in
determining the 3-D nature of limb movements
(Piazza and Cavanagh, 2000;
Besier et al., 2003;
Most et al., 2004). Indeed,
Piazza and Cavanagh (Piazza and Cavanagh,
2000) illustrated that a small misalignment between the assumed
joint axes of rotation and the true axis about which rotation occurs can
result in considerable kinematic cross-talk [when one joint rotation (e.g.
adduction) is interpreted as another (e.g. flexion)].
Avian bipeds possess a relatively upright hind-limb posture, aligned
primarily in the sagittal plane. Birds have substantial limb displacement in
the frontal plane compared to humans, however, owing primarily to a more
abducted femur. The combined effect of limb posture and joint axes alignment
may result in significant 3-D hind-limb motion in birds that may hold
important information regarding the mechanics and neuromuscular control of
bipedal locomotion and its evolution
(Hutchinson and Gatesy, 2000;
Biewener, 2002).
In this paper we present full 3-D joint kinematic data of running in the largest avian biped, the ostrich (Struthio camelus). Ostriches were chosen because they are of comparable size to humans, thus facilitating the use of established 3-D gait techniques, and furthermore, because they allow comparisons between avian and human 3-D kinematics without the confounding effect of body mass. A comparison between humans and ostriches thus provides a unique opportunity to reveal general features of bipedal locomotion and those unique to human and avian bipeds (the two extant representatives of obligate bipedalism) that arise specifically from differences in limb structure.
The first aim of this paper was the development of a 3-D joint kinematic model of the ostrich hind limb from anatomical specimens. This model uses mathematically determined functional joint axes and centers of rotation to describe joint axis alignment and motion. The second aim involved incorporating this kinematic model to investigate the 3-D joint angles of the ostrich during running.
|
Materials and methods |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionAppendixReferences |
|---|
Model development
A five-segment, 17 degree-of-freedom (d.f.) kinematic model of the ostrich
hind limb was developed from anatomical specimens that can be reconstructed on
living animals using only 3-D anatomical landmark (AL) data. This model
included the pelvis/trunk, femur, tibiotarsus, tarsometatarsus and phalanges
segments, each modeled as a rigid body. The position and orientation of each
rigid segment in space was defined using segment-embedded anatomical
coordinate systems (ACSs) that reflect functionally relevant joint centers and
joint axes of rotation (Cappozzo et al.,
1995), and were used to describe 3-D joint motion.
The kinematic modeling involved three primary steps. First, anatomical coordinate systems were initially constructed on anatomical specimens because these could not readily be constructed from anatomical landmarks that are palpable on the living animal for several segments of the ostrich hind limb. This involved determining joint centers and functional joint axes of rotation using both dynamic trials (with the exception of the hip), whereby the limb segments were moved through their range of motion, and static trials for the collection of anatomical landmark data (see Table A1 in Appendix for AL definitions). This procedure also provided a basis for comparing the unloaded (passive) joint axes to those measured during running. Secondly, the computed anatomical coordinate systems from the anatomical specimen were expressed in a coordinate system that could be constructed on the live animal using palpable and projected anatomical landmarks (referred to here as technical anatomical coordinate systems, or TACSs). Finally, segment dimensions from the anatomical specimens were collected using anatomical landmarks that were easy to locate on the live animals, allowing scaling factors to be applied to the reconstruction of the anatomical coordinate systems on the live animals.
|
Static 3-D anatomical data and 3-D segment motion were collected using a six-camera VICON motion analysis system (Oxford Metrics, Oxford, UK). Cameras were strategically placed around the limb to minimize marker occlusion and maximize marker resolution. The intact limb, including the pelvis was positioned on a steel mesh stage that enabled each segment to be either fixed securely or to be moved through its range of motion. Three stainless steel self-tapping screws were placed into the femur, tibiotarsus, tarsometatarsus and phalanges in a non-collinear configuration onto which retro-reflective markers (20 mm) were placed. The placement of the screws required only minimal dissection of surrounding muscle tissue. The markers were used to construct rigid-body technical coordinate systems (TCSs) for these segments during both static and dynamic trials.
For static trials, anatomical landmarks were located using a five-marker pointer. Marker redundancy was used to reduce the error in locating the end of the pointer. During dynamic trials, the proximal segment was secured to the mesh stage whilst the distal segment was moved through its range of motion. Motion data of the markers was collected at 50 Hz with a resolution better than 2 mm. Segment motion was allowed to follow the natural path of the joint, and because the weight of the limbs could affect the joint posture, the dynamic trials were made with the stage positioned upright.
The functional flexion/extension axis of the knee, ankle and
metatrso-phalangeal joints were derived from motion data of the distal segment
with respect to the proximal segment. To achieve this, three cycles of
flexion/extension over the joints full range of motion were captured. Using a
custom-written MATLAB program (Mathworks Inc., Natick, MA, USA) the motion
data were filtered (fourth order zero-lag Butterworth low-pass filter) and the
distal markers expressed relative to the proximal technical coordinate system.
Instantaneous finite helical axes were calculated throughout the range of
motion using the singular value decomposition method
[(Spoor and Veldpaus, 1980;
Reinschmidt and van den Bogert,
1997); any 3-D rigid body motion can be explained by a rotation
about, and translation along, an axis known as the helical (or screw) axis]. A
mean helical axis was calculated for the joint relative to the proximal
segment's technical coordinate system and was used to define the functional
flexion/extension axis of the joint as per Besier et al.
(Besier et al., 2003). The
medial and lateral borders of the knee, ankle and metatarso-phalangeal joints
were then expressed relative to the proximal segment's technical coordinate
system, thereby creating a vector that described the width of the joint. The
knee, ankle and metatarso-phalangeal joint centers were subsequently defined
as the average of two points on the mean helical axis, these being: (1) the
intersection of the mean helical axis with a plane that was normal to the mean
helical axis that went through the midpoint of the vector describing the width
of the joint, and (2) the intersection of the mean helical axis with a plane
normal to the vector describing the width of the joint and going through the
midpoint of the this vector (Fig.
1).
|
;
Leardini et al., 1999), this
is not feasible for ostriches since the femur has a very small range of motion
(Gatesy and Biewener, 1991),
which can result in error (Piazza et al.,
2004). Instead, the hip joint center was defined statically. After
disarticulating the femur from the pelvis, the center of the head of the femur
(assumed to be the joint center) was identified relative to the femur
technical coordinate system. This was done by bisecting a vector defined by
two points on opposite sides of the head of the femur, which was assumed to
represent the diameter of the head of the femur. The segment anatomical coordinate systems for the femur, tibiotarsus, tarsometatarsus and phalanges were defined using the calculated joint centers and mean flexion/extension helical axes. The pelvis/trunk ACS was defined using the following anatomical landmarks: (1) the cranial aspect of the ilium, where it meets the sixth thoracic vertebrae (IL), (2) the caudal end of the prominent ridge on the midline of the dorsal aspect of the postacetabular ilium (SUL) and (3) the caudal end of the synsacrum where it meets the first tail vertebra (SYN). See the Appendix for details of the definition of the segment ACSs and Fig. 2 for a graphical representation of the segment ACSs.
|
|
Hip, knee, ankle and metatarso-phalangeal joint angle motions on the live
animals were computed using the kinematic model (constructed from the
laboratory limb segments) in BodyBuilder software (Oxford Metrics, Oxford,
UK). For comparison, knee and ankle joint angles were also computed from the
motion of the anatomical limb specimens in the laboratory trials. This was
achieved by re-constructing each segment's ACS using the optimized joint
flexion/extension axes and joint centers, as outlined above and in the
Appendix. The ACSs of the proximal and distal segments at each joint were used
to define the joint coordinate system, the set of three ordered joint angle
rotations as per the ISB standard (Grood
and Suntay, 1983; Wu and
Cavanagh, 1995). The first rotation was about the z-axis
of the proximal segment's ACS (the flexion/extension rotation; positive
rotation represented flexion and negative rotation represented extension). The
last rotation was about the y-axis of the distal segment's ACS (the
long-axis rotation; positive rotation represented internal rotation and
negative rotation represented external rotation). The middle rotation was
about a floating axis, which is perpendicular to first and last rotation axes
(the abduction/adduction rotation; positive rotation represented adduction and
negative rotation represented abduction). The zero joint angles occur when the
segments' ACSs lie in a straight line, except for the metatarso-phalangeal
joint, where zero flexion/extension occurs when the phalanges and
tarsometatarsus are perpendicular to one another, akin to the human ankle. It
should be noted that the joint coordinate system is generally
non-orthogonal.
On the live animals, pelvic segment angles were defined by the rotation of the pelvis ACS relative to the global coordinate system. Pelvic pitch was defined as the rotation about the z-axis of the segment, where a positive angle represents an upward pitch. Roll was defined as the rotation about the x-axis of the segment, where a positive angle represents a lateral (long-axis) rotation to the right. Yaw was defined as the rotation about the y-axis of the moving frame, where a negative angle represents an external rotation of the segment relative to the direction of travel (a rotation to the right).
Running kinematics
A 50-m long and 2-m wide fenced runway was constructed within the animal's
field. The runway was surfaced with high-density rubber matting (10 mm
thickness). Within a large enclosure, two 200 Hz synchronized high-speed video
cameras (Peak Performance; Centenial, CO, USA) were placed at a 45° angle
to the track. In order to provide suitable lighting for night trials, 2000 W
floodlighting was used behind each camera. A weatherproof tent housed the
video data acquisition system.
An 11-parameter, 83 d.f. direct linear transformation (DLT) was used to
construct a 3 m3 calibration volume from the two camera views
using Peak Motus software (Peak Performance; Centenial, CO, USA). The DLT was
calculated using a custom-built 48-point moveable calibration frame. The
average mean square error in the x-, y- and z-directions
from the DLT was 6.0, 3.0 and 5.0 mm, respectively, and the average percent
volume error was 0.19%. The video cameras were manually switched on when the
birds were viewed (on real-time monitors) commencing their run. The animal's
instantaneous running velocity was determined from the pelvis origin
throughout the calibrated volume. In order to help determine if the animal was
running at a steady speed before entering and after exiting the calibrated
volume, we used either visual markers that were spatially calibrated in the
horizontal direction only, or electronic timing gates, from which running
velocity was calculated over a 10 m distance either side of the center of the
calibrated volume. All data collections were performed after sunset under
artificial lighting, which permitted the use of retro-reflective markers that
improved marker location and also avoided high ambient day temperatures.
Performing trials at night also meant that the birds were, in general, more
amenable to experimentation than in daylight hours.
To determine the 3-D position and orientation of each segment during each running trial, clusters of retro-reflective markers (20 mm) were used to define TCSs. Marker clusters were attached to the pelvis, femur, tibiotarsus and tarsometatarsus, and a single marker was attached to the third phalanx of digit III (Fig. 3). In order to secure these markers to the animal and to ensure that they were visible during testing, the feathers surrounding the marker placements were removed and some wing feathers were clipped. The pelvis markers consisted of wands that were fit with two in-line markers. These wands were placed directly over the IL, SUL and SYN (Figs 2 and 3). The wand markers were attached to a rubber base and secured to the bird using double-sided tape. The femur cluster consisted of three non-co-linear markers mounted on a high-density foam base and secured to the skin using double-sided tape. For the tibiotarsus and tarsometatarsus, rubber cuffs containing four non-co-planar markers were fastened around the limb using double sided-tape and further secured using tape on the outside of the cuff.
|
Static calibration trials were used to locate the anatomical landmarks required to re-construct the segment anatomical coordinate systems. The animals were positioned in the center of the calibration volume and, with the exception of the pelvis, the anatomical landmarks were located using a six-marker pointer device similar to that used in the anatomical modeling and expressed relative to the respective TCS (Fig. 3). The pelvis anatomical landmarks were located directly from the in-line wand markers by projecting a known distance from the bottom marker along the vector defined by the two in-line markers. Since the wands pivoted about their respective anatomical landmarks, this system of defining the pelvis/trunk TCS had the advantage of not being greatly affected by marker movement.
The motion data of the limb marker clusters from the running trials also allowed for a direct calculation of optimized helical flexion/extension axes for the knee and ankle. The computed helical axes from the running trials were compared to those reconstructed from the kinematic model via static calibration trials.
Marker locations in the video footage were digitized using PEAK Motus software. The x-, y- and z-component of each marker trajectory was filtered using a fourth order zero-lag Butterworth low-pass filter. The filter cut-off frequency was set to within the range 4–12 Hz upon visual inspection of the filtered versus unfiltered data. The video data were appended to a single C3d `REAL' data file using C3d-Editor software (Motion Lab Systems, USA). From these files, the 3-D joint kinematics were computed using BodyBuilder modeling software, as described above.
Statistics
Six trials per animal were computed. Gait data were normalized to 100
points over one stride using a cubic spline interpolation to facilitate
compilation of multiple trials so that the mean ± standard deviation
(s.d.) of the kinematic curves could be determined.
|
Results |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionAppendixReferences |
|---|
3° valgus rotation and 4° external rotation.
Flexion at the ankle was coupled to adduction and internal rotation motion. A
70° increase in ankle flexion results in 5° adduction and 3°
internal rotation. It should be noted that the passive motion of the knee
joint was greatly affected when muscles surrounding the joint were dissected.
In trials where muscles crossing the knee had been removed the joint exhibited
substantially more non-flexion/extension movement and with a different pattern
to that when the musculature was left intact. For this reason, only trials
where the musculature surrounding the knee was kept intact were used in the
model construction.
|
|
Running spatio-temporal kinematics
When prompted to run, the birds selected a relatively narrow range of
speeds (2.5–4.0 m s–1), although some faster and
slower speeds were observed outside this range. The subset of strides used for
analysis in this study (3.29±0.30 m s–1; mean ±
s.d.) were chosen on the basis of their closeness in speed and whether they
maintained their running speed through the calibrated volume. The animals'
naturally chosen running speed was 3.3 m s–1 during our
experiments and, although much slower than their maximum running speed, this
speed is biomechanically and energetically representative of running in this
species (Rubenson et al.,
2004). Nevertheless, it is not certain whether the joint kinematic
patterns are necessarily the same at much faster running speeds. The animals
ran with a stride length of 2.32±0.25 m (mean ± s.d.) and a
stride frequency of 1.42±0.05 Hz (mean ± s.d.). Time of contact
and limb-swing time (of individual limbs) were 0.30±0.02 s and
0.40±0.04 s (mean ± s.d.), respectively, resulting in a duty
factor of 0.43±0.04 (mean ± s.d.).
Running segmental and joint kinematics
Pelvic roll exhibited small excursions, with an inconsistent pattern over
the running stride (Fig. 6A). A
pattern whereby the pelvis is rotated internally about its long axis during
the early part of the swing and rotated externally at the end of swing may be
present, although difficult to discern given the measurement variability.
Pelvic pitch had two excursions of up to 6° around a mean angle of
12.5° (Fig. 6B). The pelvic
pitch peaked at mid-swing and decreased until it reached a minimum just after
toe-strike. The pelvis pitched upwards until a second peak during mid-stance
and then decreased until it reached a second minimum shortly after toe-off.
The pelvis remained very stable in the yaw direction, fluctuating less than
1° from the neutral position throughout the gait cycle
(Fig. 6C).
|
10°). After toe-strike, the hip exhibits a brief
period of extension followed by flexion (5°) until reaching a maximum
flexion during mid-stance. The second half of the stance phase was
characterized by rapid hip extension until toe-off. The pattern of hip
adduction/abduction was similar to hip flexion/extension with a marginally
smaller joint excursion (9.5°) (Fig.
7B). During the swing phase, the hip was abducted. After
toe-strike the hip undergoes a small adduction/abduction movement until a
maximum hip abduction is reached during mid-stance. The hip then adducted
rapidly during the second half of stance until maximum hip adduction was
reached at toe-off. Little internal/external motion existed throughout most of
the stride (Fig. 7C). Towards
the end of the stance phase and the early part of swing, the hip rotated
internally followed by external rotation during the later half of swing,
returning to an apparent neutral position by toe-strike.
|
15°) and during the stance phase (10°)
(Fig. 8B). The varus/valgus
joint angle peaked just after toe-strike and reached a minimum during
mid-swing. Substantial internal/external rotation (20°) occurred at
the knee throughout the running stride
(Fig. 8C). Throughout most of
the stance phase the tibia rotated externally relative to the femur. Between
toe-off and mid-swing the knee continued to rotate externally, after which the
knee rapidly rotated internally up until toe-strike.
|
|
The metatarso-phalangeal joint exhibited the largest flexion/extension
excursion of all joints (Fig.
10A), but remained in an extended posture throughout the entire
stride. After toe-off the metatarso-phalangeal joint underwent extension, but
began to flex prior to mid-swing. The metatarso-phalangeal joint flexed
through the remainder of the swing phase and reached a maximum flexion angle
at the mid-point of the stance phase. During the second half of the stance
phase, the metatarso-phalangeal joint extended. The overall flexion and
extension excursions during the stance phase were 60° and
80°, respectively. The metatarso-phalangeal joint had little
internal/external rotation (toe-in/toe-out) during the majority of stance
(Fig. 10B). However, during
late stance there was 5° of rapid external rotation which continued
during the early part of the swing phase followed by internal rotation during
the latter half of swing.
|
|
Discussion |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionAppendixReferences |
|---|
Comparison to treadmill based ostrich locomotion
Previous kinematic data for ostrich locomotion are sparse and mostly
limited to spatio-temporal analyses of animals moving on a treadmill. The
subset of strides used for analysis in this study exhibited similar
spatio-temporal kinematics to those observed for ostriches running on a
motorized treadmill at the same speed
(Rubenson et al., 2004).
Stride frequency was 10% lower in the current study compared to that
observed previously (Rubenson et al.,
2004), whereas stride length was 10% greater. Contact time
differed little between these studies, but swing time was 19% longer in
over-ground running, which consequently resulted in a 14% difference in duty
factor. Much of the differences in stride parameters that exist compared to
those previously reported (Rubenson et
al., 2004) are likely due to differences in the size of the
experimental animals. The birds in the present analysis were slightly larger
and therefore expected to possess longer stride lengths and lower stride
frequencies. In support of this interpretation, Gatesy and Biewener reported
spatio-temporal kinematics from a 90 kg ostrich moving on a treadmill that
were similar to those observed in the present study
(Gatesy and Biewener, 1991).
Nevertheless, the longer strides and slower stride frequency observed in the
present study were the result of longer swing times but not longer
ground-contact times, possibly the result of differences in treadmill running
versus over-ground running in ostriches. A study of over-ground
locomotion in ratite species (Abourachid
and Renous, 2001) indicates that cursorial birds possess longer
contact times when moving on a treadmill, resulting in higher duty factors
compared to over-ground locomotion at similar speeds.
Comparison of flexion/extension kinematics to other avian bipeds and humans
The majority of the segment motion during running in the ostrich occurs in
flexion/extension, supporting the notion that bipedal locomotion in birds is
primarily achieved by sagittal plane movement. In general terms,
flexion/extension kinematics in the ostrich is similar to that of other bird
species. The small hip excursion in ostriches is consistent with other studies
of bird running (e.g. Gatesy and Biewener,
1991; Gatesy,
1999; Reilly,
2000). It is likely, however, that greater hip flexion/extension
occurs at faster running speeds. The pattern of hip flexion followed by
extension during stance is akin to that observed for running magpies
(Verstappen at al., 2000),
whereas other avian species such as chickens
(Johnston and Bekoff, 1992;
Johnston and Bekoff, 1996;
Muir et al., 1996), and guinea
fowl (Gatesy, 1999) and humans
(Novacheck, 1998) exhibit
primarily hip extension during stance. It is possible that the
flexion–extension countermovement observed at the hip is associated with
a stretch–shorten cycle of the muscle–tendon elements and may
contribute to storage and release of elastic energy. It is also interesting
that, unlike other bird species and humans, ostriches do not exhibit hip
extension at the end of the swing phase running at 3.3 m s–1.
The knee and ankle joints are therefore solely responsible for lowering the
toes to the ground before the next stance phase.
Sagittal plane pelvic movements (pelvic pitch) are relatively small and
have little influence over the hip flexion/extension angles. This pelvic pitch
pattern is similar to that observed for guinea fowl, also a terrestrial
species, albeit with larger fluctuations
(Gatesy, 1999). Other bird
species do not exhibit any clear pattern of pelvic pitch during running, e.g.
quail (Reilly, 2000) and
magpie (Verstappen et al.,
2000), perhaps reflecting a difference in cursoriality. The mean
pelvic pitch angle (12°) is considerably less than that of smaller bird
species such as guinea fowl, quail and magpie
(Gatesy, 1999;
Reilly, 2000;
Verstappen et al., 2000),
although guinea fowl do exhibit similar pitch angles during fast running
(Gatesy, 1999). The smaller
pelvic pitch angle in ostriches supports the idea that large non-avian
theropods (e.g. Tyrannosaurus rex) may have had a more horizontal
sacral orientation compared to the earlier, more upright reconstructions [for
a discussion on this topic see Gatesy
(Gatesy, 1999)].
The overall pattern of knee flexion/extension over the running stride is
similar to that of other bird species as well as that of human running. The
majority of the knee flexion/extension occurs during the swing phase in the
ostrich, whereby the knee contributes both to lifting the toes off the ground
at the beginning of the swing phase and to returning the toes towards the
ground for the initiation of the next stance phase. The knee has a similar
pattern of flexion/extension during the swing phase in humans
(Novacheck, 1998). In birds,
however, knee flexion/extension appears somewhat more variable, with some
studies on walking chicks reporting flexion followed by extension
(Johnston and Bekoff, 1992;
Johnston and Bekoff, 1996),
while others report only knee extension during the swing phase in chicks
(Muir et al., 1996), quail
(Reilly, 2000) and magpie
(Verstappen et al., 2000). The
pattern of knee flexion followed by knee extension during stance has been
observed in other smaller running birds
(Gatesy, 1999;
Verstappen et al., 2000) and
humans (Novacheck, 1998), and
may represent a strategy for storage and release of elastic energy and/or
damping of the ground reaction force.
The ankle undergoes a large flexion/extension excursion during the swing
phase and is the major joint responsible for repositioning the lower limb
segments during swing. Other studies on chickens
(Jacobsen and Hollyday, 1982),
the silver gull (Dagg, 1977)
and magpie (Verstappen et al.,
2000) have likewise shown that flexion/extension at the ankle
dominates the sagittal plane limb movements during the swing phase.
Interestingly, however, the ankle remains static throughout most of the stance
phase. The ankle joint has been regarded as a primary cite for elastic energy
storage and return in running birds via the gastrocnemius tendon
(e.g. Roberts et al., 1997).
The lack of a flexion/extension movement at the ankle during stance in
ostriches does not support this view, however, at least for the narrow range
of speeds examined in this study. Interestingly, studies on chickens
(Jacobsen and Hollyday, 1982;
Johnston and Bekoff, 1992) and
quail (Clark and Alexander,
1975) have also shown minimal flexion/extension during stance,
indicating that spring-like behavior at the ankle should not be generalized to
all birds over all running speeds.
The metatarso-phalangeal joint exhibits a very large flexion/extension
excursion, in particular during the swing phase. The flexion/extension
observed during the stance phase likely contributes to storage/release of
elastic strain energy in digital flexor tendons. These tendons are ideally
suited for storage/release of elastic energy owing to their small cross
sectional area and long length (80 cm). It should be pointed out that the
measured metatarso-phalangeal joint angle assumes a single phalanx segment and
does not take into consideration movement at the inter-phalangeal joints.
These joints likely undergo flexion/extension, especially during stance, and
accurate measurements of muscle–tendon strain will benefit from their
inclusion. For the purpose of this study a single segment is used to represent
the overall movement of the phalanges. Interestingly, it is the
metatarso-phalangeal joint rather than the ankle that likely provides the
majority of the elastic energy storage/release via the digital flexor
muscles (at least for the speeds examined in this study). In contrast, human
bipedal running exhibits an ankle-based elastic storage/release system
via the gastrocnemius muscles
(Fukunaga et al., 2002;
Lichtwark et al., 2007).
Further examination of metatarso-phalangeal and ankle mechanics in other
species will help reveal whether this represents a general difference in
locomotor strategies between avian and human bipedalism.
The extent to which the metatarso-phalangeal joint excursion is actively
mediated via muscle during the swing phase has been the topic of some
discussion (Verstappen et al.,
2000). Verstappen and colleagues raised the possibility that the
biarticular nature of the digital flexors and extensors (these also cross the
ankle) may facilitate passive joint motion during the swing phase. However,
while the action of the ankle may indeed transfer energy to move the phalanges
via two-joint muscles, these muscles may need to be active to produce
the required force, and would therefore still consume metabolic energy
(although not producing any mechanical work). During the stance phase, where
little ankle motion is present, strain in the muscle–tendon units
crossing the metatarso-phalangeal joint are expected to primarily account for
the movement of this joint.
Influence of flexion/extension axes alignment on 3-D kinematics
A critical feature of the ostrich knee and ankle joint anatomy that
drastically influences the interpretation of 3-D segment motion is the
alignment of their flexion/extension axes relative to the animal's direction
of travel (relative to the sagittal plane). While the flexion/extension axis
of the knee, and to a lesser extent the ankle, may shift throughout the
joints' range of motion, the average helical axes are rotated externally to
the direction of travel (see Fig.
5). This is evident not only from the average helical axes
reconstructed from the anatomical modeling, but from helical axes calculated
directly from the running trials (although these axes exhibit greater
variability compared to those reconstructed from the anatomical specimens). As
a result, pure flexion and extension at the knee will act to adduct and abduct
the tibiotarsus relative to the plane of movement, and pure flexion and
extension at the ankle will act to abduct and adduct the tarsometatarsus
relative to the plane of movement.
Knowledge of the axis alignment of the joints is thus clearly important for
interpreting locomotor kinematics and understanding how segment motion is
controlled. In 2-D planar analyses it is often assumed that the
flexion/extension axes of the joints lie perpendicular to the sagittal plane.
In this situation, segment motion in the frontal plane may be erroneously
interpreted as adduction/abduction at the level of the joint, or
alternatively, what has been measured as joint flexion/extension in a sagittal
plane analysis may actually incorporate rotation about non-flexion/extension
axes (Gard et al., 1996). In
3-D analyses, joint kinematics are often based on joint axes constructed from
anatomical landmarks (Cappozzo et al.,
1995; Wu et al.,
2002). For instance, many studies define the flexion/extension
axis of the human knee from the medial and lateral femoral condyles (e.g.
Cappozzo, 1995;
Lucchetti et al., 1998).
However, the actual flexion/extension axes can differ from these anatomical
axes. As in 2-D analyses, misalignment of the flexion/extension axes results
in kinematic cross-talk, where rotation about one axis is interpreted as
rotation about another. In 3-D studies of human locomotion substantial
kinematic cross-talk has been observed at the hip, knee and ankle depending on
the alignment of flexion/extension axes
(Kadaba et al., 1990;
Piazza and Cavanagh, 2000;
Marin et al., 2003;
Besier et al., 2003). In the
ostrich the average helical axes of the knee and ankle differ substantially
from the assumed axes of rotation based on the medial and lateral borders of
the joints (the medial and lateral femoral condyles and the medial and lateral
base of the tarsometatarsus, respectively). Although we did not specifically
quantify the degree of kinematic cross-talk that would result from using axes
based on these anatomical landmarks, it is clear that this approach would
substantially affect the rotations about all three axes at these joints.
In light of these observations the non-sagittal limb movements observed in the ostrich result, in large part, from flexion/extension at the level of the joint. Most notable is the motion of the tarsometatarsus during the swing phase. Because the ankle's flexion/extension axis is rotated externally relative to the sagittal plane (partly due to the orientation of the knee's flexion/extension axis that rotates the tibia externally), when the ankle flexes after toe-off the tarsometatarsus is abducted away from the body. This abduction is considerably larger than that of human running, as can be seen by a lateral displacement of the phalanx marker of 20 cm from toe-off to mid-swing. The segment is subsequently adducted back towards the body's centerline with ankle extension during the second half of the swing phase. Non-sagittal displacement of the tarsometatarsus is, therefore, not the result of adduction/abduction at the level of the joint, but rather due to the orientation of the ankle joint flexion/extension axis.
These 3-D features of the joint kinematics may also exist in other avian
species. In an anatomical study of pigeon, a diagonal orientation of the
knee's articulating surfaces that resulted in substantial
`lateral–medial swing' (abduction/adduction of the tibiotarsus) was
described (Cracraft, 1971).
This non-sagittal motion in the pigeon tibiotarsus thus appears to occur as a
result of a rotated knee flexion/extension axis (relative to the sagittal
plane). Furthermore, similar non-sagittal limb movements to those of the
ostrich have been observed in running guineafowl; the tibiotarsus and
tarsometatarsus have been reported to adduct relative to the animal's line of
travel during stance and the tarsometatarsus exhibits an
abduction–adduction pattern during swing
(Gatesy, 1999). It is possible
that these segment motions also result from the alignment of the
flexion/extension axis of their knee and ankle. At least in the ostrich, this
characteristic of the joint anatomy appears to provide the major lateral
displacement of the lower limb necessary for steering the swinging limb clear
of the stance limb and may be a general feature of the avian limb.
Non-flexion/extension kinematics
Although the majority of joint motion in the ostrich occurs about the joint
flexion/extension axes, it is evident that 3-D segment motion in this species
depends also on rotations about the joints' adduction/abduction and
internal/external rotation axes. For instance, hip abduction and adduction
during the stance phase has similar magnitude to the joint flexion/extension
range of motion, and during the swing phase the hip exhibits a similar
magnitude of abduction as flexion. This may reflect an equal requirement of
this joint to provide the lateral displacement of the limb and to swing the
limb forward. Interestingly, abduction at the hip will increase the degree of
external rotation of the ankle flexion/extension axis by rotating the entire
limb about the cranial axis (due to the horizontal posture of the femur). This
results in greater abduction of the lower limb that is coupled to ankle
flexion.
The requirement for hip abduction during the swing phase may stem in part
from the minimal pelvic yaw that could otherwise aid in abducting the limb
segments and provide clearance between the swing and stance limbs. In this
regard, it is interesting to note that the magnitude of hip abduction is
similar to that observed for guineafowl
(Gatesy, 1999), a species that
also exhibits little pelvic yaw when running. Other `waddling' species (e.g.
ducks, penguins) exhibit considerable pelvic yaw and roll, in part to position
the body center of mass over the stance foot. Further studies incorporating
3-D joint kinematics are required to reveal whether waddling bird species also
exhibit substantial joint adduction/abduction to provide limb clearance and
balance, or whether limb adduction/abduction and waddling represent two
distinct strategies for avian bipedal locomotion.
Throughout the stride the femur is in an externally rotated orientation relative to the pelvis. However, the results from this study suggest that little internal/external rotation occurs at the hip, although some internal rotation may exist during late stance and the early part of the swing phase. It is important to note, however, that the hip internal/external rotation exhibited large variability between the animals and between separate trials of the same animal, possibly reflecting limitations in the measurement techniques. The calculation of long-axis femur rotation assumed that the external femur marker cluster represented the underlying limb movement. Because the markers cannot easily be secured around the thigh segment on ostriches, some long-axis rotation may occur underneath the marker cluster. More accurate calculation of femoral rotation in this species may require cineradiography techniques or the use of bone pins secured directly to the femur.
The magnitude of the knee's varus/valgus and internal/external range of
motion are similar to studies on human locomotion
(Lafortune et al., 1992). The
knee exhibits a surprisingly similar varus/valgus pattern to that found in
human walking, whereby the knee undergoes a valgus–varus excursion both
during the stance phase and during the swing phase
(Besier et al., 2003), albeit
with a slightly greater range of motion compared to humans. During human
running, however, the knee has been found to undergo a small
valgus–varus–valgus excursion during stance
(Ferber et al., 2003). Given
the bow-legged frontal plane limb posture in ostriches, the increase in the
valgus joint angle during stance was unexpected, since it is likely that the
forces at the knee tend to adduct it at this time. The magnitude of knee
internal/external rotation is only moderately greater in ostriches compared to
humans, although during stance the ostrich knee rotates externally, compared
to the internal rotation found in humans. During swing, external rotation
followed by internal rotation is evident in both humans and ostriches.
Given that valgus and external tibial rotation were coupled to knee
flexion, and that varus and internal tibial rotation were coupled to knee
extension in the unloaded ostrich knee, it is possible that similar coupling
occurs during running as a result of joint architecture and ligamentous
constraints at the knee. Interestingly, similar coupled motions have been
reported in the ostrich and pigeon knee joint
(Cracraft, 1971;
Fuss, 1996), and are thought
to be controlled by ligamentous constraints and the shape of the
meniscus-fibular and condyle surfaces
(Cracraft, 1971;
Fuss and Gasser, 1992;
Fuss, 1996). It should be
noted that the internal tibiotarsus rotation, coupled with external femur
rotation during knee flexion reported in Fuss
(Fuss, 1996), is represented
by valgus rotation in the present study due to the definition of the knee
joint coordinate system. These coupled motions are commonly referred to as
`screw-home' motion and are also a characteristic feature of the human knee
joint (Markolf et al., 1976;
Wilson et al., 2000). The
magnitude of the varus/valgus and internal/external motion was, however,
considerably greater in running ostriches compared to the in situ
analyses, suggesting that the joint path could be exaggerated under load. It
is also possible that the coupled joint motions observed at the knee are, in
part, the result of kinematic cross-talk. Using functionally derived axes,
such as those applied in this study, should minimize kinematic cross-talk
(Besier et al., 2003). However,
when the flexion/extension axis of rotation shifts throughout the joint range
of motion, the average flexion/extension axis is not representative of the
true axis at all joint angles and kinematic cross-talk may result. Whether the
observed non-flexion/extension motion observed at the knee during running
should be regarded as true varus/valgus and internal/external rotation, or
whether it is the result of a rotating flexion–extension axis is
therefore debatable. In the latter case, little or no varus/valgus and
internal/external rotation outside of the knee's `neutral' position would have
been calculated over the range of flexion/extension angles, although the
rotation of the axis would itself cause the tibiotarsus to rotate
substantially within the current joint coordinate system axes. Finally, it
should not be ruled out that errors in varus/valgus rotation at the knee
propagate from errors in calculating internal/external rotation of the
femur.
Although the three-dimensional kinematics of the knee joint are complex and not fully understood, there are aspects that can be viewed in a functional context. In this regard it is perhaps easier to interpret the swing phase of running. Here, external rotation and valgus motion during the early and middle part of the swing phase, respectively, aid in abducting the lower limb segments away from the centerline, thereby improving the clearance between the swing and stance limb. Subsequently, the large varus motion and internal rotation during the end of the swing phase contributes to returning the phalanges underneath the body prior to toe-strike.
The lack of substantial ankle adduction/abduction and internal/external
rotation during the stance phase is consistent with the view that the ankle in
birds is a simple hinge joint (Clark and
Alexander, 1975) and also reflects the static nature of the ankle
joint during stance. However, during swing the ankle exhibits moderate
non-flexion/extension rotations. These rotations seem unlikely, given the
traditional notion of the ankle as a hinge joint and since the unloaded joint
excursion indicates that external rotation is coupled to ankle flexion rather
than ankle extension. Ankle joint kinematics may be different under load, when
the joint compressive force and muscle moments have an influence. In this
case, the function of the adduction and long-axis rotation of the
tarsometatarsus at the end of swing may align the phalanges in the plane of
movement prior to toe-strike, a motion that may be required given that the
tarsometatarsus is itself not aligned in this plane. The notion that
considerable non-flexion/extension motions occurs at the avian ankle joint is
also supported by a study on pigeon
(Cracraft, 1971), where as much
as 50° internal/external rotation and 15° abduction/adduction were
reported to exist in anatomical specimens.
The non-flexion/extension rotation at the ankle may also be due to systematic measurement error. Although no such error is obvious, kinematic cross-talk or systematic movement of the tarsometatarsus marker cluster may play a role. The prominent internal/external rotation of the metatarso-phalangeal joint during the end of stance and through the swing phase was also unexpected, considering this joint is also primarily a hinge joint. This result may be due to the placement of the phalanx marker that did not completely isolate movement of the inter-phalangeal joints, and thus any lateral displacement of the phalanges could influence the internal/external rotation angle. It is also possible that the calculated flexion/extension axis differed slightly from the true axis, resulting in kinematic cross-talk.
Implications for avian bipedal biomechanics
The current study adopted techniques developed in 3-D human gait analysis
in the study of avian bipedal gait. Amongst the most central findings arising
from this study is the discrepancy between the alignment of the joint axes of
rotation assumed in 2-D analyses (parallel with frontal plane) and those
calculated in 3-D. This observation not only influences measurements of 3-D
joint kinematics and interpretation of 3-D segment motion, but has important
implications for other aspects of avian bipedal biomechanics. For instance,
axis misalignment has the potential to alter calculations of net joint moments
and muscle moment arms about joint axes, which can lead to subsequent errors
in calculating joint mechanical power or when decomposing net joint moments
into lumped muscle forces or individual muscle forces using optimization
modeling. These errors would be expected to alter conclusions regarding the
motor control of locomotion as well as conclusions regarding
mechanical/muscular efficiency and the metabolic cost of producing muscle
force. Further work is required to address this issue.
The current study shows how these potential errors can be minimized in 3-D analyses of locomotor biomechanics in birds. Although the reconstructions of the ACSs depend on relatively simple geometric scaling between the live animal and anatomical specimens, the modeling techniques used here provide greater accuracy than more simple identification of joint centers and axes; the errors in predicting the joint center locations between two anatomical specimens were within 15 mm in nearly all the TACS axes and approach the digitizing error of the kinematic data acquisition used in the running trials. Similar anatomical modeling can be applied to other bipedal species using suitable anatomical landmark data, or by combining methods described in the present study with x-ray data, or alternatively, the sacrifice of the experimental animal for validation of landmark location may be desired. For small species, the methods outlined can be adopted in x-ray cinematography to provide superior identification of the skeletal features used in constructing the kinematic model.
Finally, our results illustrate that locomotion in avian bipeds is a complex, 3-D task requiring coordination of more than just flexion/extension of the joints. A good example of this level of complexity is seen during the swing phase, where abduction at the hip, varus/valgus and internal/external rotation at the knee and flexion/extension at the ankle may all contribute to abducting the swing limb away from the stance limb and repositioning the phalanges under the body prior to the next toe-strike. Interestingly, the alignment of the ankle flexion/extension axis in birds may replace what would otherwise require adduction/abduction and/or internal/external rotation, allowing for a less complex joint, musculoskeletal geometry and neuromuscular control. These findings may provide valuable clues into the relationships between avian bipedal musculoskeletal structure and function, and its evolution.
|
Appendix |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionAppendixReferences |
|---|
Definition of segment anatomical coordinate systems (ACSs) and joint motion
The segment anatomical coordinate systems are right-handed Cartesian
coordinate systems defined either from palpable anatomical landmarks (pelvis)
or the joint centers and joint flexion/extension helical axes (femur,
tibiotarsus, tarsometatarsus and phalanges). The joint centers and helical
axes are located from their position within the TACSs, expressed relative to
their scaling factors (see Table
A2). The definitions of the ACSs are listed below (for definitions
of the landmark abbreviations, see Table
A1).
Reconstruction sequence for the anatomical coordinate systems
The anatomical coordinate systems on the live animal were reconstructed
from a series of spatial transformations based on the anatomical landmark data
collected during the static calibration trials. First, the pelvis anatomical
landmarks were used to define the pelvis/trunk ACS, and with the use of each
bird's pelvic scaling factors the location of the HJC was estimated. After the
HJC was transposed into the femur TCS, the femur TACS and scaling factor could
be defined, from which the femur ACS could be reconstructed, which included
the knee joint center (KJC) and the knee helical flexion/extension axis. After
this, the KJC from the femur ACS was transposed into the tibiotarsus TCS so
that the tibia TACS and scaling factor could be defined, from which the tibia
ACS was reconstructed. A transformation matrix of the femur's ACS relative to
the tibiotarsus TACS allowed the KJC to be located from both the femur and
tibiotarsus TACS. The tarsometatarsus TACS and scaling factor were defined
directly from the ALs located with the pointer, allowing reconstruction of the
tarsometatarsus ACS. Finally, the phalanges ACS was constructed from the ALs
of the tarsometatarsus and the phalanx marker. These spatial transformations
made it possible to reconstruct each segment ACS from the motion data of the
segment marker clusters across running strides.
|
Acknowledgments |
|---|
|
References |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionAppendixReferences |
|---|
Abourachid, A. and Renous, S. (2001). Bipedal locomotion in ratites (Paleognatiform): examples of cursorial birds. Ibis 142,538 -549.
Besier, T. F., Sturnieks, D. L., Alderson, J. A. and Lloyd, D. G. (2003). Repeatability of gait data using a functional hip joint centre and a mean helical knee axis. J. Biomech. 36,1159 -1168.[CrossRef][Medline]
Biewener, A. A. (2002). Future directions for the analysis of musculoskeletal design and locomotor performance. J. Morphol. 252,38 -51.[CrossRef][Medline]
Cappozzo, A. (1984). Gait analysis methodology. Hum. Mov. Sci. 3,27 -54.[CrossRef]
Cappozzo, A., Catani, F., Della Croce, F. and Leardini, A. (1995). Position and orientation in space of bones during movement: anatomical frame definition and determination. Clin. Biomech. 10,171 -178.[CrossRef][Medline]
Clark, J. and Alexander, R. M. (1975). Mechanics of running by quail (Coturnix). J. Zool. Lond. 176,87 -113.
Cracraft, J. (1971). The functional morphology of the hind limb of the domestic pigeon, Columba livia. Bull. Am. Nat. Hist. 144,171 -268.
Dagg, A. L. (1977). The walk of the silver gull (Larus novaehollandiae) and of other birds. J. Zool. Lond. 182,529 -540.
Fedak, M. A., Heglund, N. C. and Taylor, C. R.
(1982). Energetics and mechanics of terrestrial locomotion. II.
Kinetic energy changes of the limbs and body as a function of speed and body
size in birds and mammals. J. Exp. Biol.
97, 23-40.
Ferber, R., Davis, I. M. and Williams, D. S., 3rd (2003). Gender differences in lower extremity mechanics during running. Clin. Biomech. 18,350 -357.[CrossRef][Medline]
Fukunaga, T., Kawakami, Y., Kubu, K. and Kanehisa, H. (2002). Muscle and tendon interaction during human movements. Exerc. Sports. Sci. Rev. 30,106 -110.[CrossRef]
Fuss, F. K. (1996). Tibiofibular junction of the South African ostrich (Struthio camelus australis). J. Morphol. 227,213 -226.[CrossRef]
Fuss, F. K. and Gasser, C. R. (1992). Cruciate ligaments of the avian knee: insights into a complex system. J. Morphol. 214,139 -151.[CrossRef]
Gard, S. A., Knox, E. H. and Childress, D. S. (1996). Two-dimensional representation of three-dimensional pelvic motion during walking: an example of how projections can be misleading. J. Biomech. 29,1387 -1391.[CrossRef][Medline]
Gatesy, S. M. (1991). Hind limb movements of the American alligator (Alligator mississippiensis) and postural grades. J. Zool. Lond. 224,577 -588.
Gatesy, S. M. (1999). Guineafowl hind limb function. I: Cineradiographic analysis and speed effects. J. Morphol. 240,115 -125.[CrossRef]
Gatesy, S. M. and Biewener, A. A. (1991). Bipedal locomotion: effects of speed, size and limb posture in birds and humans. J. Zool. Lond. 224,127 -147.
Grood, E. S. and Suntay, W. J. (1983). A joint coordinate system for the clinical description of three-dimensional motions: application to the knee. J. Biomech. Eng. 105,136 -144.[Medline]
Hutchinson, J. R. (2004). Biomechanical modeling and sensitivity analysis of bipedal running ability. II. Extinct taxa. J. Morphol. 262,441 -461.[CrossRef][Medline]
Hutchinson, J. R. and Gatesy, S. M. (2000).
Adductors, abductors, and the evolution of archosaur locomotion.
Paleobiology 26,734
-751.
Irschick, D. J. and Jayne, B. C. (1999). Comparative three-dimensional kinematics of the hindlimb for high-speed bipedal and quadrupedal locomotion of lizards. J. Exp. Biol. 202,1047 -1065.[Abstract]
Jacobsen, R. D. and Hollyday, M. (1982). A
behavioral and electromyographic study of walking in the chick. J.
Neurophysiol. 48,238
-256.
Jayne, B. C. and Irschick, D. J. (1999). Effects of incline and speed on three-dimensional hindlimb kinematics of a generalized iguanian lizard (Dipsosaurus dorsalis). J. Exp. Biol. 202,143 -159.[Abstract]
Johnston, R. M. and Bekoff, A. (1992).
Constrained and flexible features of rhythmical hindlimb movements in chicks:
kinematic profiles of walking, swimming and airstepping. J. Exp.
Biol. 171,43
-66.
Johnston, R. M. and Bekoff, A. (1996). Patterns of muscle activity during different behaviors in chicks: implications for neural control. J. Comp. Physiol. A 179,169 -184.[Medline]
Kadaba, M. P., Ramakrishnan, H. K. and Wootten, M. E. (1990). Measurement of lower extremity kinematics during level walking. J. Orthop. Res. 8, 383-392.[CrossRef][Medline]
Lafortune, M. A., Cavanagh, P. R., Sommer, H. J., 3rd and Kalenak, A. (1992). Three-dimensional kinematics of the human knee during walking. J. Biomech. 25,347 -357.[CrossRef][Medline]
Leardini, A., Cappozzo, A., Catani, F., Toksvig-Larsen, S., Petitto, A., Sforza, V., Cassanelli, G. and Giannini, S. (1999). Validation of a functional method for the estimation of hip joint center of location. J. Biomech. 32, 99-103.[CrossRef][Medline]
Lichtwark, G. A., Bougoulias, K. and Wilson, A. M. (2007). Muscle fascicle and series elastic element length changes along the length of the human gastrocnemius during walking and running. J. Biomech. 40,157 -164.[CrossRef][Medline]
Lucchetti, L., Cappozzo, A., Cappello, A. and Della Croce, U. (1998). Skin movement artefact assesment and compensation in the estimation of knee joint kinematics. J. Biomech. 31,977 -984.[CrossRef][Medline]
Marin, F., Mannel, H., Claes, L. and Durselen, L. (2003). Correction of axis misalignment in the analysis of knee rotations. Hum. Mov. Sci. 22,285 -296.[CrossRef][Medline]
Markolf, K. L., Mensch, J. S. and Amstutz, H. C.
(1976). Stiffness and laxity of the knee: the contributions of
the supporting structures. A quantitative in vitro study. J. Bone
Joint Surg. Am. 58,583
-594.
Most, E., Axe, J., Rubash, H. and Li, G. (2004). Sensitivity of the knee joint kinematics calculation to selection of flexion axes. J. Biomech. 37,1743 -1748.[CrossRef][Medline]
Muir, G. D., Gosline, J. M. and Steeves, J. D.
(1996). Ontogeny of bipedal locomotion: walking and running in
the chick. J. Physiol.
493,589
-601.
Novacheck, T. F. (1998). The biomechanics of running. Gait Posture 7,77 -95.[CrossRef][Medline]
Piazza, S. J. and Cavanagh, P. R. (2000). Measurement of the screw-home motion of the knee is sensitive to errors in axis alignment. J. Biomech. 33,1029 -1034.[CrossRef][Medline]
Piazza, S. J., Erdemir, A., Okita, N. and Cavanagh, P. R. (2004). Assessment of the functional method of hip joint center location subject to reduced range of hip motion. J. Biomech. 37,349 -356.[CrossRef][Medline]
Reilly, S. M. (2000). Locomotion in the quail (Coturnix japonica): the kinematics of walking and increasing speed. J. Morphol. 243,173 -185.[CrossRef][Medline]
Reilly, S. M. and Elias, J. A. (1998). Locomotion in Alligator mississippiensis: kinematic effects of speed and posture and their relavance to the sprawling-to-erect paradigm. J. Exp. Biol. 201,2559 -2574.[Abstract]
Reinschmidt, C. and van den Bogert, A. J. (1997). KineMat: a MATLAB Toolbox for Three-dimensional Kinematic Analysis. Calgary: Human Performance Laboratory, University of Calgary.
Roberts, T. J. and Scales, J. A. (2004).
Adjusting muscle function to demand: joint work during acceleration in wild
turkeys. J. Exp. Biol.
207,4165
-4174.
Roberts, T. J., Marsh, R. L., Weyand, P. G. and Taylor, C.
R. (1997). Muscular force in running turkeys: the economy of
minimizing work. Science
275,1113
-1115.
Roberts, T. J., Chen, M. S. and Taylor, C. R. (1998). Energetics of bipedal running. II. Limb design and running mechanics. J. Exp. Biol. 201,2753 -2762.[Abstract]
Rubenson, J., Heliams, D. B., Lloyd, D. G. and Fournier, P. A. (2004). Gait selection in the ostrich: mechanical and metabolic characteristics of walking and running with and without an aerial phase. Proc. R. Soc. Lond. B Biol. Sci. 271,1091 -1099.[Medline]
Spoor, C. W. and Veldpaus, F. E. (1980). Rigid body motion calculated from spatial co-ordinates of markers. J. Biomech. 13,391 -393.[CrossRef][Medline]
Verstappen, M. and Aerts, P. (2000). Terrestrial locomotion in the black-billed magpie. I. Spatio-temporal gait characteristics. Motor Control 4, 150-164.[Medline]
Verstappen, M., Aerts, P. and Van Damme, R. (2000). Terrestrial locomotion in the black-billed magpie: kinematic analysis of walking, running and out-of-phase hopping. J. Exp. Biol. 203,2159 -2170.[Abstract]
Whittle, M. W. (1995). Musculoskeletal applications of three-dimensional analysis. In Three-dimensional Analysis of Human Movement (ed. P. Allard, I. A. F. Stokes and J. Blanchi), pp. 295-310. Champaigne, IL: Human Kinetics.
Wilson, D. R., Feikes, J. D., Zavatsky, A. B. and O'Connor, J. J. (2000). The components of passive knee movement are coupled to flexion angle. J. Biomech. 33,465 -473.[CrossRef][Medline]
Wu, G. and Cavanagh, P. R. (1995). ISB recommendations for standardization in the reporting of kinematic data. J. Biomech. 28,1257 -1261.[CrossRef][Medline]
Wu, G., Siegler, S., Allard, P., Kirtley, C., Leardini, A., Rosenbaum, D., Whittle, M., D'Lima, D. D., Cristofolini, L., Witte, H. et al. (2002). ISB recomendation on definitions of joint coordinate system of various joints for the reporting of human joint motion – part I: ankle, hip, spine. J. Biomech. 35,543 -548.[CrossRef][Medline]
CiteULike 
Complore 
Connotea 
Del.icio.us 
Digg 
Reddit 
Technorati 
Twitter What's this?
This article has been cited by other articles:
|
|
 |
|
  C. M. Pace and A. C. Gibb Mudskipper pectoral fin kinematics in aquatic and terrestrial environments J. Exp. Biol., July 15, 2009; 212(14): 2279 - 2286. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Ren, M. Butler, C. Miller, H. Paxton, D. Schwerda, M. S. Fischer, and J. R. Hutchinson The movements of limb segments and joints during locomotion in African and Asian elephants J. Exp. Biol., September 1, 2008; 211(17): 2735 - 2751. [Abstract] [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
