Hindlimb function in the alligator: integrating movements, motor patterns, ground reaction forces and bone strain of terrestrial locomotion
1 Department of Biological Sciences, Ohio University, Athens, OH 45701,
USA
2 Department of Biological Sciences, Clemson University, Clemson, SC 29634,
USA
3 Department of Biomedical Sciences, Ohio University College of Osteopathic
Medicine, Athens, OH 45701, USA
* Author for correspondence (e-mail: reilly{at}ohiou.edu)
Accepted 21 December 2004
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Summary |
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Key words: locomotion, kinematics, kinetics, bone strain, motor patterns, alligator
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Introduction |
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Though torsional loads are clearly present in the limb bones of the
non-parasagittal species that have been tested, the underlying causes of this
torsion remain to be clarified. In the few vertebrates that have been found to
exhibit strong torsional loading of limb bones (e.g. walking chickens, flying
bats and birds; Pennycuick,
1967; Swartz et al.,
1992
; Biewener and Dial,
1995
; Carrano,
1998
), these torsional loads are believed to be induced by
locomotor forces acting at a distance from the long axis of the limb bone
which, therefore, generate a torsional moment. In species using
non-parasagittal terrestrial locomotion, two different forces are likely to
act at a distance from limb bone long axes and potentially contribute to
torsional moments. First, because species using non-parasagittal locomotion
hold their limbs out to the side of the body for much of limb support, the
ground reaction force (GRF) will be directed either anterior or posterior to
the long axis of limb bones for most of the step in these animals (Blob and
Biewener, 1999
,
2001
). At the same time, the
GRF will be directed more nearly perpendicular to the femur of
non-parasagittal animals than it will be in parasagittal animals. As a result,
the GRF will tend to rotate limb bones about their long axis in these species,
contributing to torsional loading. Second, the major limb retractor muscle in
many non-parasagittal species (including alligators and iguanas) is the
caudofemoralis longus (CFL), which inserts on the ventral surface of the
proximal femur (Snyder, 1962
;
Reilly, 1995
;
Gatesy, 1997
). When this
muscle contracts to retract the leg during the stance phase of locomotion, it
acts at a distance from the long axis of the femur equal to the radius of the
bone, and this distance is a moment arm for long axis rotation of the femur.
Thus, contraction of CFL should produce inward (medial) rotation of the femur
and torsional loading.
Though both mechanisms for the induction of torsion are viable, the relative contributions of each (and their potential interactions) are uncertain. As a result, it is difficult to predict whether torsion should be expected to predominate in the limb bones of all species that use non-parasagittal limb movements or whether specific differences in limb movements or mechanics might lead to alternative expectations for some lineages. To evaluate the contributions of these mechanisms to torsional loading of limb bones during locomotion, several types of data must be integrated, including information on limb position and movements, locomotor forces, muscular action and bone loading. The integration of such diverse sets of data is crucial not only for a complete understanding of bone loading mechanics, but also, ultimately, for a thorough understanding of the functional dynamics of how animals control forward propulsion with their limbs. Data on locomotor dynamics are available for only a narrow range of vertebrate taxa. Though studies focusing on multiple levels of analysis have provided major insights into propulsive dynamics in tetrapods, most studies have focused on animals with erect postures (cursorial mammals, primates) and, in particular, bipedal species (kangaroos, birds, humans). To date, no study has combined analyses of locomotor forces, limb bone loads, motor patterns, kinematics and foot fall patterns to evaluate how a non-erect quadrupedal animal supports its body weight and generates propulsive forces with its limbs.
In this study, we present an integrative analysis of propulsive dynamics in
the hindlimb of the American alligator (Alligator mississippiensis
Daudin). By integrating data on limb forces, bone loads, kinematics and motor
patterns, we are able to evaluate specific questions about locomotor mechanics
in this species. In particular, we assess the potential mechanisms underlying
limb bone torsion during non-parasagittal locomotion in alligators.
Additionally, our analyses allow us to refine evaluations of limb muscle
function and the roles that these muscles play in supporting body weight and
retracting the limb. Based on limb movement, force and motor pattern data, we
distinguish three dynamic phases during hindlimb stance: a limb-loading phase,
a support-and-propulsive phase, and a limb-unloading phase. Comparisons of
locomotor patterns among tetrapods suggest that limb function, forces, and the
use of femoral rotation in alligators may be quite different from patterns
understood for other species that use either more sprawling or more erect limb
posture. These results suggest that species using non-parasagittal posture may
exhibit considerable diversity in their locomotor mechanics. Furthermore, tail
dragging has been shown to have serious consequences for locomotor mechanics
in alligators (Willey et al.,
2004) which are borne out in patterns of femoral function in this
study. Thus, distinctive features of locomotor dynamics in alligators may be a
consequence of dragging the tail rather than general features of
non-parasagittal postures.
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Materials and methods |
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In our synthesis of data from different sources, we based our analyses on trials that were collected from animals as similar in size as possible, under locomotor situations that were as similar as possible. In general, data were collected at temperatures between 22°C and 29°C, from subadult individuals 0.5-1.0 m in length and 0.5-4.0 kg in mass, at speeds from 0.1-0.6 m s-1, using a standard `high walk' limb posture (limbs adducted 55±5° below horizontal at midstance), and a duty factor (ratio of hindlimb stance duration to stride duration) of approximately 0.7. Specifics for animal sizes, locomotor speeds and gait parameters are noted in the descriptions of methods provided for each set of experimental data. Although there is variation in some of these parameters, many were very closely matched across studies (e.g. mean duty factors across kinematic, force, bone strain and electromyography datasets ranged from 0.70-0.73). Moreover, we believe that over the extensive ranges of size and behavior of alligators, variation among the individuals and trials in our analyses is minimal, and that the insights gained from our synthesis outweigh the potential complications that arise from the combination of data collected during different experiments.
Kinematics and gait analyses
Kinematic angles and gait patterns were calculated and graphed to indicate
the general position and direction of movement of the limb segments. Data on
hindlimb kinematics and gait patterns were collected from five alligators
(total length 0.48-0.54 m, body mass 247-333 g); detailed analyses for the
strides used in the present analysis are presented in Reilly and Elias
(1998). Alligators were filmed
under strobe lights at 200 fields s-1 using a NAC HSV-400
high-speed video system. Both lateral and dorsal views of the alligators were
filmed (using mirrors) as they `high walked' on a 70 cm long canvas treadmill.
Only strides during which the animals very nearly matched the speed of the
treadmill (0.146 m s-1) were analyzed, during which the position of
a landmark painted on the hip stayed within a 1 cm zone (i.e. ±0.005
m). Based on the measured durations of these strides, the complete range of
speed variation among strides for all individuals was 0.141-0.151 m
s-1. This is less than 7% variation among strides, well within the
range of variation reported in previous studies of alligator kinematics
(Gatesy, 1991
) and muscle
activity patterns (Gatesy,
1997
). Electromyographical data were collected from these exact
same strides.
Reflective landmarks (2 mm diameter dots visible in both the lateral and
dorsal views: Fig. 1A,B) were
painted on the skin of the alligators to mark positions along the vertebral
column (T), the hip joints (directly over the acetabula; H), and three
landmarks on the right hindlimb: the knee joint (on the anterolateral point of
the knee when flexed; K), the ankle joint (posterolateral point of the ankle
when flexed; A) and the foot (lateral aspect of the metatarsaltarsal
articulation; F). Three-dimensional coordinates of each landmark were
digitized using stereo measurement TV (sMTV;
Updegraff, 1990), and
kinematic angles were calculated from these coordinates with an accuracy of
±1° for each joint.
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The knee and ankle angles calculated were the actual three-dimensional
angles for these joints based on the landmarks above
(Fig. 1B,C). Femoral movements
were quantified using two three-dimensional angles: femoral retraction
(retraction/protraction movements relative to the longitudinal axis of the
pelvis) and femoral adduction (adduction/abduction position relative to the
mediolateral axis of the pelvis). Femoral retraction was measured as the angle
between the femur and a line from the acetabulum to the trunk landmark. This
calculation produces angles that are 5-10° greater (not 15° as
indicated by Reilly and Elias,
1998) than those that would be calculated if femoral position were
measured relative to the sagittal plane (e.g.
Gatesy, 1991
) but produces
kinematic profiles that are nearly identical (within 5-10%;
Reilly and Elias, 1998
).
Femoral adduction was measured as the angle between the femur and a transverse
axis through the acetabula (based on three-dimensional coordinates of both
hips), with 0° indicating no femoral adduction (the femur held straight
out laterally from the acetabulum) and 90° indicating a position parallel
to the sagittal plane of the alligator
(Reilly and Elias, 1998
). This
convention for reporting femoral adduction angles follows the evolutionary
sprawling-to-erect paradigm, which categorizes sprawling femoral angles as
0° and erect ones as 90° (Bakker,
1971
; Charig,
1972
; Parrish,
1986
,
1987
;
Reilly and Elias, 1998
;
Blob, 2001
). Our femoral
adduction calculations also account for pelvic roll about a longitudinal axis
(<6° to each side; Gatesy,
1991
) and, thus, effectively represent the angle between the femur
and the horizontal plane of the body of the alligator. However, from a
practical perspective, because pelvic roll is not very large in alligators
(Gatesy, 1991
) the difference
between the convention of Reilly and Elias
(1998
) that we use in this
analysis and conventions that refer to absolute planes is minimal.
Gaits used by alligators were identified by limb phase
(Hildebrand, 1976;
Reilly and Biknevicius, 2003
),
the elapsed time between a hindlimb strike and the ipsilateral forelimb strike
normalized to hindlimb stride duration. Gaits used during kinematic,
electromyographic, force platform and bone strain experiments had nearly
identical duty factors and limb phase relationships.
For the analyses performed in this study, mean kinematic profiles and gait
patterns for three-dimensional joint movements during high walks were taken
from figs 4 and 5 of Reilly and Elias
(1998). These plots were
aligned with data on limb forces, limb bone strains, and limb muscle activity
in order to evaluate how limb forces and their bone loading consequences are
produced.
Electromyography
To quantify patterns of activity (motor patterns) for alligator hindlimb
muscles during the high walk, electromyographic (EMG) recordings were
collected from 12 muscles (all on the right side of the body). A previous
study (Reilly and Blob, 2003)
examined EMG data from the same alligator experiments but sampled muscle
activity patterns across a range of femoral angles from 19-55° and
compared
30° to
50° patterns to test for statistical effects
of posture on the modulation of the timing and amplitudes of motor patterns.
The present study presents new EMG data for the alligators normal high walk
posture (femurs adducted 55±5° below horizontal at mid-stance),
from the exact same strides (10 each from five animals of total length
0.48-0.54 m, body mass 247-333 g; speed (0.141-0.151 m s-1) of
treadmill locomotion examined in the synchronized kinematic analyses described
above (Reilly and Elias,
1998
).
EMG recordings were made from bipolar stainless steel electrodes implanted
into each muscle as in previous research
(Reilly, 1995). All electrodes
were implanted while the animals were under anesthesia induced by placing the
animals in a closed container with 1 ml of halothane for 15 min. Bared metal
tips of each bifiler insulated electrode were 0.5 mm long. Electrodes were
implanted percutaneously through the skin directly into the belly of each
target muscle. The bundle of electrodes was glued together and sutured to a
scale on the midline dorsal to the pelvis. Animals completely recovered from
anesthesia within 2 h and all synchronized EMG and kinematic data were
recorded during the next 2 h. Animals were rested (about 15-30 min) between
bouts of walking (45 s maximum). Immediately following each experiment, the
test animal was sacrificed by overdose of anesthetic and preserved in 10%
formalin. Electrode position was then confirmed by dissection, and EMG data
were considered valid for analysis only for preparations in which the
electrode lay completely within the muscle.
EMG signals were amplified 10 000 times using AM Systems model 1700
differential AC amplifiers with a bandpass of 100-3000 Hz (and a 60 Hz notch
filter) and then recorded on a TEAC XR-5000 multichannel FM tape recorder
along with a synchronization pulse simultaneously recorded on the video
frames. The analog signals (EMG channels plus a synchronization pulse) for
each stride were converted to a digital data file using custom software with a
Keithley analog-to-digital converter and a microcomputer. The effective sample
rate for each channel was 10 kHz at 12-bit resolution. A 10 kHz sample rate
was used because previous work has shown that this rate allows the faithful
reproduction of EMG spikes from vertebrate locomotor muscles
(Jayne et al., 1990). Prior to
the experiments, an extensive calibration of the system revealed no crosstalk
downstream of the electrodes, and crosstalk has not been a problem in previous
work using the same electrode materials, construction and placement protocols.
EMG profiles were inspected for possible patterns revealing crosstalk, and
none were found.
Ten electrodes were implanted during each EMG experiment and, of these, five to six usually supplied successful data recordings, providing data from between one and three individuals for each target muscle (Table 1). Although we did not record from every target muscle in each of our five experimental alligators, we were able to record data from multiple individuals for seven muscles and it is upon these data that we based our primary conclusions. Custom software was used to digitize the times of burst onset and offset for each muscle relative to the timing of foot down within each stride. This was done to assess changes in muscle activity relative to the onset of stance phase (i.e. when the foot contacts the ground and limb movements begin to directly affect the propulsive dynamics of the limb cycle). To quantitatively characterize patterns of muscle activity, calculations of average burst patterns (EMG bars on Fig. 3F) were based on 10 strides from each individual for which muscles were successfully implanted. To facilitate the calculation of average EMG patterns among strides, and allow alignment of EMG, kinematic and gait data with force and strain datasets, durations of muscle bursts were scaled as a percentage of stride duration.
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To gain more complete insight into muscular contributions to locomotor
movements, forces and bone loading patterns (including femoral torsion), we
supplemented our own recordings of 12 muscle activity patterns with EMG data
for four additional muscles published by Gatesy
(1997). Details of the data
collection methods for those muscles (caudofemoralis longus, flexor tibialis
head 2, iliofibularis, and puboischiofemoralis externus head 2; indicated by
asterisks in Table 1 and Figs
2,
3) are provided in Gatesy's
original publication. Gatesy's data
(Gatesy, 1997
) can be
reasonably compared to those for the other muscles examined in this analysis
because Gatesy also collected EMGs during treadmill walking, and he recorded
from animals of similar size (50-70 cm total length) under similar locomotor
conditions (speed: 0.1-0.15 m s-1; duty factor: 0.73±0.03;
femoral adduction angle: 60°) to those used here. Gatesy's study
(Gatesy, 1997
) normalized
burst timings to stride duration, but reported values relative to the onset of
the caudofemoralis muscle burst. To coordinate data from Gatesy's study with
EMGs from Reilly and Blob
(2003
) and force and strain
records, Gatesy's burst timing data were adjusted by subtracting 6% from all
onset and offset values (adjustment based on fig. 5 in
Gatesy, 1997
), thus realigning
his EMG records relative to the beginning of stance phase. It should also be
noted that eight muscles we recorded were also examined by Gatesy
(1997
). For two of these
(flexor tibialis externus, iliotibialis head 2) our data provide positive
verification of weak or sporadic patterns found by Gatesy
(1997
), and for the remaining
six muscles EMG patterns were similar in both studies.
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Myology
By combining EMG data from Gatesy
(1997) with our EMG data, we
were able to coordinate examination of the motor patterns of 16 alligator
hindlimb muscles (including axial, thigh, and crural muscles) with kinematic,
gait, force and bone strain data. Detailed anatomical descriptions of most of
these muscles (except the tibialis anterior) have been published
(Romer, 1923
;
Gatesy, 1997
). However, to aid
understanding of muscle function and our analyses, in this section we provide
a brief summary of muscle morphology (together with a schematic illustration,
Fig. 2). Previous studies have
evaluated alligator muscle functions based on anatomical topography
(Romer, 1923
) or EMG patterns
(Gatesy, 1997
). By correlating
EMGs with limb force and bone strain data, our present analyses allow us to
test many of these proposed functions. Muscles are described in anatomical and
functional groups based on results of Gatesy
(1997
), Reilly and Blob
(2003
), and this analysis.
Refined details of muscle functions found in this study are presented in the
results.
Posterodorsal thigh muscles (femoral retractors)
Flexor tibialis externus (FTE; Fig.
2A; one individual). Origin: tip of the postacetabular iliac
process. Insertion: medially by a large tendon to the proximal tibia; distally
by a smaller tendon passing down the leg to the calcaneus. It extends along
the posterior aspect of the femur where it joins the heads of the flexor
tibialis internus. FTE is the largest and most posteriorly located muscle of
the posterior thigh. FTE also functions as a knee flexor and ankle extensor
(plantarflexor).
Flexor tibialis internus, head 2 (FTI2;
Fig. 2A; two individuals).
Origin: postacetabular iliac blade. Insertion: medially on proximal tibia. The
FTI2 lies just ventral to FTE and is the largest of the four flexor tibialis
internus slips. FTI2 shares a wide tendon with the puboischiotibialis (PIT)
before inserting with the FTE on the proximal tibia. EMG data from Gatesy
(1997).
Caudofemoralis longus (CFL; Fig.
2A; four individuals). Origin: caudal vertebrae 3-15, filling the
space in the tail between vertebral haemal arches and transverse processes.
Insertion: proximally by a tendon on to the fourth trochanter and surrounding
area of femur; distally (not illustrated) by a smaller auxiliary tendon to the
knee and calf musculature. The CFL is the largest muscle affecting hindlimb
movements, producing femoral long axis rotation as well as retraction. EMG
data from Gatesy (1997).
Anterodorsal thigh muscles (knee extensors)
Iliotibialis, head 1 (ILTIB1; Fig.
2B; one individual). Origin: anterodorsal rim of iliac blade.
Insertion: via extensor tendon over anterior surface of knee to the
proximal tibia. The iliotibialis has three heads originating along the rim of
the iliac blade. All three heads join the distal tendon of femorotibialis
internus (FMTI) to form a common extensor tendon inserting on the front of the
tibia. ILTIB1 is the most anterior of the three heads, smaller and deep to the
ILTIB2.
Iliotibialis, head 2 (ILTIB2; Fig. 2B; two individuals). Origin: anterodorsal rim of iliac blade. Insertion: via extensor tendon over anterior surface of knee to the proximal tibia. The ILTIB2 is the middle head of the iliotibialis group. It is the largest muscle on the anterodorsal aspect of the thigh and originates from a wide portion of the iliac crest.
Both the ILTIB1 and 2 may play a role in hip and knee stabilization as well
as knee extension (Reilly and Blob,
2003).
Femorotibialis internus (FMTI; Fig. 2B; three individuals). Origin: dorsal surface of central femoral shaft. Insertion: via extensor tendon over anterior surface of knee to the proximal tibia. The FMTI is the larger, more anterior belly of the two heads of the femorotibialis group. It shares a broad, tendinous insertion with femorotibialis externus, iliotibialis and ambiens.
Ventral thigh muscles (femoral adductors)
Adductor femoris 1 (ADD1; Fig.
2C; three individuals). Origin: ventral aspect of ischium.
Insertion: ventral shaft of femur. The ADD1 is one of two heads of the
adductor femoris muscle and the most superficial ventral muscle of the
thigh.
Puboischiotibialis (PIT; Fig. 2C; 1 individual). Origin: anterior edge of ischium, well below acetabulum. Insertion: medial aspect of tibia. The PIT is a large muscle lying just posterior to ADD1. It passes along the ventral surface of the thigh to join FTI2 before inserting on the tibia.
Puboischiofemoralis externus, head 3 (PIFE3; Fig. 2C; two individuals). Origin: ventral surface of ischium. Insertion: Posteroventral surface of proximal femur. The three heads of the puboischiofemoralis externus complex converge to a common insertion on the proximal femur but are distinguished by their origins. The first and second heads (PIFE1 and 2) are more anterior and originate from the pubis and ribs, whereas PIFE3 is located more posteriorly.
Dorsal thigh muscles (femoral abductors)
Iliofibularis (ILFIB; Fig.
2C; three individuals). Origin: central iliac blade. Insertion:
Fibular tubercle and gastrocnemius. The ILFIB extends across the hip and knee
joints parallel to the femur. EMG data from Gatesy
(1997).
Iliofemoralis (ILFEM; Fig. 2C; one individual). Origin: postacetabular iliac blade. Insertion: posterodorsal aspect of proximal femur. The ILFEM runs parallel to insert between the origins of the two heads of the femorotibialis group.
Anterior thigh muscles (femoral protractors)
Puboischiofemoralis internus, head 2 (PIFI2;
Fig. 2D; one individual).
Origin: centra of lumbar vertebrae and the ventral surfaces of their
transverse processes. Insertion: Anterodorsal aspect of proximal femur. One of
two heads in the puboischiofemoralis internus group, PIFI2 lies along the
anterior surface of the proximal thigh. It is larger and originates more
anteriorly than PIFI1 (not sampled).
Ambiens, head 1 (AMB1; Fig. 2D; two individuals). Origin: ilioischiadic junction anterior to the acetabulum. Insertion: proximally, over the anterior surface of the knee to the proximal tibia via the common extensor tendon with femorotibialis and iliotibialis; distally, a weaker tendon continues through the extensor sheet lateral the knee joint, inserting on the gastrocnemius and Achilles tendon (not shown). The AMB1 is a large muscle that extends along the anterior aspect of the thigh. AMB1 is one of two heads of ambiens that is more superficial and considerably larger than AMB2 (not sampled).
Puboischiofemoralis externus, head 2 (PIFE2;
Fig. 2D; two individuals).
Origin: ventral surface of the pubis and last abdominal rib. Insertion:
posteroventral surface of the proximal femur. The PIFE2 runs from the anterior
to the posteroventral aspect of the thigh. It is one of three heads of the
PIFE group originating from the ventral pelvic elements that converge to
insert on proximal femur. It is located anteriorly to PIFE3 (described above
under femoral adductors). EMG data from Gatesy
(1997).
Crural muscles
Gastrocnemius (G; Fig. 2D;
three individuals). Origin: ventral aspect of distal femur and posterior
proximal tibia. Insertion: calcaneal tuber via Achilles tendon. This
ankle extensor is the largest muscle of the crus and appears to act as a knee
stabilizer or flexor as well as ankle extensor
(Blob and Biewener, 2001;
Reilly and Blob, 2003
).
Tibialis anterior (TA; Fig. 2D; two individuals). Origin: Anterior aspect of distal femur and proximal tibia and fibula. Insertion: Distal dorsolateral surfaces of the four most medial metatarsals. The TA passes through a laterally offset groove in the proximal end of the tibia to act as a dorsiflexor of the ankle.
Hindlimb ground reaction forces
To evaluate hindlimb ground reaction forces (GRFs) in the context of other
datasets, a subset of GRF data reported by Willey et al.
(2004) were selected that had
been collected under locomotor conditions as close as possible to those of the
kinematic, gait, and EMG data. GRFs were collected from five alligators
(00.99-1.09 m total length; 2.24-4.00 kg body mass) as they walked over a
force platform (Kistler Corporation, plate Type 9281B) inserted into a 6.1 m
runway. To capture records for individual footfalls of the hindlimb and reduce
the potential for interference from contacts with other feet, a triangular
insert (244.25 cm) was firmly affixed to the surface of the force platform and
made flush with the floor of the trackway, with the uninstrumented part of the
track covering the rest of the platform. Analog signals from the force
platform were amplified (Kistler Corporation, amplifier Type 9865C), digitized
at 500 Hz, and imported into Bioware 2.0 software for analysis. Trials were
synchronously recorded by two 60 Hz cameras (JVC TK-C1380U) oriented to
provide views that would allow evaluation of whether footfalls were acceptable
for analysis (e.g. whether a single foot landed fully on the platform without
overlapping feet). A single high-speed camera (Redlake Motionscope 500)
simultaneously recorded the trials from a lateral view at 250 Hz in order to
determine the velocity of each trial. Mean locomotor speed of each trial was
determined from the time it took the animal to walk past a 70 cm calibration
grid located on the back wall of the runway. Forward speeds were also
calculated between successive 10 cm vertical bars immediately over the force
platform. These velocities were compared with the mean velocity, and trials
were accepted only if the successive velocities differed by less than 5% from
the mean velocity (indicating the animals were not accelerating or
decelerating). Duty factor (percentage of stride duration that the individual
limb contacted the force platform) also was calculated from force and video
records.
GRFs were collected in the vertical, fore-aft (craniocaudal), and mediolateral directions relative to the alligators (Fig. 1D). Vertical forces reflect body support and vertical acceleration of the center of mass due to gravity. Fore-aft forces are divided into braking (-) or propulsive (+) components. Mediolateral forces indicate whether a limb is pushing medially (+) or laterally (-). All GRFs were converted to body weight units (BWU) to adjust for differences in body mass among the animals. Five parameters of the GRF and their timing (percentage stance duration) were measured: peak vertical force, peak braking force, braking-to-propulsive transition (fore-aft force crosses zero), peak propulsive force, and peak lateral force.
From the 60 trials (12 runs per animal) analyzed by Willey et al.
(2004), 20 high walk trials
were selected from four of the alligators to produce a sample that very
closely matched the mean speed (0.146 m s-1) and duty factor
(0.70±0.01) of the trials used in the analyses of kinematics, gait, and
EMGs. This final sample (Table
2) included three to seven trials per individual, with a mean
speed of 0.148±0.021 m s-1 and a mean duty factor of
0.70±0.03. Gaits from steps used in the force measurements were found
to be essentially identical to those used in the treadmill data collection. To
compare patterns of GRF to other locomotor parameters, traces from typical GRF
records were normalized to stance duration and aligned with kinematic, gait,
and EMG data in Fig. 3 and with
bone strain data in Fig. 4.
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Femoral torsion
Profiles of locomotor forces, kinematics and EMGs were compared to
evaluations of femoral torsion based on in vivo bone strain
recordings (Blob and Biewener,
1999). Bone strains were recorded by surgically implanting strain
gauges on the right femur of three subadult alligators (total length 0.98-1.04
m; body mass 1.73-2.27 kg) while the animals were under anesthesia (following
protocols of Biewener, 1992
).
Rosette gauges were attached to the dorsal and ventral surfaces of the femur
with cyanoacrylate adhesive, after the removal of a window of periosteum and
cleaning of the attachment site with ether. Central elements of the rosette
gauges were aligned with the long axis of the femur and indicated longitudinal
strains (tension or compression along the axis of the bone). The use of
rosette gauges also allowed calculation of the magnitude and orientation of
principal strains (maximum and minimum strains at a site, potentially not
aligned with the long axis of the bone;
Daley and Riley, 1978
), as
well as shear strains (calculated following methods of
Biewener and Dial, 1995
).
These calculations allowed evaluation of the importance of torsional loading
on the femur and the timing of its development through the stride cycle.
After gauge attachment, lead wires from the gauges were passed
subcutaneously out of an incision dorsal to the acetabulum and soldered into a
microconnector for connection to Vishay conditioning bridge amplifiers (model
2120, Measurements Group). After 2-4 days of recovery from surgery, data were
collected during 40 s bouts of treadmill locomotion at either 0.17 or 0.37 m
s-1 [note that Reilly and Elias
(1998) found no speed effects
on femoral retraction and adduction kinematics, thus we believe that strain
data captured at slightly higher speeds should be comparable to the other data
sets]. Raw strain signals were sampled through an A/D converter at 100 Hz and
stored on computer for analysis. Locomotor trials were filmed with 60 Hz video
to allow evaluation of limb movements, speed, and duty factor for each stride.
To evaluate the timing of peak shear strains and the development of other
strains relative to muscle activity and limb forces, representative strain
traces were normalized for stride duration and aligned with traces for other
locomotor parameters (see Fig.
4).
In addition to strain recordings, force platform records
(Blob and Biewener, 2001) also
provided data on femoral torsion by allowing calculation of the torsional
moment of the GRF about the long axis of the femur. These data were obtained
from six trials for a single alligator (1.98 kg) moving faster than those in
the other datasets considered in this study (0.62±0.21 m
s-1) but using the same gait (fast walking trot; sensu
Hildebrand, 1976
). Data were
collected from this alligator at 500 Hz as it walked down a runway and stepped
with a single hind foot on a custom-built force platform (inserted so its
surface was flush with the trackway) that measured the three-dimensional GRF.
Using a mirror in the trackway, both lateral and dorsal views of the alligator
were simultaneously filmed with a high speed video camera (250 Hz, Kodak
EktaPro model 1012) as it stepped on the platform. The positions of the limb
joints were digitized in the video frames and, combined with data on the
magnitude and orientation of the GRF, the torsional moment of the GRF about
the long axis of the femur was calculated using custom software. This moment
indicates the tendency of the GRF to rotate the femur. If the GRF is directed
posterior to the femoral long axis, it would tend to rotate the femur medially
or inward (counterclockwise if viewing the right femur from its
proximal end); if the GRF is directed anterior to the femoral long axis, it
would tend to rotate the femur laterally or outward (clockwise if
viewing the right femur from its proximal end). To evaluate the timing and
direction of torsional moments relative to limb kinematics, muscle activity,
and bone strains, a representative trace of the torsional moment of the GRF
was normalized for stride duration and aligned with traces for other locomotor
parameters (Fig. 3B).
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Results |
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Hindlimb muscle activity patterns
Mean motor patterns for 12 muscles quantified in this study and four from
Gatesy (1997; indicated with
asterisks) are presented in Table
1 and illustrated in Fig.
3F. For nearly all of the muscles that were examined by both
Gatesy (1997
) and here
(Table 1), motor patterns were
remarkably similar between the studies, with mean onsets and offsets differing
by at most only 10% of stride duration. One exception was ILTIB2, for which we
found burst durations to be longer by almost 20% stride duration (offsets of
52.3% versus 33.5% of stride duration). In addition, although some
muscles recorded by Gatesy
(1997
) displayed pulsatile EMG
signals, all of the muscles we recorded consistently showed discrete EMG
bursts rather than pulsatile signals. For FTE and FTI2 in particular, we found
discrete burst patterns that confirm the patterns identified by Gatesy
(1997
) from more sporadic
bursts. Of the 16 muscles under consideration, eight had a majority of their
activity during stance phase (red in Fig.
2), six were active primarily during swing phase (blue in
Fig. 2), and two were active in
both phases (black in Fig. 2),
the continuously active ILTIB1 and the PIT with discrete bursts in both
phases. Reilly and Blob (2003
)
provided the first summaries of motor patterns for four of these muscles
(ILTIB1, PIFE3, G and TA) but their analysis focused on changes in burst
characteristics related to limb posture, rather than propulsive dynamics.
Therefore, we will describe the motor patterns of these four muscles in detail
before outlining the new clarifications of muscle action patterns derived from
coordinated analyses of the 16 muscles considered in this study. Summaries of
mean onset and offset times for each muscle are reported in
Table 1 and illustrated in
Fig. 3F.
Iliotibialis, head 1
Extending from the dorsal pelvis to the knee
(Fig. 2B),Iliotibialis, head 1
(ILTIB1) is in a position to abduct the femur and extend the knee. ILTIB1 has
the earliest onset of any of the primarily stance phase muscles
(Table 1), with activity
beginning just before the middle of swing phase (-18% of stride duration) and
ending just after mid-stance (38% of stride duration). Its onset coincides
with the beginning of both hip adduction and knee extension in mid-swing phase
(Fig. 3E). Thus, ILTIB1
contraction seems likely to contribute to protracting the thigh and extending
the knee during swing phase. However, ILTIB1 activity during stance phase
coincides with a long period during which the knee and hip adduction angle are
held nearly constant (Fig.
3E,F). Thus, ILTIB1 activity during stance phase appears to
stabilize the hip and knee joints.
Puboischiofemoralis externus
This ventral thigh muscle extends from the ventral surface of the ischium
to the proximal femur (Fig. 2C)
and is in a position to adduct the femur. Puboischiofemoralis externus 3
(PIFE3) becomes active in the last quarter of swing phase and continues to
fire for the first three-fourths of stance; thus, its activity coincides with
the entire time during which the femur retracts. Because actual femoral
adduction is slight during this period, PIFE3 appears to serve as hip
stabilizer during stance.
Gastrocnemius
Extending from the posterior aspect of the knee to the heel
(Fig. 2D) this muscle is
clearly positioned to extend the ankle as well as flex the knee. It is active
from just after foot down until almost the end (90%) of stance phase.
Ankle extension begins at about 35% of stance duration; thus, during the
second two-thirds of its activity period, the gastrocnemius (G) clearly serves
as an ankle extensor (plantarflexor). However, the ankle flexes during the
first third of the activity period of the gastrocnemius. Contraction of the
gastrocnemius during ankle flexion probably serves to control the degree of
ankle flexion and, thereby, stabilize the ankle prior to the onset of its
extension.
Tibialis anterior
Extending from the proximal tibia to the metatarsals
(Fig. 2D) Tibialis anterior
(TA) is well-situated to act as an ankle flexor (dorsiflexor). Corresponding
to this role, TA is active in the first half of swing phase (68-91% of stride
duration), essentially matching duration of ankle flexion during swing
(Fig. 3). However, the TA was
not active during ankle flexion in early stance phase suggesting that
dorsiflexion at this time is a result of another muscle or passive effects of
higher limb movements.
Motor control of swing phase hindlimb movements
Six muscles were active primarily during swing phase
(Fig. 2C,D: blue). Although no
ground reaction forces are associated with this portion of the limb cycle as
the leg protracts, the motor patterns of muscles active during this time can
be compared to joint kinematics to evaluate muscular function.
Femoral abduction and knee flexion
Of the many possible muscles in position to abduct the femur, only ILFIB
and ILFEM (Fig. 2C) were active
primarily during swing phase. Both muscles initiate their activity in late
stance phase (Fig. 3F; first
group of swing phase muscles). Activity in ILFEM, which is positioned to act
solely as a femoral abductor, ends at about one third through the duration of
swing phase, while activity in ILFIB, which passes over the knee joint, is
active through nearly half of swing phase. These bursts coincide with the
continuing abduction of the femur in early swing phase right after the foot is
raised from the ground (Fig.
3E). These bursts also coincide with the swing phase burst of PIT,
a femoral adductor. The synchronization of these bursts seems to indicate a
controlled abduction (ILFEM) and adduction (PIT) of the femur early in swing
phase before the femur is quickly adducted back to its position at foot down
by the stance phase bursts of PIT and other femoral adductors. With regard to
ILFIB, Gatesy (1997) showed
that with its low origin on the iliac blade and oblique crossing of the knee
joint, ILFIB is anatomically well positioned to flex the knee.
Correspondingly, the period of ILFIB activity matches the rapid period of knee
flexion during early swing phase (Fig.
3E). Therefore, ILFIB appears to contribute to both femoral
abduction and knee flexion in swing phase.
Femoral protraction and knee extension
Two anteriorly positioned, proximal thigh muscles, PIFI2 and PIFE2,
exhibited focused bursts of activity in the swing phase
(Fig. 3F; second group of swing
phase muscles). PIFI2 is positioned to oppose the action of CFL
(Fig. 2D); thus, PIFI2 probably
serves to protract the femur and rotate it laterally (in the opposite
direction from CFL). Its activity closely parallels the period of femoral
protraction during swing phase. PIFE2 is active in the latter half of femoral
protraction during swing. Its ventral position (originating from the pubis)
suggests it could contribute to femoral adduction during swing phase, but its
anterior position suggests that, like PIFI2, PIFE2 may act as a primary
protractor of the femur. The ambiens (AMB1,
Fig. 2D) is also located in a
position where its contraction could protract the femur. It is active somewhat
later than PIFI2 and PIFE2, during the period of knee extension that occurs
during femoral protraction (Fig.
3E,F). Because AMB1 spans the knee as well as the hip
(Fig. 2D), the timing of its
activity indicates it serves as a primary swing phase knee extensor as well as
a limb protractor during late swing phase. Several other muscles that are
anatomically positioned to extend the knee also become active during mid to
late swing phase as knee extension commences. ILTIB1 activity begins just
after that of AMB1 (Fig. 3F),
indicating that ILTIB1 probably also contributes to the initiation of swing
phase knee extension. ILTIB2 and FMTI become active toward the end of swing
phase (Fig. 3F), so their
contraction also may contribute to knee extension that occurs during this time
(Fig. 3E).
Ankle flexion and extension
The ankle undergoes first flexion, then extension during swing phase. TA is
anatomically situated to flex the ankle, extending from the tibia to the
dorsal aspect of the foot (Fig.
2D). It exhibits a strong EMG burst during the first two-thirds of
swing phase, coinciding very closely with the swing phase period of ankle
flexion (Fig. 3E,F). Although G
is anatomically located to act as a major ankle extensor, it is not active
during swing phase ankle extension. However, AMB1 is active during mid to late
swing phase, and its auxiliary tendon to the heel appears to have an important
role in extending the ankle prior to the placement of the foot on the
ground.
Motor control of stance phase hindlimb movements
Femoral retraction and rotation
Of the nine dorsally positioned thigh muscles considered in this analysis,
only six were active during stance phase
(Fig. 2A,B). Of these, three
(FTE, FTI2, CFL; Fig. 2A,
Fig. 3F; first set of three
stance phase muscles) are positioned posteriorly and represent a functional
unit that could retract and rotate the limb. CFL has been identified as the
primary femoral retractor and medial rotator during limb retraction in
crocodilians (Gatesy, 1990,
1997
). EMG data show that CFL
activity coincides with the entire period of femoral retraction, from its
start during late swing phase until retraction stops nearly three quarters
through the duration of stance phase (Fig.
3E,F). FTE and FTI2 are also located in positions suited to
contribute to femoral retraction, and were considered ancillary stance phase
hip retractors by Gatesy
(1997
). With insertions on the
lateral aspect of the upper shank (Fig.
2A), both could also contribute to femoral rotation and,
potentially, knee flexion (see below). However, these muscles have somewhat
different motor patterns. FTI2 activity parallels the first two-thirds of the
CFL burst, suggesting it contributes primarily to early retraction. Like CFL,
FTI2 is situated to contribute to medial femoral rotation; however, FTI2 is
active primarily when the GRF would tend to rotate the femur laterally (i.e.
in the opposite direction; Fig.
3B,F), suggesting that this muscle might help to stabilize the
femur against rotation during early retraction. The same may be true for the
CFL early in stance phase. In contrast, FTE has a later burst of activity,
beginning at foot down and ceasing nearly simultaneously with the end of the
CFL burst by the end of femoral retraction
(Fig. 3E,F). The rotational
moment of the GRF shifts from lateral to medial during this time, acting in
the same direction as FTE and CFL by the midpoint of their bursts. This
suggests that FTE, like CFL, contributes to femoral rotation as well as
femoral retraction.
Knee stabilization and knee flexion
FTI2 and FTE are anatomically situated to flex the knee joint as well as
retract the femur. However, during stance phase the knee joint is static
before it flexes (Fig. 3E).
Thus, FTI2, which is active only while the knee is static, appears to
stabilize the knee rather than flex it. In contrast, FTE is active well into
the period of knee flexion during the latter half of stance and, therefore,
probably helps to actively flex the knee. Although knee flexion continues into
late stance (Fig. 3E), activity
ceases in both of these potential knee flexors well before the end of the step
(Fig. 3F). Body weight might
passively contribute to knee flexion during later portions of stance phase,
but the hindlimb will tend to be unloaded when the next limb couplet of the
trot contacts the ground later in stance phase
(Fig. 3D; see later Results).
As mentioned above, knee flexion during late stance might be actively
controlled by the shank muscle gastrocnemius, which spans the flexor side of
the knee joint and is active until almost the end of stance
(Fig. 3F).
Three other dorsally positioned thigh muscles that are active during stance
phase (FMTI, ILTIB1 and ILTIB2; Figs
2B,
3F; second set of three stance
phase muscles) are aligned more closely with the long axis of the femur and
share a wide tendinous insertion extending to the proximal tibia. These
muscles all become active in mid to late swing phase as the knee extends
(Fig. 3E). However, both the
onset and offset of ILTIB1 activity are shifted earlier relative to those of
the other two muscles by almost 20% stance duration. Unlike ILTIB1, both
ILTIB2 and FMTI become active during the end of swing phase and fire through
the first three quarters of stance phase. Gatesy
(1997) reported knee extension
during the latter half of stance phase and, therefore, described these three
muscles as stance phase knee extensors. However, because our results (and data
on other speeds and postures; Reilly and
Elias, 1998
) show the knee remaining static or flexing during
stance phase, we conclude that these muscles act to stabilize the knee as it
accommodates and supports body weight through the first three quarters of
stance. In fact, it is not until activity ceases in these muscles that stance
phase knee flexion becomes substantial, further suggesting that these muscles
act to limit knee flexion during stance and that late in stance they no longer
counter the effects of body weight and flexor muscles on the knee joint.
Femoral adduction
The last three thigh muscles active during stance phase (ADD1, PIT, PIFE3,
Figs 2C,
3F; third set of three stance
phase muscles) are anatomically situated to act as femoral adductors. These
three muscles are active from mid to late swing phase until well into stance
phase, but their burst patterns are somewhat staggered in time. PIT appears to
act as a swing phase femoral adductor, becoming active before the middle of
swing phase coincident with a major period of femoral adduction. There are two
lines of evidence that the PIT actively powers adduction during the swing
phase. First, the swing phase burst is associated with the complete
repositioning of the limb in adduction during swing
(Fig. 3E,F). Second, the swing
phase PIT EMG intensity (mean area) is approximately the same as that during
stance phase (Reilly and Blob,
2003). In contrast, ADD1 and PIFE3 become active in the last third
to fourth of swing phase, after femoral adduction has stopped. All three
muscles are active through most of the first three quarters of stance, but
PIFE3 activity continues longer than that of the other muscles, lasting until
femoral retraction stops and vertical GRFs begin to decrease. Because the
activity of these muscles coincides with phases when the femur is static (or
actually abducted as much as 5°), these three muscles appear to stabilize
the hip, counteracting the weight of the body as it is supported during stance
phase.
Ankle extension
The remaining stance phase muscle studied was the G, which appears to be a
primary ankle extensor (Fig.
1D; Fig. 3F; last
stance phase muscle). Our EMG data show that G activity begins after the start
of stance and continues longer than that of any other stance phase muscle
(until nearly 90% stance duration). Its activity begins near the end of ankle
flexion during early stance and continues through the entire period of ankle
extension during stance phase. It is not active during swing phase; thus,
another muscle must control ankle extension that occurs while the foot is not
in contact with the ground. It is noteworthy that FTE not only has an
auxiliary tendon extending to the calcaneum, but that it has essentially the
same motor pattern as G. Thus, FTE seems likely to also contribute to stance
phase ankle extension.
Hindlimb ground reaction forces
Typical three-dimensional GRF traces for alligator hindlimb steps for
animals moving the same speed as in the EMG studies are presented in
Fig. 3C. Means for key events
of the force patterns are presented in
Table 2. Alligator hindlimb
steps exhibited vertical force profiles that consistently increased to near
peak values of about half of body weight in the first fifth of the stance
phase. Near peak forces are maintained until about the last third of stance
phase when body support wanes. Fore-aft forces indicate a brief braking
component in the first fifth (15.4%) of stance phase with maximum braking
force of 5.4% of body weight at 6% of stance duration. Thereafter, a long
gradually increasing propulsive component occurs during the middle (from 15.4
to 64.4%) of stance phase coincident with the period when vertical forces
plateau. Maximum propulsive force of 5.9% of body weight occurs at 64.4% of
stance duration. Propulsive effort then decreases to around zero early in the
last third of stance duration. Mediolateral GRFs are consistently negative
(i.e. medially directed), and these forces reach maximum values of about 10.6%
of body weight in the first fifth (19.1%) of stance duration and then
gradually decrease over the rest of the stance phase, dropping to zero just
before the foot is picked up.
Hindlimb force vectors
Ground reaction forces were reconfigured to reflect hindlimb output forces.
Sagittal (Fig. 4A) and
transverse (Fig. 4B)
two-dimensional limb force vectors illustrate how the hindlimb pushes on the
ground during the stance phase. Once the foot has settled in after impact the
net hindlimb vertical force vector is directed about 10° anterior to
vertical (80° on Fig.
4A) and about 60° lateral to the direction of travel
(Fig. 4B). In the first
one-fifth of stance phase the hindlimb force vector swings posteriorly to
about 4° posterior to vertical (
94° in
Fig. 4A) and 110° relative
to the direction of travel. Throughout the middle portion of stance, the
sagittal force vector then remains relatively constant (about 95°) whereas
the transverse component swings continually more posteriorly (from
110-130°) until the greatest posterolateral force direction occurs at
about two-thirds of stance phase. During the last quarter of stance phase, the
longitudinal propulsive component becomes negligible
(Fig. 3C) and the sagittal
hindlimb force vector swings anteriorly to about 90°
(Fig. 4A). At the same time,
the transverse forces are dominated by a lateral push on the ground by the
hindlimb. This indicates that the last portion of the stance phase (after the
time that the fore-aft forces return to zero;
Fig. 3C) involves only vertical
and lateral forces. Because of the relatively small mediolateral forces, the
limb is primarily supporting the body with a secondary role of providing
mediolateral stability. The final noisy shifts in hindlimb force orientation
just prior to lift-off are inconsequential as they are associated with
increasingly trivial force magnitudes.
Integrative dynamics of stance phase for the alligator hindlimb
Our coordinated analyses of hindlimb kinematic, gait, motor pattern, force
and bone loading data during stance in alligators (Figs
3,
4) indicate three distinct
dynamic phases during this portion of the locomotor cycle for the
hindlimb.
Limb-loading phase
During the first fifth of the step, the hindlimb is loaded as body weight
is transferred fully to the stance phase forelimb-hindlimb couplet. This
limb-loading phase is distinguished by several dynamic features. First, loads
on the femur (axial, principal, and shear strains,
Fig. 4C-E) increase throughout
this phase, rising toward maxima nearly simultaneously by the end of this
portion of the step. Gait data (Fig.
3D) show that this phase begins when the hindlimb contacts the
substrate and continues until the limbs of the opposing forelimb-hindlimb
couplet begin their swing phases (coincident with the left vertical shaded bar
in Figs 3,
4). Joint kinematics
(Fig. 3E) show that the knee
and ankle both flex as the limb is loaded. However, as the femur is retracted
during this phase (continuing motion that began during the previous swing
phase), femoral adduction remains fairly constant. All of the muscles that
will be active during the following propulsive phase have started to contract
by the end of the limb-loading phase; in fact, many of these muscles
(including CFL, the major limb retractor) start to contract at the end of the
swing phase prior to limb loading (Fig.
3F). During the limb loading period, the vertical component of the
GRF rises to near maximum levels (>40% body weight), the medial component
of the GRF rises to its maximum (10.6% body weight at 19% stance phase), and a
small hindlimb braking impulse occurs (Fig.
3C, Table 2). When
force components are recalculated to reflect the orientations of forces that
the hindlimb exerts on the ground (Fig.
4A,B), sagittally oriented hindlimb forces reflect deceleration
during most of the limb-loading phase (i.e. the foot pushing anteriorly on the
ground, Fig. 4A), and
transversely-oriented hindlimb forces transition from anterolateral at the
start of the phase to posterolateral by the end of the phase
(Fig. 4B). In addition, the
torsional moment of the GRF rises towards its maximum in the lateral direction
during the limb-loading phase (clockwise if the right femur is viewed from its
proximal end; Fig. 3B),
opposite of the direction of rotation that would be expected to result from
CFL contraction.
Support-and-propulsion phase
The middle portion of stance phase (between the vertical shaded bars in
Figs 3 and
4) is distinguished by several
features indicating that hindlimb contributions to body support and propulsion
are maximized during this phase. High vertical forces are maintained
throughout this phase (Fig.
3C), indicating more or less constant support of body weight by
the hindlimb. However, bone strains decrease throughout this phase
(Fig. 4C-E) despite the fact
that gait diagrams show that the body is supported only by a single limb
couplet during this entire phase (Fig.
3D). For the first half of the support and propulsion phase, while
the GRF is still increasing (Fig.
3C), decreases in strain probably reflect an increasingly closer
alignment between the GRF and the femur. During the second half of the support
and propulsion phase, the orientations of the GRF and femur will tend to
diverge, but strains continue to decline in correspondence with decreases in
GRF magnitude.
Virtually all of the propulsive impulse occurs during this phase
(Fig. 3C) with increases to
near maximal levels early in this phase. The medially directed GRF decreases
from its maximum (of about 6% of body weight) at the onset of this phase to
about half maximal values by the end of the support-and-propulsion phase
(64.4% of stance). Ratios of vertical and lateral hindlimb forces to
fore-aft hindlimb forces show that the foot exerts a more or less constant but
slightly posteriorly directed force on the ground during this phase
(Fig. 4A). However, throughout
this phase, increases in the rearward force exerted by the foot, and
coincident decreases in the lateral force it exerts, result in a 20°
posteromedial shift in the direction of the force that the hindfoot exerts on
the ground (i.e. transverse forces applied by the hind foot become more
posteriorly oriented; Fig. 4B).
Limb joint kinematics show that the femur continues to retract during this
phase, but that the knee, ankle and femoral adduction angles change little
during the first two-thirds of support and propulsion
(Fig. 3E). In the last third of
the support-and-propulsion phase, femoral retraction continues at the same
rate while the knee begins to flex and the ankle begins to extend
(plantarflex); thus, shortening of the functional length of the limb caused by
knee flexion is counteracted by ankle extension. Consequently, femoral
retraction (which stops at the end of this phase) is primarily responsible for
overall changes in hindlimb position during the support-and-propulsion phase
in alligators. During support-and-propulsion phase, the hip and knee move
anteriorly relative to the foot. As a result, when the femur is nearly
perpendicular to the body of the alligator (95-100° femoral retraction
angle, Fig. 3E), the GRF will
shift from being directed anterior to the long axis of the femur (as in the
limb-loading phase) to being directed posterior to the long axis of the femur
(Blob and Biewener, 2001
). As
this shift occurs by the midpoint of the support-and-propulsion phase (close
to the time of peak vertical force; Fig.
3B), the torsional moment of the GRF about the femur shifts from
exerting a lateral moment to a medial moment (counterclockwise when the right
femur is viewed from its proximal end; Fig.
3B). This moment reaches its maximum by the end of the
support-and-propulsion phase, and it acts to produce femoral rotation in the
same direction that is expected from contraction of the CFL. Thus, the actions
of both the GRF and CFL have the potential to induce substantial medial
rotation of the femur during its retraction in the support-and-propulsion
phase. It should be noted, however, that shear strain magnitudes have declined
from their maxima by the time during the step that both CFL and the GRF would
induce femoral rotation in the same direction
(Fig. 4D). Moreover, CFL
activity ceases by the end of this phase
(Fig. 3F).
Limb-unloading phase
Dynamic changes in the last third of stance phase delineate the unloading
of the hindlimb at the end of the step as the opposite forelimb-hindlimb
couplet touchdown and begin their loading phase
(Fig. 3D). Limb bone strains
decline to zero (Fig. 4C-E) as
does propulsive force. The mediolateral component of the GRF decreases to zero
during the second half of this phase. Consequently, during the first half of
the unloading phase, the sagittal limb forces become more purely vertically
oriented as the transverse limb forces become more lateral
(Fig. 4A,B). The final, more
irregular, portion of the unloading phase reflects rolling over the hindfoot
toes. Ratios of vertical and lateral hindlimb forces to fore-aft hindlimb
forces decrease from maxima (respectively 130° and 98°,
Fig. 4A,B) to minima
(90°) in the first half of this phase, reflecting the decline of all
force components to zero toward the end of the step. Most muscles active
during the support-and-propulsion phase cease activity very early in the limb
unloading phase, with the exception of the knee flexor/ankle extensor
gastrocnemius, which is active for nearly the first three quarters of this
phase (Fig. 3F). Joint
kinematics show that the femur is held in a maximally retracted position
during the limb-unloading phase, but that knee flexion and ankle extension
continue to counteract each other throughout this phase
(Fig. 3E), so that as vertical
forces decline the functional length of the limb distal to the knee changes
very little in length. The rotational moment about the long axis of the femur
also falls to zero by the end of this phase
(Fig. 3B).
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Discussion |
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Propulsive forces, in vivo strains, and the hindlimb loading phase
At touchdown, when an alligator first places its hindfoot on the ground,
some of its limb joints begin to flex, compressing the functional length of
the limb as it begins to support the weight of the body. Although the knee
flexes briefly just after foot down, most of the shortening of functional
hindlimb length during the limb-loading phase results from ankle flexion. By
the end of the limb-loading phase, every stance phase muscle examined was
fully active, and the activity of these muscles held the ankle, knee and hip
adduction angles nearly constant while the femur is retracted and rotated.
Thus, the limb motions that elicit propulsive GRFs by the end of the
limb-loading phase (Figs 3C,
4A,B) relate primarily to
femoral retraction and rotation (see also
Gatesy, 1991;
Blob and Biewener, 2001
).
In the alligator femur, principal, shear and longitudinal strains all reach their highest values early in the step by the end of the limb-loading phase or the beginning of the support-and-propulsion phase (Fig. 4C-E). These peak strains coincide with several events, including the point when body weight becomes fully supported by a single limb couplet (Fig. 3D), the onset of the plateau in vertical hindlimb forces (Fig. 3C), the development of peak medial GRFs acting on the hindlimb (Fig. 3C), the end of the hindlimb braking impulse (Fig. 3C), and the peak lateral (outward) rotational moment of the GRF (Fig. 3B). Thus, peak bone loads (i.e., maximum strains) are associated with peak mediolateral forces and moments and the initial loading of body weight onto the limb just prior to the support-and-propulsion phase, rather than with the highest forces associated with propulsion or the support of body weight. Strain magnitudes actually decrease rapidly during the support-and propulsion-phase, even though the body is completely supported by one limb couplet and all hindlimb stance phase muscles are active. Principal and shear strains ultimately return to zero by the end of the support-and-propulsion phase (Fig. 4C,D) as the opposite limb couplet contacts the ground and begins to support body weight (Fig. 3D). Axial strain, however, decreases to zero later during the step than shear strains. This suggests a decline in the importance of torsion relative to bending and axial loads later in the step (perhaps as the leg becomes more closely aligned with the GRF), although this occurs at strain magnitudes much lower than the peak loads experienced earlier in the step.
Mechanisms underlying torsional loading of the alligator femur
Alignment of rotational moments of the GRF with shear strains and muscle
activity patterns provides insight into the mechanisms underlying torsional
loading of the femur in alligators. Strain records directly indicate the
actual deformation of the bone surface, and thus reflect the net loads
resulting from all forces acting on the bone. Shear strains (reflecting
torsion) increase to their maxima by the end of the limb-loading phase of
stance (Fig. 4D) and indicate a
medial twisting of the distal end of the femur
(Blob and Biewener, 1999).
Such twisting could be induced either by the contraction of limb retractor
muscles with ventral insertions on the femur, by the rotational moment of the
GRF if the GRF is directed posterior to the long axis of the femur or,
perhaps, by combined action of both processes. Femoral retractors such as CFL,
FTI2 and FTE are active at the end of the limb-loading phase when shear
strains are at their highest levels (Fig.
3F), and thus these muscles appear to contribute to the generation
of torsional loads on the femur with a tendency to rotate the femur medially.
However, when shear strains are highest the GRF is directed anterior
to the long axis of the femur (Blob and
Biewener, 2001
) and the GRF exerts a moment that would tend to
rotate the femur laterally (Fig.
3B), i.e. in the opposite direction from rotation induced by the
limb retractor muscles. This means that the unusually high shear strains seen
in the alligator femur must be produced by contraction of CFL and other
muscles against the rotational moment of the GRF. This conclusion
differs from the hypothesis of Blob and Biewener
(2001
), who had suggested that
high torsional loads in alligator limb bones result because both the GRF and
CFL would act additively and induce a moment that would tend to rotate the
femur in the same direction. The GRF and CFL do act additively to produce
medial femoral rotation later in stance but only after shear strains have
begun to decline from their peak. In fact, by the time the GRF exerts its
maximum rotational moment in the medial direction at the end of the
support-and-propulsion phase (Fig.
3B), activity in the limb retractor muscles ceases
(Fig. 3F). Thus, additive
action of the GRF and limb retractors (such as CFL) is not a primary factor in
the generation of high torsional loads in the alligator femur near the end of
the limb-loading phase.
Is femoral torsion a general feature of non-parasagittal locomotion?
The predominance of torsion as a mode of limb bone loading is an unusual
feature that distinguishes alligators and iguanas from most tetrapods in which
limb bone loads have been evaluated during terrestrial locomotion
(Blob and Biewener, 1999).
Blob and Biewener (1999
)
suggested that, if limb bone torsion was a common feature of limb bone loading
among crocodilians and lepidosaurs (the broader clades to which alligators and
iguanas belong), then it might be a general and, perhaps, ancestral feature of
terrestrial locomotor mechanics among species that do not use strictly
parasagittal limb movements. However, alligators (and iguanas) exhibit several
distinctive kinematic features that are not seen among taxa that habitually
use either more or less sprawling limb posture. For example, salamanders,
sprawling lizards and mammals all share a distinct pattern of knee kinematics
in which flexion is followed by extension during stance phase
(Peters and Goslow, 1983
;
Ashley-Ross, 1995
; Reilly,
1995
,
2000
), whereas alligator and
iguana knees are held fixed in early stance and then either extend or flex
(Fig. 3;
Brinkman, 1980
;
Reilly and Elias, 1998
;
Blob and Biewener, 1999
). In
addition, at the beginning of stance, hip protraction, knee extension, and
ankle extension are all greater (by 7-35°, 35-55°, and 30-45°,
respectively) in salamanders and sprawling lizards
(Ashley-Ross, 1994b
;
Reilly and Delancey, 1997b
;
Irschick and Jayne, 1999
) than
in alligators and iguanas. Thus, whereas alligators and iguanas place the
hindfoot under or behind the knee at touchdown, more sprawling taxa (e.g.
salamanders and sprawling lizards) use greater limb joint extension at
touchdown and are hypothesized to flex these joints to actively pull the body
over the foot (Ashley-Ross,
1994b
,
1995
;
Reilly and Delancey, 1997b
).
Such comparisons of tetrapod kinematics led Ashley-Ross
(1994b
) to conclude that, in
conjunction with femoral retraction, knee flexion and extension are
plesiomorphic features of the tetrapod hindlimb cycle. Alligators differ in
that medial rotation of the femur occurs with little change in knee angle.
Generalized tetrapod hindlimb kinematics also appear to be controlled by
muscle activity patterns that differ from those used by alligators. For
example, the sprawling lizard Sceloporus clarkii exhibits distinct
EMG patterns in which (1) onset of G activity begins late in swing phase to
actively extend the ankle before the foot is placed on the ground, (2) FMTI
has a swing phase burst to extend the knee before placing the foot on the
ground, and (3) TA has a large burst during early stance that could help to
pull the body over the foot (Reilly,
1995). None of these EMG patterns occur in alligators
(Fig. 3F).
Even the common muscular function of using the CFL to power hindlimb
retraction in alligators and more sprawling taxa
(Peters and Goslow, 1983;
Reilly, 1995
;
Gatesy, 1997
) could have a
different effect on femoral loading because of differences in limb positions
used by these animals. In highly sprawling taxa that place the foot far
forward at the beginning of stance, the GRF may be directed posterior to the
long axis of the femur throughout the duration of stance. If true, then the
rotational moment of the GRF and CFL would be in the same direction (both
medial). Such an orientation of the GRF might generate low torsional loads
(reduced femoral shear strains) among highly sprawling species that initially
place the foot far anteriorly, as was found in alligators during the
support-and-propulsion phase. Thus, high torsional loads might be a derived
feature found among some non-parasagittal taxa including alligators, as
opposed to a general feature of non-parasagittal locomotion. Rather than
reflecting an ancestral condition, the limb kinematics, muscle activity
patterns, and femoral loading patterns of alligators appear to be derived
relative to those of other non-parasagittal tetrapods.
Two features of the locomotor apparatus of alligators may result in
reductions in overall locomotor effectiveness. First, alligators limit knee
flexion-extension and femoral adduction during stance phase. Instead, hindlimb
retraction during the support-and-propulsion and limb unloading phases is
associated primarily with femoral medial rotation (together with ankle
plantarflexion). Consequently, effective vaulting over the stance limbs may be
limited. Indeed, walking efficiency is reduced in alligators: although the
center of mass rises and falls with each step, little external mechanical
energy is recovered by the pendulum-like exchange of kinetic and gravitation
potential energies (19.8±2.0%;
Willey et al., 2004). The
second unusual feature of alligator terrestrial locomotion is that the tail is
dragged behind the body rather than elevated off of the ground. The long,
heavy tail causes the center of mass of alligators to lie more caudally (just
in front of the pelvis), so that body weight support is concentrated over the
hindlimb (52%) during locomotion (Willey
et al., 2004
). The constant braking impulse of the tail is
countered by propulsive efforts of the limbs. Indeed, in order to balance the
braking impulse of the tail, the hindlimb exerts four times the accelerative
impulse needed to balance the braking impulse of the forelimb alone
(Willey et al., 2004
). These
necessary modifications in hindlimb function may further limit the ability of
alligators to effectively use vaulting mechanics to recover external
mechanical energy
It is noteworthy that iguanas, which also exhibit substantial femoral
rotation (and torsion; Blob and Biewener,
1999) also drag large tails behind the body. In contrast,
sprawling lizards that lift the tail during locomotion show net propulsive
impulses of the hindlimb that balance the net braking impulses of the forelimb
(our unpublished data) and much (two to three-fold) greater mechanical
efficiency than alligators when walking
(Farley and Ko, 1997
; S.
Reilly, K. Hickey and A. Parchman, unpublished data). With the tail raised,
the hindlimbs are only required to counteract the decelerative impulse of the
limbs and, thus, lizards may exhibit less axial rotation of the femur and,
thereby, lower torsional loads. Experimental verification of these hypotheses
remains to be performed. However, the results of our analyses suggest the
possibility that patterns of femoral loading in quadrupedal, terrestrial
tetrapods may have diversified through evolutionary changes in several
lineages, rather than along a single path.
One consequence of the advent of limb rotation in alligators is that
several muscles that actively shorten to flex and extend limb joints during
stance phase in sprawling (salamanders;
Ashley-Ross, 1994b; lizards:
Reilly, 1995
;
Reilly and DeLancey, 1997b
)
and erect quadrupeds (mammals; Goslow et al.,
1973
,
1981
;
Halbertsma, 1983
;
Smith et al., 1993
;
Vilensky and Gankiewicz, 1990
)
must now act in isometric or even eccentric contraction to stabilize the knee
and ankle during the support-and-propulsion phase. Although hindlimb EMG data
are lacking for iguana, the knee and ankle flexors in alligators are clearly
modulated to stiffen the limb during limb rotation. In addition, the same
basic leg stiffening pattern is modulated to maintain different fixed joint
angles during stance phase across a range of postural heights
(Reilly and Blob, 2003
). This
adds to other recent discoveries (Gillis and Biewener,
2001
,
2002
,
2003
) that counter common
assumptions that homologous muscles are used at the same time in the limb
cycle across quadrupeds, or to move joints in the same way. In addition, motor
patterns in alligator reveal the presence of local and temporal segregation of
muscle functions during locomotion. Local segregation is evident in muscles
lying side by side (such as the ILTIB1, ILTIB2 and AMB1) that are dedicated to
performing different functions in the stance (knee stabilization in the former
two) and swing phases (knee extension in AMB1) of the stride. Furthermore,
only two (PIT, ILTIB1) of our 16 muscles had clear functions in both stance
and swing phases. Most notably, PIT appears to aid other muscles (ADD1, PIFE3)
in supporting the body weight during the stance phase, while it is alone in
counteracting femoral abduction (by the ILFIB, ILFEM) during swing phase.
These results point to several future directions for research on iguanas,
sprawling lizards and semierect mammals that could improve understanding of
the effects of posture, tail dragging, and phylogeny on the diversity of
quadrupedal locomotor mechanisms.
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