Motor control of locomotor hindlimb posture in the American alligator (Alligator mississippiensis)
1 Department of Biological Sciences, Ohio University, Athens, OH 45701,
USA
2 Department of Biological Sciences, Clemson University, Clemson, SC 29634,
USA
* Author for correspondence (e-mail: rblob{at}clemson.edu)
Accepted 27 August 2003
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Summary |
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Previous force platform analyses suggested that upright posture in alligators would require greater activation by hindlimb extensors to counter increases in the flexor moments exerted about joints by the ground reaction force during upright stance. Consistent with these predictions, ankle extensors (gastrocnemius) and knee extensors (femorotibialis internus and iliotibialis 2) exhibit increases in signal intensity during the use of more upright stance. Bone loading data also predicted that activation patterns for hip adductors spanning the length of the femur would not differ between sprawling and more upright posture. Correspondingly, motor patterns of the adductor femoris were not altered as posture became more upright. However, the adductor puboischiofemoralis externus 3, which inserts far proximally on the femur, displays significant increases in burst intensity that could contribute to the greater femoral adduction that is integral to upright posture.
In contrast to patterns in alligators, in mammals EMG burst intensity typically decreases during the use of upright posture. This difference in the motor control of limb posture between these taxa may be related to differences in the relative sizes of their feet. Alligator feet are large relative to the hindlimb and, as a result, the ground reaction force shifts farther from the limb joints during upright steps than in mammals, increasing flexor moments at joints and requiring alligator extensor muscles to exert greater forces to keep the limb in equilibrium. However, several alligator hindlimb muscles show no differences in motor pattern between sprawling and upright posture. The wide range of motor pattern modulations between different postures in alligators suggests considerable independence of neural control among the muscles of the alligator hindlimb.
Key words: locomotion, biomechanics, kinematics, EMG, muscle, electromyography, modulation, neural control, bone stress, posture, evolution, vertebrate, alligator, Sauria, Crocodylia
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Introduction |
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Crocodilian hindlimb musculature, like that of many tetrapods, is highly
redundant, with multiple muscles in different positions capable of producing
each of the major movements (protraction/retraction, abduction/adduction,
flexion/extension) at each joint (Romer,
1923; Gatesy,
1994
,1997
).
As a result, on the basis of anatomical data it is difficult to predict which
muscle activity patterns might be required to change in order for crocodilians
to use more upright posture. However, data on bone loading during locomotion
by American alligators (Alligator mississippiensis; Blob and Biewener
1999
,
2001
) provide a biomechanical
basis for predicting differences in motor control between sprawling and
upright stance (Zernicke and Smith,
1996
). In alligators, in vivo bending strains and
stresses are greater on dorsal and ventral femoral cortices when more upright
posture is used (Blob and Biewener,
1999
,
2001
). Because the magnitude of
the ground reaction force does not change significantly as alligators use more
upright posture, these changes in bone loading must be the result of changes
in the forces exerted by limb muscles (Blob
and Biewener, 2001
). One possibility is that hip adductors (on the
ventral aspect of the femur) might exert less force during more upright steps
(Fig. 1A). This would cause the
adductors to mitigate bending due to the ground reaction force less
effectively, contributing to higher dorsal and ventral femoral bending loads
(Blob, 1998
;
Blob and Biewener, 2001
).
However, analyses of joint equilibrium based on force platform data do not
indicate posture-related changes in adductor force. Instead, force platform
data indicate a cascade of changes in locomotor mechanics during upright
posture that begin at the ankle (Blob and
Biewener, 2001
; Fig.
1B). During the use of more upright limb posture, the center of
pressure of the ground reaction force is shifted anteriorly, away from the
ankle. This shift increases the moment arm of the ground reaction force at the
ankle; as a result, ankle extensors (e.g. gastrocnemius) must exert higher
forces to maintain joint equilibrium by countering the larger ankle flexor
moment during more upright steps. Because gastrocnemius also spans the knee,
it makes a greater contribution to the flexor moment at the knee during more
upright steps, and knee extensors (femorotibialis and iliotibialis, on the
dorsal aspect of the femur) must exert greater force to counter this moment
and prevent the knee from collapsing. These increases in knee extensor forces
could then raise dorsal and ventral femoral strains and stresses as alligators
use more upright posture (Blob and Biewener,
1999
,
2001
).
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Although force platform data suggest that the activity patterns of several
hindlimb muscles might be modulated between sprawling steps and high walk
steps in crocodilians, force platforms provide only an indirect indication of
muscle action. In the present study, we use electromyographic (EMG) recordings
from the hindlimb muscles of American alligators synchronized with video of
locomotor kinematics to test for modulations of hindlimb motor patterns
correlated with the use of different limb postures. EMG patterns have been
recorded for alligator hindlimb muscles during the high walk (Gatesy,
1994,
1997
), but explicit analyses
of postural effects on muscle motor patterns have not been performed
previously. Our analyses will, therefore, provide insight into the basis for
the ability to use both sprawling and more upright limb postures, a trait that
has made crocodilians feature prominently in many analyses of the evolution of
tetrapod locomotion (e.g. Bakker,
1971
; Charig,
1972
; Kemp, 1978
;
Brinkman, 1980
;
Parrish, 1987
;
Gatesy, 1991
;
Reilly and Elias, 1998
; Blob
and Biewener, 1999
,
2001
). In addition, our
analyses of motor pattern modulation across limb postures in alligators will
provide a new data set for comparison with other studies of behavioral
modulation of motor patterns (e.g. Gruner
and Altman, 1980
; Nilsson et
al., 1985
; Buchanan et al.,
1986
; Macpherson,
1991
; Johnston and Bekoff,
1996
; Gillis and Blob,
2001
), allowing us to explore potential general patterns in how
muscle activity and patterns of recruitment change to allow the same
morphological structure to perform a variety of tasks.
In performing these analyses, we recognize that the relationship between
EMG and force production in muscles is not necessarily direct and can be
complicated by several factors (Loeb and
Gans, 1986). However, force/length curves that could clarify these
relationships are not currently available for alligator limb muscles.
Therefore, our premise that increases in the force exerted by a muscle would
be reflected in increases in the intensity of EMG bursts for that muscle must
be regarded as an assumption. However, in the absence of contradictory
evidence, we believe that this assumption is a reasonable starting point from
which to generate and test hypotheses about how the activation of alligator
limb muscles should be expected to differ during the use of sprawling and more
upright limb posture.
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Materials and methods |
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Kinematics
The alligators were filmed on a treadmill under strobe lights at 200 fields
s1 using a NAC HSV-400 high-speed video system, while muscle
activity patterns were simultaneously recorded. Both lateral and dorsal views
of the alligators were filmed (using mirrors) during locomotion on a 70
cm-long canvas treadmill. Reflective landmarks (2 mm-diameter dots visible in
both the lateral and dorsal views) were painted on the skin of the alligators
to mark a position on the vertebral column, the position of each hip joint
(directly over the acetabulum) and three landmarks on the right hindlimb: the
knee joint (on the anterolateral point of the knee when flexed), the ankle
joint (posterolateral point of the ankle when flexed) and the foot (lateral
aspect of the metatarsalphalangeal articulation). 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, following the conventions of Reilly and Elias
(1998
).
The knee and ankle angles calculated were the actual three-dimensional
angles for these joints based on the landmarks above. Femoral movements were
quantified using two three-dimensional angular variables: hip retraction
(indicating retraction/protraction movements relative to the longitudinal axis
of the pelvis) and hip adduction (indicating adduction/abduction position
relative to the mediolateral axis of the pelvis). Femoral retraction angle was
measured relative to a line from the acetabulum to the trunk landmark. This
calculation produces angles that are 510° 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 essentially identical (within 510%:
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 angles as 90° (Bakker,
1971
; Charig,
1972
; Parrish,
1987
; Blob, 2001
).
Our method of calculating femoral adduction also accounts for the slight roll
of the pelvis about a longitudinal axis (''6° to each side:
Gatesy, 1991
) and, thus,
effectively represents the angle between the femur and the horizontal plane of
the body of the alligator. This convention for calculating femoral adduction
was chosen over reference to the absolute horizontal and sagittal planes
because it represents limb motion with reference to the body of the animal,
which should be most relevant to the actions of muscles (attached to the body)
that are examined in this study. However, from a practical perspective,
because pelvic roll is not very large in alligators
(Gatesy, 1991
) the difference
between the convention we employ here and conventions that refer to absolute
planes (e.g. Blob and Biewener,
2001
) are minimal. Although other studies (e.g.
Gatesy, 1991
;
Irschick and Jayne, 1999
) have
used different conventions for some of the angular calculations we report
here, the conventions we have used are appropriate for the purposes of this
study. Most kinematic angles were calculated and graphed to indicate the
general position and direction of movement of limb segments for comparison
with patterns of muscle activation (e.g. to determine whether a muscle was
active during swing-phase protraction or stance-phase retraction). The only
quantitative kinematic data that we extracted for use in further analyses were
values of femoral adduction at mid-stance (see Analyses and statistical
considerations below), a time during the stride cycle when any differences in
results among approaches for angular calculations would be minimized.
Electromyography
We examined the activity patterns of 12 different alligator hindlimb
muscles (Fig. 2) during strides
in which alligators used a range of femoral posture angles (ranges for each
individual are presented in Table
1). Femoral adduction angle at mid-stance was used as the
`postural angle' for each stride to reflect the degree of adduction when the
femur is approximately perpendicular to the pelvis. Although we did not record
from all of these muscles in each of our five experimental alligators, we
recorded data from seven of these muscles in multiple individuals (see
Myology), and it is upon these data that our primary conclusions are based
(see Results). Muscle activity patterns (motor patterns) of limb muscles (all
on the right side of the body) were quantified by recording electrical
activity patterns (EMGs) during treadmill locomotion. Electromyographical
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. The bared metal tips
of each bifilar insulated electrode were 0.5 mm long. Electrodes were
implanted percutaneously through the skin directly into the belly of each
muscle. The bundle of electrodes was glued together and sutured to a scale on
the midline of the animal, dorsal to the pelvis. Animals completely recovered
from anesthesia within two hours, and all synchronized EMG and kinematic data
were recorded during the following two hours. Animals were rested
(approximately 1530 min) between bouts of walking (45 s maximum).
Immediately following the experiment the animal was euthanized by overdose of
anesthetic and preserved in 10% formalin. Electrode position was then
confirmed by dissection. EMG data were considered valid for analysis only for
preparations in which the electrode lay completely within the muscle.
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EMG signals were amplified 10 000 times using differential AC amplifiers (model 1700; AM Systems, Carlsborg, WA, USA) with a bandpass of 1003000 Hz (and a 60 Hz notch filter) and then recorded on a multichannel FM tape recorder (XR-5000; TEAC, Montebello, CA, USA) 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 an analog-to-digital converter (Keithley, Cleveland, OH, USA) and a microcomputer. The effective sample rate for each channel was 10 000 Hz at 12-bit resolution. 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.
Custom software was used to digitize several standard EMG variables to quantify motor patterns from each muscle for each stride analyzed. For all muscles, these included: times of burst onset and offset, relative to the beginning of stance; burst duration; burst duration normalized by stance duration; the integrated area of rectified burst signals; mean burst amplitude (integrated area divided by burst duration); and integrated area normalized by stance duration. For muscles active primarily during the swing phase of strides, the integrated areas and durations of activity bursts normalized by the duration of swing phase were also calculated. These last two variables were calculated to control for possible changes in stance (or swing) duration between different postures.
Myology
The 12 muscles from which we recorded EMGs
(Fig. 2)included muscles that
spanned the hip, knee and ankle joints, allowing us to test the hypotheses of
muscular control of limb posture that were suggested by force platform
analyses of alligator locomotion (Blob and
Biewener, 2001). Detailed descriptions of the anatomy of these
structures are provided in a number of studies. To facilitate understanding of
the analyses we present in this report, in this section we briefly summarize
the origins, insertions and hypothesized functions of these muscles that have
been outlined in previous anatomical
(Romer, 1923
) and
electromyographic (Gatesy,
1997
) research. For each muscle, we list an abbreviation, together
with the figure in which the muscle is illustrated and the number of
individuals from which we recorded data in parentheses.
Stance-phase femoral retractors
Flexor tibialis externus (FTE; Fig.
2A; 1 individual). Origin: postacetabular process of ilium.
Insertion: proximally on proximal tibia, distally via auxiliary
tendon to ankle.
Stance-phase femoral adductors
Adductor femoris, head 1 (ADDFEM1; Fig.
2C; 3 individuals). Origin: ventral aspect of ischium. Insertion:
ventral femoral shaft.
Puboischiofemoralis externus, head 3 (PIFE3; Fig. 2C; 2 individuals). Origin: ventral aspect of ischium. Insertion: postero-ventral aspect of the proximal femur.
Puboischiotibialis (PIT; Fig. 2C; 1 individual). Origin: anterior aspect of ischium, ventral to acetabulum. Insertion: medial aspect of proximal tibia. Additional hypothesized functions: knee flexor at stanceswing transition.
Stance-phase knee extensors
Femorotibialis internus (FEMTIB; Fig.
2B; 3 individuals). Origin: most of the femoral shaft. Insertion:
knee extensor tendon.
Iliotibialis, head 1 (ILTIB1; Fig. 2B; 1 individual). Origin: anterior aspect of the rim of the iliac blade. Insertion: surface of the femorotibialis leading into the knee extensor tendon. Additional notes: no previous EMG data.
Iliotibialis, head 2 (ILTIB2; Fig. 2B; 2 individuals). Origin: central aspect of the rim of the iliac blade. Insertion: surface of the femorotibialis leading into the knee extensor tendon.
Stance-phase ankle extensors
Gastrocnemius (GAST; Fig.
2A; 3 individuals). Origin: ventral aspect of distal femur.
Insertion: tuber calcis of ankle. Additional notes: no previous EMG data.
Swing-phase femoral protractors
Puboischiofemoralis internus, head 2 (PIFI2;
Fig. 2A; 1 individual). Origin:
ventral aspect of lumbar vertebrae. Insertion: dorsal aspect of the proximal
femur. Additional hypothesized functions: adducts femur during late swing.
Swing-phase femoral abductors
Iliofemoralis (ILFEM; Fig.
2C; 1 individual). Origin: blade of the ilium posterior to
acetabulum, deep to iliotibialis. Insertion: lateral and posterior femoral
shaft.
Swing-phase knee extensors
Ambiens, head 1 (AMB1; Fig.
2A; 2 individuals). Origin: junction of the ilium and
preacetabular ischium, anterior to the acetabulum. Insertion: extensor tendon
attaching to the tibia.
Swing-phase ankle flexors
Tibialis anterior (TA; Fig.
2A; 2 individuals). Origin: anterior aspect of tibia and fibula.
Insertion: dorsal aspect of metatarsals. Additional notes: no previous EMG
data.
Analyses and statistical considerations
We performed two analyses to examine how alligators modulate muscle
activity between low- (sprawling) and high-walk limb postures. First, we
compared mean patterns of EMG burst timing for low (30° femoral
adduction) and high (
50° femoral adduction) postured strides with
mean kinematic profiles for three-dimensional joint movements reported in the
detailed analyses of alligator joint kinematics (at 0.146 m
s1) by Reilly and Elias
(1998
). Second, for each
individual animal we regressed the values of each EMG variable for each muscle
on femoral posture angle at mid-stance (ranges in
Table 1). The correlation
coefficients and probabilities of significance from these regressions allowed
us to evaluate whether changes in the timing or intensity of activation of
individual muscles were required for alligators to use sprawling
versus upright postures. Because we examined multiple correlations
for each muscle, we adjusted for multiple comparisons within individuals using
the more conservative sequential Bonferroni tests
(Rice, 1989
) to determine
which EMG variables exhibited significant changes with posture.
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Results |
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Our primary conclusions are based upon the seven muscles in which we recorded EMGs from multiple individuals. We report supplementary data from single individuals for additional muscles in order to provide a more comprehensive picture of how muscle activation patterns must change in order for alligators to use a high walk versus a sprawl. EMG data from single individuals must be interpreted cautiously. However, none of the muscles that were tested in multiple individuals showed markedly different changes in EMG pattern between sprawling and upright posture among those individuals. Given this consistency in EMGs among individuals, we are confident that even the patterns we report for muscles recorded in single individuals are likely to be reliable indicators of general patterns in alligators.
General patterns of alligator hindlimb muscle activation
Stance phase
Seven of the alligator thigh muscles that we examined show major EMG bursts
during the stance phase of locomotion (Fig.
3). For several muscles, the onset of activation is nearly
synchronous, so that stance-phase muscles are activated in four groups, three
of which begin activity during the swing phase prior to stance. The first
group consists of ILTIB1 (knee extensor) and PIT (hip adductor and knee
flexor), which onset together midway through swing phase. The second group,
including the hip adductor ADDFEM1 and the knee extensors ILTIB2 and FEMTIB,
onset together two-thirds of the way through swing phase. The third group
consists of the hip adductor PIFE3, which is activated near 85% swing-phase
duration, and the fourth group consists of the femoral retractor FTE, which is
activated at the beginning of stance.
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One of the crural muscles examined, the ankle extensor GAST, is active during stance, with an onset just after that of FTE (<10% stance duration) and an offset just after that of ILTIB2 and FTE (>80% stance duration).
Gatesy (1997) measured EMGs
for many of the same stance-phase muscles during walking in alligators,
including ADDFEM1, FEMTIB, FTE, ILTIB2, PIFE3 and PIT. Patterns measured for
those muscles in the present study were largely consistent with those
described by Gatesy (1997
),
although ILTIB2 was active for a somewhat longer portion of the stride in the
present study (offset at almost 60% stride cycle) than in Gatesy's study
(offset at 3050% stride cycle).
Swing phase
Four of the alligator thigh muscles we examined show major EMG bursts
during swing phase (Fig. 3).
ILFEM, a hypothesized femoral abductor, is activated nearly 90% through stance
duration and ceases activity nearly 30% through swing duration. PIT, the
hypothesized hip adductor and knee flexor that is active during stance, shows
a second burst of activity that is almost synchronous with that of ILFEM.
PIFI2 (a hypothesized hip protractor) and AMB1 (a hypothesized hip protractor
and knee extensor) are activated nearly synchronously just at the offset of
activity by ILFEM and PIT; both PIFI2 and AMB1 remain active for almost all of
the rest of swing phase.
One of the crural muscles examined, the hypothesized ankle flexor TA, is activated just after the start of swing phase and ceases activity at nearly 70% through swing duration.
Gatesy (1997) also measured
EMGs for some of the same swing-phase muscles during walking in alligators,
including AMB1, ILFEM and PIFI2. Patterns measured for these swing-phase
muscles were also generally consistent with those described by Gatesy
(1997
), although the offset of
ILFEM was somewhat earlier in the present study (nearly 80% stride cycle) than
in Gatesy's study (9095% stride cycle).
Changes in hindlimb motor patterns accompanying the use of more
upright posture
Four of the five alligators tested showed no significant relationship
between limb posture and the duration of swing phase, stance phase or the
entire stride (Table 1). In a
single alligator (Individual 2), stride duration and stance duration decreased
significantly with the use of upright posture. However, with the exception of
EMG changes for FTE (for which Individual 2 was the only animal recorded), all
of the changes in muscle motor pattern exhibited by Individual 2 were also
exhibited by at least one additional individual in which phase and stride
durations were not correlated with posture
(Table 2). Therefore, we are
confident that the motor pattern changes we observed were related to
differences in limb posture rather than differences in footfall timing.
Stance phase
Several stance-phase muscles exhibit significant changes in EMG burst
timing, intensity or both as posture becomes more upright, but a few maintain
constant patterns as different postures are used
(Fig. 3). These patterns of
change (or lack of change) in EMGs were remarkably consistent among the
individual alligators examined. For example, in both individuals in which EMGs
were measured for the ankle extensor GAST, neither burst timing nor duration
changed during the use of more upright postures; however, all three indicators
of burst intensity (rectified burst area, mean burst amplitude and mean burst
amplitude normalized by stance duration) increased significantly as posture
became more upright (Fig. 4;
Table 2). Two of the three knee
extensors examined, FEMTIB and ILTIB2, showed similar patterns. Neither muscle
showed significant changes in burst timing or duration as different postures
were used. However, both individuals in which ILTIB2 was examined showed
increases in burst area, mean burst amplitude and mean burst amplitude
normalized by stance duration (Table
2). In addition, all three individuals in which FEMTIB was
examined showed significant increases in mean burst amplitude and normalized
mean burst amplitude during the use of more upright posture, and two of these
three also showed significant increases in rectified area (with the third
showing a nearly significant increase; Fig.
4; Table 2). The
third knee extensor examined, ILTIB1, was only recorded in one individual but
showed no significant changes in activity as posture became more upright
(Fig. 3;
Table 2).
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The stance-phase femoral retractor, FTE, displays a more complicated pattern of posture-related activation changes than the ankle or knee extensors (Fig. 3). The onset and offset of FTE bursts shift earlier relative to the beginning of stance during more upright steps (Fig. 3), but offset shifts more than onset, so that upright steps have shorter-duration FTE bursts (Table 2). Rectified burst area does not change, however, causing both mean burst amplitude and normalized mean burst amplitude to increase for FTE with the use of more upright posture (Table 2). Two stance-phase adductors (PIFE3 and PIT) also showed posture-related changes in burst pattern (Fig. 3). In both individuals in which PIFE3 was examined, burst onset and offset shifted earlier, relative to the beginning of stance, among more upright steps. PIFE3 burst duration also decreased significantly in one individual (and nearly significantly in the other) during steps in which more upright posture was used. However, the rectified area of PIFE3 bursts increased as posture became more upright in both individuals, as did mean burst amplitude and mean normalized burst amplitude (Table 2). PIT activity was recorded in only one individual, but in that animal it also showed a significant increase in normalized mean amplitude among more upright steps (Table 2). Like the knee extensors, however, one of the femoral adductors, ADDFEM1 (sampled in three animals), showed no significant changes in burst timing or intensity as posture became more upright (Table 2).
Swing phase
One swing-phase muscle, the knee extensor AMB 1, exhibited no significant
changes in burst timing or intensity during more upright steps
(Table 2;
Fig. 3). Another muscle, the
limb protractor PIFI2, exhibited no significant changes in burst intensity,
onset or offset with the use of upright posture and only a marginally
significant increase in normalized burst duration
(Table 2). However, the ankle
flexor TA exhibited increases in burst area, mean burst amplitude and mean
normalized burst amplitude that paralleled those observed in the stance-phase
ankle extensor GAST (Table 2). The swing-phase burst by PIT also exhibited posture-correlated changes: the
offset of the swing phase burst of this muscle shifted earlier relative to
foot-down among more upright steps, producing a shorter burst duration with
more upright posture (Table 2).
The remaining swing-phase muscle examined, ILFEM, exhibited posture-related
changes in both burst timing and intensity: burst duration [by a later shift
in onset, which is marginally significant (P=0.027)] and rectified
area both decreased as posture became more upright, but mean burst amplitude
and mean normalized burst amplitude both increased as more upright posture was
used.
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Discussion |
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Although PIT and PIFE3 show burst intensity modulations that were not
predicted by force platform analyses, increases in burst intensity by
these muscles during upright stance are not inconsistent with the model that
Blob and Biewener (2001)
proposed, in which higher femoral strains during upright posture result from
correlated increases in forces exerted by ankle and knee extensor muscles
(Fig. 1B). The clearest
evidence for an increase in adductor force is in PIFE3, in which all three
indicators of burst intensity increase during upright stance
(Table 2). However, this muscle
inserts on the proximal femur and does not span the femoral midshaft; thus,
PIFE3 does not contribute directly to midshaft strains and stresses
(Blob and Biewener, 2001
). An
increase in PIFE3 force (spanning the ventral aspect of the hip) might lead to
a corresponding increase in ILTIB2 force (spanning the dorsal aspect of the
hip) in order to maintain joint equilibrium but would not produce femoral
bending that countered the dorsal compression of the femur imposed by ILTIB2
and the other knee extensors. As a result, an increase in PIFE3 force during
upright posture can be accommodated by Blob and Biewener's model of femoral
loading in alligators (Fig. 1B)
because it either would not alter femoral load patterns or, if anything, would
reinforce the pattern of strains and stresses identified in bone loading
analyses. Even an increase in force exerted by PIT might not significantly
counter the dorsal bending imposed on the femur by the knee extensors, because
the cross-sectional area (proportional to the force the muscle exerts:
Alexander, 1974
) of PIT in
alligators is only one-third that of adductor femoris
(Blob and Biewener, 2001
),
which shows no change in activation as posture becomes more upright.
It should be noted that the alternative
(Fig. 1A) to Blob and
Biewener's favored model (Blob and
Biewener, 2001) for how changes in muscle activation produce
increases in femoral stress during upright posture in alligators required that
adductor force decrease, thereby countering the ground reaction force less
effectively and raising femoral stresses. Increases in PIT and PIFE3 burst
intensity might not have been predicted by Blob and Biewener's preferred
model, but they run distinctly counter to its alternative. In addition, the
fact that at least some of the femoral adductors display more intense EMG
bursts during upright stance is functionally reasonable, as more intense
activity by these muscles could help to produce the greater femoral adduction
that upright posture entails.
Specific muscular mechanisms underlying the use of different limb
postures in alligators: interspecific comparisons and implications for neural
control
In order for alligators to use upright locomotion rather than sprawling
locomotion, changes in EMG burst timing and/or intensity are required for
eight of the 12 hindlimb muscles that we studied, including both stance- and
swing-phase muscles. A number of these changes in activation pattern between
sprawling and upright stance directly reflect the kinematic differences
between these two postures. For example, the earlier onset of activity by the
retractor FTE during upright posture is probably responsible for the
significantly smaller maximum protraction of the femur during high walks
relative to sprawling steps (Reilly and
Elias, 1998). In addition, as noted previously, the increased
burst intensity of the hip adductors PIFE3 and PIT during upright steps
probably contributes to the greater femoral adduction that is integral to
upright limb posture in alligators. Similarly, greater burst intensity by the
knee extensors FEMTIB and ILTIB2 probably contributes to the greater
stance-phase knee extension typical of high walks, and increased burst
intensity of the swing-phase ankle flexor TA may contribute to the earlier
attainment of maximum ankle flexion during upright steps
(Fig. 3;
Reilly and Elias, 1998
).
However, the mechanical requirements of locomotion with upright limb posture
in alligators also appear to contribute to some changes in muscular activation
between sprawling and upright stance in these animals
(Zernicke and Smith, 1996
),
particularly for the stance-phase ankle extensor GAST. Ankle movements are
similar between sprawling and high-walk steps for most of stance phase
(Reilly and Elias, 1998
),
providing little kinematic basis to explain posture-related changes in GAST
activity. However, in the context of the increased ankle flexor moment induced
by the ground reaction force during upright steps in alligators
(Blob and Biewener, 2001
), an
increase in GAST burst intensity is clearly explained as a mechanism for
maintaining the equilibrium of ankle joint moments despite a change in limb
posture (Fig. 1B).
Hindlimb motor pattern data through ranges of limb postures are available
for two other species: domestic cats
(Trank et al., 1996), which
use a crouched posture during predatory stalking
(Leyhausen, 1979
), and humans
(Grasso et al., 2000
). In
studies of each of these two species, motor patterns of hindlimb muscles were
recorded for narrow ranges of speeds over a broad range of limb postures. In
contrast to alligators, in both humans and cats the intensity of EMG bursts by
hindlimb extensor muscles is typically greater during crouched posture than
upright posture (Trank et al.,
1996
; Grasso et al.,
2000
). One possible explanation for these patterns in mammals is
that crouched posture demands greater motor recruitment because it requires
muscles to contract at lengths that are not optimal for force production
(Trank et al., 1996
). However,
crouching might also lead to more intense bursts of motor activity in mammals
because, in mammals, crouched posture increases the flexor moments of the
ground reaction force about joints (Biewener,
1989
,
1990
), requiring extensor
muscles to exert greater forces to keep the joints in equilibrium
(Perell et al., 1993
;
Trank et al., 1996
;
Grasso et al., 2000
). Because
humans and cats have fairly small feet relative to the length of their
hindlimb, when they use an upright limb posture they align the limb with the
ground reaction force, decreasing its moment arms about the joints and,
thereby, decreasing joint flexor moments and the extensor muscle forces needed
to counter them in order to prevent the limb from collapsing (Biewener,
1989
,
1990
). Alligators, by contrast,
have much longer feet (relative to their hindlimbs) than either humans or cats
(Blob and Biewener, 2001
).
During upright steps, the ankle is lifted from the substrate earlier than in
sprawling steps and, as a result, the ground reaction force shifts far
anteriorly along the foot, increasing its flexor moment arm at the ankle and
requiring greater ankle extensor forces for the maintenance of joint
equilibrium during upright posture (Blob
and Biewener, 2001
). Thus, it is entirely possible that the same
principles (i.e. joint equilibrium) are ultimately mediating the modulation of
muscle activity that produces different postures in mammals and alligators,
but that differences in the limb anatomy of these animals lead to the
different patterns of modulation that these species use in order to achieve
upright and non-upright locomotor postures.
Changes in motor pattern between sprawling and upright posture are
widespread in the alligator hindlimb but they are not universal. In fact,
muscles belonging to the same functional group (e.g. the knee extensors ILTIB1
and ILTIB2), as well as muscles that typically burst on or off simultaneously
(e.g. ILTIB1 and PIT), can display very different modulations of EMG pattern
between sprawling and upright steps, with some muscles maintaining consistent
motor patterns through the full range of limb postures. Such variety in the
behavioral modulation of activity patterns among muscles has been documented
in the limb muscles of a wide range of tetrapod species
(Gillis and Blob, 2001) and
suggests considerable independence of neural control among the muscles of the
alligator hindlimb. Immutability of the motor pattern of a muscle between
behaviors has been cited as evidence that central pattern generator input
dominates its neural control, with supraspinal input and motion-related
feedback playing less important roles
(Buford and Smith, 1990
;
Pratt et al., 1996
). Although
some hindlimb muscles of alligators showed no difference in motor pattern with
the use of different postures (e.g. ILTIB1, ADDFEM), the possibility that
other behaviors (e.g. walking at faster speeds:
Nilsson et al., 1985
;
Reilly, 1998
) might elicit
changes in the activation patterns of these muscles remains to be tested. The
specific roles of some alligator hindlimb muscles may not be well understood
until their actions have been measured in a wide range of behaviors that more
completely sample the functional repertoires of these animals.
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