SUMMARY

The human gluteus maximus is a distinctive muscle in terms of size, anatomy
and function compared to apes and other non-human primates. Here we employ
electromyographic and kinematic analyses of human subjects to test the
hypothesis that the human gluteus maximus plays a more important role in
running than walking. The results indicate that the gluteus maximus is mostly
quiescent with low levels of activity during level and uphill walking, but
increases substantially in activity and alters its timing with respect to
speed during running. The major functions of the gluteus maximus during
running are to control flexion of the trunk on the stance-side and to
decelerate the swing leg; contractions of the stance-side gluteus maximus may
also help to control flexion of the hip and to extend the thigh. Evidence for
when the gluteus maximus became enlarged in human evolution is equivocal, but
the muscle's minimal functional role during walking supports the hypothesis
that enlargement of the gluteus maximus was likely important in the evolution
of hominid running capabilities.

Introduction

Bipedalism has long been considered a characteristic feature of the hominid
lineage (Darwin, 1859), and
recent fossil evidence suggests that the very earliest hominids may have been
bipedal in some manner (Haile-Selassie,
2001; Zollikofer et al.,
2005). Not surprisingly, many aspects of the hominid
musculoskeletal system, especially in the leg and foot, have undergone
substantial reorganization for bipedal posture and locomotion (see
Lovejoy, 1988;
Aiello and Dean, 1990;
Ward, 2002). One of these
features may be the gluteus maximus (GM). The human GM is anatomically
distinctive compared to other non-human primates in several respects, notably
in its overall enlargement, in the expansion of its cranial portion and in the
loss of its caudal portion. Since Cuvier
(Cuvier, 1835), anatomists have
speculated that the distinctive human GM is an adaptation for either walking
or maintaining upright posture, but electromyographic (EMG) studies have shown
that the GM has little or no activity in walking or normal upright standing
(Joseph and Williams, 1957;
Karlsson and Jonsson, 1965;
Stern, 1972;
Marzke et al., 1988). Instead,
the human GM is primarily active during climbing (Zimmerman et al., 1994), as
well as running and other activities that involve stabilizing the trunk
against flexion (Stern et al.,
1980; Marzke et al.,
1988; McLay et al.,
1990). Although there has been no systematic comparison of GM
activity during walking and running (see below), the available evidence has
led to the proposal that enlargement and reorganization of the GM may have
played a role in, and possibly were selected for, the evolution of human
endurance running capabilities (Bramble and
Lieberman, 2004). In order to test this hypothesis, however, more
data are needed on how the GM functions during running versus
walking. This study therefore compares GM activity, combined with trunk and
hindlimb kinematics, during bipedal walking and running in humans to test
several hypotheses about the function and evolution of this distinctive
muscle.

Comparative anatomy

To test hypotheses about GM function during locomotion in humans, it is
useful to begin with a comparison of the muscle's anatomy and function in
humans versus our closest relatives, the great apes. The human GM
differs not only in relative size but also in its pattern of origin and
insertion (Fig. 1). In apes,
the GM has two very distinctive compartments with different origins and
insertions. The more cranial portion, the gluteus maximus proprius (GMP), is a
thin sheet of muscle that arises from the gluteal aponeurosis and the
sacroilliac ligament, from the dorsal aspect of the sacrum, and from the upper
portion of the coccyx; the GMP inserts on the iliotibial tract
(Stern, 1972;
Sigmon, 1975;
Aiello and Dean, 1990). The
more caudal portion, the gluteus maximus ischiofemoralis (GMIF), comprises by
far the greatest proportion of the ape GM. This thicker portion of the muscle
arises primarily from the ischial tuberosity
(Stern, 1972), and inserts
along the entire lateral aspect of the femur all the way from the gluteal
tuberosity to the lateral epicondyle
(Stern, 1972;
Swindler and Wood, 1973;
Sigmon, 1975;
Aiello and Dean, 1990;
Lovejoy et al., 2002). The GMP
and GMIF are considered two separate muscles in the orangutan
(Sigmon, 1975).

The most substantial difference between humans and apes is that humans lack
the GMIF and have only an enlarged GMP portion of the muscle (hereafter
referred to as the human GM). The human GM arises from several sites including
the broad, roughened surface on the superior margin of the posterior portion
of iliac crest, the gluteal fascia that covers the gluteus medius, the fascial
aponeurosis of the erector spinae on the sacrum, the posterior surface of the
inferior portion of the sacrum, the lateral aspect of the upper coccyx, and
the sacrotuberous ligament (see Aiello and
Dean, 1990; Standring,
2005). The fibers from these various sites of origin unite to form
a broad, thick, quadrilaterally shaped muscle with thick fascicular bundles.
Fibers from the more cranial sites of origin primarily end in a thick laminar
tendon that inserts on the iliotibial tract; some fibers from deeper portions
of the muscle insert onto the gluteal ridge of the femur, generally on the
proximal 25% of the femur (Stern,
1972).

Comparison of gluteus maximus anatomy in Pan troglodytes (A,B) and
Homo sapiens (C,D). Note that the gluteus maximus in Pan has
a cranial component, the gluteus maximus proprius (GMP), and a caudal
component, the gluteus maximus ischiofemoralis (GMIF); humans have just the
GMP, but it functions primarily like the ape GMIF. The GMP in humans is much
thicker and larger than either portion of the GM in apes. The asterisk
indicates the approximate location of GM electrodes used in this study.

Although humans lack a GMIF, the GM as a whole is relatively larger in
humans because of considerable expansion of the muscle's GMP portion. The GM
as a whole is approximately 1.6 times larger relative to body mass in humans
compared to chimpanzees (Thorpe et al.,
1996; Voronov,
2003). Dissections indicate that the GM comprises 18.3% of the
total mass of the hip musculature in humans, compared to 11.7% and 13.3% for
chimpanzees and gorillas, respectively
(Haughton, 1873;
Zihlman and Brunker,
1979).

Comparative function

A number of researchers have examined the functional implications of the
anatomical differences between the human and non-human primate GM. In terms of
function, the human GM is primarily an extensor of the hip, although its
anterior and posterior fibers can be medial or lateral rotators, respectively.
In contrast, the GMP in apes acts primarily as an abductor of the hip because
it passes lateral to the hip joint. Despite differences in origin and
insertion, the ape GMIF functions somewhat like the human GM as an extensor
and lateral rotator of the hip (Stern,
1972; Tuttle et al.,
1975; Tuttle et al.,
1978; Tuttle et al.,
1979). It has been suggested
(Stern, 1972) that differences
in femoral insertion between humans and nonhuman primates are mostly explained
by pelvic reorganization for bipedality. In particular, the reduced and more
proximal insertion of the GM on the femur in humans may be a function of the
reduced resting length of caudal GM fibers when the femur is in line with the
trunk, rather than at a 90° angle, as in a primate quadruped
(Stern, 1972). Stern also
noted (Stern, 1972) that
angulation of the sacrum in upright humans increases the leverage of the GM
during extension.

Although the GM has an apparently minor role during walking, several
studies have found GM activity to be important in running. The GM was reported
to be active at strong to moderate levels at the end of swing phase and during
the first third of stance during running
(Mann and Hagy, 1980a;
Mann and Hagy, 1980b;
Montgomery et al., 1984; Nilsson et al.,
1985). In addition, it has been reported that GM activity during
running peaks near the time of footstrike, and has a similar pattern of
contract to the hamstrings (Jonhagen et
al., 1996). Unfortunately, only one study has directly compared GM
activity in walking and running (Stern et
al., 1980), and only in a general qualitative way in one subject.
Stern et al. nonetheless found that GM contractions during walking are
`minimal' compared to the `considerable' increases in GM activity during
jogging and running, particularly in the cranial portions of the muscle
(Stern et al., 1980). In a
comparison of level versus incline running, Swanson and Caldwell
further showed that incline running (30°) at 4.5 m s-1
increased the intensity of GM contractions and resulted in an earlier onset
relative to footstrike (Swanson and
Caldwell, 2000). However, while EMG analyses of the GM generally
indicate a far more important role in running than walking, there has yet to
be a comprehensive and quantitative comparison of GM function in both
gaits.

Running as a potential explanation for GM enlargement

When viewed in the context of comparative anatomy, the studies reviewed
above suggest three functional explanations other than bipedal walking that
may help account for the distinctive morphology of the GM in humans. The first
is climbing, since the GMIF has been shown to contract in conjunction with the
hamstrings to extend the hip during climbing in apes
(Tuttle et al., 1975;
Stern and Susman, 1981),
whereas in humans the more cranial portions play a role in similar activities
such as getting up from a chair or rising from a squatting position. Thus
reorganization of the GM may have been necessary for the muscle to be involved
in climbing in early bipeds. Although the climbing hypothesis has not received
much attention, presumably because the activity does not appear to be a major
part of the modern human locomotor repertoire, tree climbing may have been an
important activity among early hominids
(Susman et al., 1984). A
second possibility, noted above, is that an enlarged GM evolved in bipedal
hominids as a means to help control flexion of the trunk during foraging
activities such as digging, throwing or clubbing that require leverage and/or
stabilization of the trunk (Marzke et al.,
1988). Since an upright trunk may be subject to greater flexion
during uphill walking or carrying heavy objects, a related hypothesis is that
the GM in humans is enlarged for controlling flexion of the trunk during
non-steady bipedal walking.

A final hypothesized functional explanation for enlargement of the human GM
is running, which is biomechanically very different from walking, and appears
to stimulate higher levels of EMG activity than walking as noted above. As
Bramble and Lieberman have argued (Bramble
and Lieberman, 2004), humans are exceptional endurance runners
compared to other mammals in terms of several criteria such as speed and
distance. While many of the functional bases for human running clearly stem
from adaptations for bipedal walking, humans have a number of derived
features, such as elongated leg tendons, which may improve endurance running
performance but play little or no role in walking
(Bramble and Lieberman, 2004).
The enlarged GM may be such a feature.

Three major biomechanical differences between running and walking are
particularly relevant to GM function. First, running differs from walking in
having an aerial phase that generates a much higher ground reaction force
(GRF) at heel strike (HS) when the body collides with the ground. GRFs at HS
in running are typically twice as high as during walking, and may exceed four
times body weight at peak endurance speeds
(Keller, 1996). In addition,
during endurance running (although not necessarily sprinting), the trunk is
more flexed at the hip than during walking, typically by approximately 10°
(Thorstensson et al., 1984).
Thus during running the hip extensors such as the GM and the erector spinae
must counteract greater pitching forces that tend to flex the trunk
anteriorly. In addition, the trunk may also be subjected to higher forces at
HS in the coronal plane that tend to flex the trunk medially relative to the
stance-side hip, and which are counteracted by the stance-side abductors of
the hip (Stern, 1972;
Stern et al., 1980).

A second potentially relevant biomechanical difference between running and
walking is hip flexion during stance. During running, the hip tends to be more
flexed than during walking, not only at HS but also during much of the stance
phase, as the center of mass falls between HS and midstance (MS) and then
rises between MS and toe-off (TO). Flexion of the hips, knees and ankles
between HS and MS during running functions to store up elastic energy in the
tendons of the legs; this energy is then released as kinetic energy through
recoil during the second half of stance, helping to propel the body back into
the air (Alexander, 1991). The
higher impact forces experienced while running, combined with hip flexion
during early stance phase, lead to a tendency of both the thigh and the trunk
to collapse into flexion after heel strike. As already observed
(Stern, 1972;
Marzke et al., 1988), the
human GM is uniquely suited to prevent both types of collapse in humans,
whereas in apes, GMIF contractions only extend the thigh at the hip or prevent
it from flexing.

A final difference between running and walking that is relevant to GM
function is leg swing. During running, the swing leg is accelerated and then
decelerated at much higher velocities than during walking. The GM in humans
may thus act to slow the swing leg at the end of swing phase.

Hypotheses to be tested

This study uses EMG recordings of muscle contractions in conjunction with
kinematic data on limb and trunk movements in human subjects while walking and
running on a treadmill to characterize both the timing and magnitude of GM
activity. Based on the above model, five specific hypotheses about GM function
are tested:

Hypothesis 1. If the primary functional role of the GM is for running
rather than walking, then overall normalized activity of the GM is predicted
to be greater during running than during walking, including uphill
walking.

Hypothesis 2. If contractions of the stance-side GM during running and
walking function to control anterior flexion of the trunk, then normalized
levels of GM activity should correlate positively with forward trunk pitch; in
addition, timing of GM activity should correspond with differences in the
timing of peak trunk flexion in walking (after MS) and running (at HS).

Hypothesis 3. If contractions of the stance-side GM during running function
as hip stabilizers to control flexion of the thigh during bent-hip postures,
then normalized levels of GM activity should be higher during
bent-knee-bent-hip than normal gaits.

Hypothesis 4. If contractions of the stance-side GM during running are
predicted to function as propulsive muscles to help extend the thigh along
with the hamstrings during stance phase, then the timing and normalized levels
of GM and hamstring activity should correlate strongly with each other.

Hypothesis 5. If contractions of the GM on the swing-side function to
decelerate the swing-side leg prior to HS, then normalized levels of GM
activity on the swing side should correlate positively with speed.

Materials and methods

Subjects

Nine volunteers participated in this study. The sample included five
females and four males, all between the ages of 20 and 28. All subjects were
Harvard University students who regularly do long-distance running, with no
history of problems with their gait, and who participate in athletics on a
regular basis. Mean stature was 172.4±8.9 cm (range: 164-186 cm); mean
body mass was 87.7±5.1 kg (range: 83-95 kg). All subjects were barefoot
during the experiment, and all recordings were made on the same treadmill
(Vision Fitness T9250, Lake Mills, WI, USA). After the sensors and EMG
electrodes (see below) had been attached, calibrated and tested, the subjects
walked and ran at a variety of speeds in order to habituate themselves to the
treadmill and the experimental conditions prior to recording. Once the
subjects were comfortable and warmed-up, they were then recorded at three
sequential walking speeds (1.0 m s-1, 1.5 m s-1 and 2.0
m s-1) followed by three sequential running speeds (2.0 m
s-1, 3.0 m s-1 and 4.0 m s-1) during normal
walking and running, and then while walking and running with a bent-hip and
bent-knee (`Groucho' gait). The sequence of trials was generally the same for
all subjects, but trials were repeated on a regular basis to test for signal
similarity, and to ensure that the footswitches were operating properly.
Repeatability was assessed by calculating the standard error of the mean for
peak GM voltages and the onset of GM activity relative to foot strike at
various speeds. These were found to be acceptable. For example, at a 3 m
s-1 run for one subject, the standard error of the peak was 8.2% of
the mean peak value, and the standard error of timing was 6.38 ms. Subjects
were allowed to rest between trials. In order to ensure accurate
normalization, no trials were used if EMG amplifications had been altered
during the experiment. A subset of subjects also walked and ran both on level
conditions and at a 12° incline (the maximum for the treadmill), a slope
that has been shown to generate significant differences in the kinematics of
the lower limb (Milliron and Cavanagh,
1990). All subjects signed informed consent forms, and all methods
used were approved by the Harvard University Human Subjects Committee.

Electromyographic and kinematic data collection

Disposable, self-sticking, pre-wired surface EMG electrodes (Kendall, LTP,
Chicopee, MA, USA) were placed over the center of their right and left GM
approximately 5-6 cm below the cranial origin of the muscle (see
Fig. 1). This electrode
position corresponds approximately with the location of the muscle's
innervation zone (IZ) as determined by Rainoldi et al.
(Rainoldi et al., 2004).
Surface EMGs were used in this experiment because there are no nearby muscles
likely to interfere with GM signal, and because they record from a number of
motor units to give a general view of the muscle's activity. Preliminary
studies found that this location gave very consistent results that
corresponded well to EMG signals from electrodes placed in various different
locations of the muscle. Surface EMGs were also secured to the skin at the
approximate midpoints between origin and insertion of the biceps femoris
(hamstrings), and the gluteus medius. Electrodes were plugged into grounded
preamplifiers worn on a waist belt connected via a lightweight
fiber-optic cable to a MA300 EMG amplifier (Motion Analysis Inc., Baton Rouge,
LA, USA). Loose wires were taped to the skin to prevent signal artifacts
associated with wire movement during locomotion. The analog signal was passed
through an A/D board (PowerLab, ADInstruments Inc., Colorado Springs, CO, USA)
and data were captured at 4000 Hz and monitored in real time using Chart
software (ADInstruments, Inc.).

In order to record kinematic data on the different portions of the stance
phase, thin, flexible footswitches (Motion Analysis Inc.) were taped under the
heel and under the head of the first metatarsal of each foot. Because the heel
and toe footswitches have different voltage signals, the footswitches record
for both feet the onset of heel-strike (HS), foot-flat (FF), heel-off (HO),
and toe-off (TO). A rate gyro (Watson Industries, Inc., Eau Claire, WI, USA)
which outputs 0.31 V deg.-1 s-1 was firmly taped to the
upper back inbetween the vertebral borders of the scapulae to measure trunk
pitch velocity.

Data analysis

Data from the footswitches were analyzed using custom designed software in
Matlab (written by D.A.R.) to determine the timing of HS, FF, HO and TO. EMG
data were also processed using custom-designed Matlab software (by D.A.R.)
that performed the following functions. First, all raw data were filtered
using a 4th order zero-lag Butterworth bandpass filter with frequency cut-offs
at 60 and 300 Hz. After filtering, the onset of each muscle burst was
determined using Thexton's randomization method
(Thexton, 1996). First, the
signal was rectified and then binned using a 10 ms reset integral (see
Winter, 1990). A threshold was
set at 1% of the maximum amplitude of the integrated signal, and the number of
times the signal rose above this threshold (`runs') was calculated. The
threshold was raised by 0.5% of the maximum amplitude and the number of runs
above the threshold was recorded. This calculation was repeated until the
threshold was equal to 100% of the maximum amplitude. Next, the signal was
randomized and the threshold method was repeated on the new randomized signal.
The threshold for the lowest value of the muscle signal was then calculated by
subtracting the number of runs in the randomized signal from the number of
runs in the original signal to find the maximum difference. All values below
this threshold (e.g. values lower than random muscle activity) were eliminated
from the original signal. The maximum value and time of onset for each muscle
burst was determined from this processed signal. All maximum amplitudes were
normalized to the maximum mean muscle burst recorded for each subject during
the session.

Maximum anteroposterior rate of trunk pitching was determined as the
maximum amplitude following heel-strike. For all EMG magnitudes and timing
values, as well as kinematic variables, means were calculated from a minimum
of five strides from each subject at a given velocity and experimental
condition.

Statistical analyses

Means for each subject at each velocity and experimental condition were
calculated using Excel. Since the standard errors of the pooled means for
normalized GM levels differed significantly (P<0.05) between
speeds and conditions (as determined by ANOVA), repeated-measures ANOVA (with
a Tukey-Kramer post-hoc test to account for multiple comparisons) was
used to assess the effects of individual differences on variance. By using the
mean value of each individual for each trial, this method partitions variance
attributed to differences between individuals within a given trial condition
from variance attributed to difference between trials
(Sokal and Rohlf, 1995).
Additionally, means and standard errors for each individual were compared
within each experimental condition to test for the effects of velocity on the
variable of interest.

Results

As predicted by Hypothesis 1, the most salient characteristic of GM
activity during locomotion is that the basic pattern and magnitude of GM
contractions differ substantially between walking and running, as shown in
Fig. 2 and
Table 1. During a walk
(Fig. 2A), the GM tends to
contract at low levels following HS and throughout the ipsilateral stance
phase with no obvious peak. During a run
(Fig. 2B), the GM tends to
contract biphasically with a first burst just prior to HS on the ipsilateral
side, and a second, shorter burst prior to mid-swing about the time of HS on
the contralateral side. In addition, normalized EMG magnitudes in the GM
become higher with increasing velocity (at very high speeds the magnitude and
duration of activity increases for both bursts blurring the distinction
between these bursts in some individuals). During level walking
(Fig. 3A), peak GM magnitudes
around the time of ipsilateral HS are quite low, less than 10% of maximum
amplitudes, but increase by about 2.5-fold between 1.0 and 2.0 m
s-1. Peak GM magnitudes at ipsilateral HS during running are
approximately 50% higher (P<0.05) than for a walk at 2.0 m
s-1 (a slow run, below the preferred walk-run transition for all
subjects), and increase by approximately twofold between 2.0 and 4.0 m
s-1. As shown in Fig.
3B, peak magnitudes of GM activity during the swing phase also
increase as a function of speed, and are significantly (P<0.05)
higher in running than walking at the same speed (2.0 m s-1). In
addition, walking on an incline increased peak stance-side EMG magnitudes only
slightly, well below levels for running; moreover, in contrast to level
running, EMG magnitudes during uphill running do not significantly increase
with speed (Fig. 3A).

Comparison of kinematics and muscle activity in walking and running at
2.0 m s−1

Hypothesis 2 - that normalized levels of GM activity correlate positively
with forward trunk pitch, and that timing of GM activity correlates with
differences in the timing of peak trunk flexion in walking (after midstance)
and running (at heelstrike) - is also supported. Trunk pitching rate is much
lower in walking than running, even at the same speeds. Maximum pitch rates
during walking ranged from approximately -25 to -75 deg. s-1, but
were between -150 and -250 deg. s-1 during running
(Fig. 4A). As hypothesized,
trunk pitch correlates well (r2=0.96) with normalized EMG
magnitudes in both gaits (Fig.
4B). These results corroborate findings from earlier studies that
the GM plays an active role in stabilizing the trunk against sagittal pitching
(Marzke et al., 1988).

As noted above, Hypothesis 2 also predicts differences in the timing of the
onset of GM contractions in running compared to walking. As illustrated in
Fig. 2 and quantified in
Fig. 5, the onset of GM always
occurs after HS in a walk but always prior to HS in a run,
with significantly earlier onset relative to HS as a percentage of stride
duration with increasing speed during running. Note also that for both gaits
(as predicted), the timing of maximum muscle activation occurs after the time
of maximum trunk pitch rate (Fig.
5B).

Hypothesis 4 - that the GM also functions as a thigh extensor at the hip to
help perform work - predicts that the timing and normalized levels of GM and
the other major thigh extensor group, the hamstrings, should correlate well
with each other. The magnitudes of maximum stance-side muscle activity for
both GM and one of the hamstrings (the biceps femoris) were quite similar
(F=0.593, P=0.705) as they both increased with velocity
(Fig. 6A). Additionally, the
time of onset for these two muscle groups
(Fig. 6B) did not differ
significantly (F=0.201, P=0.961).

Finally, subjects were asked to walk and run using a bent-hip bent-knee
(`Groucho') gait in order to test the hypothesis that the GM may help to
prevent the hip from collapsing into flexion during stance phase (Hypothesis
3). As Fig. 7A indicates, GM
activity during `Groucho' gaits was not significantly different from normal
trials in walking, but was significantly lower compared to normal trials
during running (F=5.549, P<0.05). Although these results
suggest that the GM does not play an important role in resisting hip flexion
(see below), maximum trunk pitch velocities also decreased significantly
(F=2.952, P<0.05) during `Groucho' running trials
compared to control trials (Fig.
7B). As previously demonstrated
(McMahon et al., 1987), ground
reaction forces decrease significantly and subjects adopt a more vertical
trunk posture during `Groucho' running. Normalized EMG magnitudes during
`Groucho' running correlate very tightly (r2=0.93) with
the predicted relationship (Hypothesis 2) between EMG activity and maximum
trunk pitch velocities noted above for normal and uphill walking and running
(Fig. 7C).

Discussion

This is the first study to test quantitatively differences in GM function
during walking versus running. The results reported in this study
support some but not all of the five hypotheses outlined above. First, and
most clearly, the GM is considerably more active during running than either
normal walking or incline walking (Hypothesis 1). In particular, EMGs both are
higher by several-fold and begin earlier relative to HS in walking
versus running, supporting the findings of the only previous study
that specifically compared GM activity for both gaits
(Stern et al., 1980), as well
as studies that solely examined walking (e.g.
Joseph and Williams, 1957;
Sutherland et al., 1960;
Karlsson and Johnsson, 1965;
Marzke et al., 1988). These
results reported in the present study, however, do not indicate that GM has no
functional role during walking. GM activity during walking in this study
increased with speed, and as noted elsewhere by modeling analyses
(Anderson and Pandy, 2003;
Jonkers et al., 2003a), low
levels of GM activity may contribute to hip extension during stance, and to
restraint of hip flexion during swing. While there is no simple relationship
between normalized EMG magnitudes and muscle force production, the relatively
lower levels of activity recorded here and in other studies do not support the
hypothesis that enlargement of the GM in humans is primarily related to
bipedal walking on flat surfaces (e.g. treadmills). Since larger muscles
typically have greater force generation capabilities, other functional roles
are needed to account for the relative expansion in humans compared to
non-human primates in the absence of any apparent need to generate large
forces during bipedal posture and walking.

One caveat, however, that requires more study is that GM activity may be
important in walking up very steep inclines or very uneven terrain. The
maximum incline in this study was only 12%, which is not particularly steep
but nonetheless sufficient to induce noticeable changes in hindlimb kinematics
(Milliron and Cavanagh, 1990),
and which may require increased control of trunk flexion. Future experiments
are needed to assess role of GM in such walking conditions, but there is some
reason to suspect that they will be minor. Tokuhiro et al. found that GM
activity is only subtly affected by uphill walking
(Tokuhiro et al., 1985), and
Swanson and Caldwell found that while the onset of GM contractions were
relatively earlier in stance during running at a 30% incline (at 4.5 m
s-1), activity levels were not significantly higher
(Swanson and Caldwell, 2000).
In addition, the major added challenge of walking on uneven terrain is control
of hip abduction, which is mostly accomplished by the gluteus medius and
gluteus minimus (Soderberg and Dostal,
1978).

Although GM activity is demonstrably important in a wide variety of tasks
including climbing and bending (see Marzke
et al., 1988; Zimmerman et al., 1994), the above results support
several specific hypotheses about the role of the GM during running
(Stern et al., 1980;
McLay et al., 1990;
Bramble and Lieberman, 2004).
Just as it was shown (Marzke et al.,
1988) that the GM plays an important role in controlling flexion
of the trunk during upright bipedal posture, the above results support
Hypothesis 2 (above) that a major role of the GM is to extend the hip on the
stance side to help control flexion of the trunk during running. Several lines
of evidence support this hypothesis. First, as speed increases, so does trunk
pitch rate and relative activation of the GM, leading to a nearly perfect
correlation between maximum peak EMG magnitudes on the stance side and maximum
peak trunk velocities across a range of speeds in both gaits. Importantly,
this relationship is also true during `Groucho' running when peak EMG activity
was much lower relative to speed than during normal running
(Fig. 7B), but at the level
predicted for trunk pitch rate (Fig.
7C). The timing of GM activation also makes sense in terms of
controlling trunk pitch rate. Peak flexion of the trunk in a walk occurs after
MS as the body's center of gravity is beginning to fall, but in a run occurs
at the time of HS. As Hypothesis 2 predicts, the stance-side GM contracts
after HS in a walk but before HS in a run, thereby helping the GM extend the
hip as the trunk pitches anteriorly. Additional evidence for the GM's role in
controlling trunk flexion is provided by the results of the `Groucho' gait
trials. Although the timing of GM contractions during running could indicate
that the stance-side GM functions as an antigravity muscle to resist flexion
of the thigh relative to the trunk at HS, normalized peak magnitudes of the GM
at HS were lower during `Groucho' gaits than normal trials. This decrease in
activity during `Groucho' trials suggests that stabilizing the thigh to
counteract flexion is not a major function of the GM. Instead, decreases in
normalized peak EMG magnitudes during `Groucho' trials relative to normal
trials are predicted by the strong correlation between maximum trunk pitch
rate and GM activation for normal walking and running
(Fig. 7C). This result provides
strong support for the hypothesis that GM functions largely as a trunk
stabilizer during running.

Although the above results do not support the hypothesis that the GM
functions as a postural muscle to control flexion of the thigh during stance
when the hip is flexed (Hypothesis 3), they do suggest that the GM has
additional functions. One of these functions may be to help actively extend
the thigh during stance (Hypothesis 4). In particular, the timing and
magnitude of stance-side GM contractions were very similar to those of the
hamstrings during both walking and running, confirming the results of several
previous studies (Mann and Hagy,
1980b; Montgomery et al., 1984;
Nilsson et al., 1985;
Jonhagen et al., 1996). Such
results are particularly interesting in terms of uphill locomotion. Roberts
and Belliveau calculated that hip extensors such as the hamstrings and the GM
may not produce much work output during horizontal running, but have
increasingly high moments during uphill running
(Roberts and Belliveau, 2005).
It has also been shown (Sloniger et al.,
1997; Belli et al.,
2002) that the hip extensors have low moments and comparatively
lower activity levels compared to the ankle and knee during flat running at
normal speeds, but become increasingly important at very fast sprinting
speeds. Further studies are needed to assess the contributions of the GM to
hip extension during uphill running. As noted above, one explanation for the
observed decrease in GM activation during uphill versus level running
could be a decrease in trunk pitch caused by lower GRFs or possibly other
changes in kinematics (e.g. contact time, or more vertical trunk postures).
However, one other study that examined GM activity during running at an
incline (Swanson and Caldwell,
2000) found earlier timing as well as higher levels of GM activity
during uphill running, but at a much steeper incline (30°) and a faster
speed (4.5 m s-1) than examined in this study.

Finally, the GM is also active on the swing side during the aerial phase of
running, when it can play little or no role either to control flexion of the
trunk or to help extend the leg. As suggested
(McLay et al., 1990), the most
likely function of swing-side contractions of the GM is to decelerate the leg
during swing phase. These results are also consistent with those reported by
previous studies (Mann and Hagy,
1980b; Montgomery et al., 1984;
Nilsson et al., 1985;
Jonhagen et al., 1996). While
this hypothesis is difficult to test, it is consistent with data on both the
timing and magnitude of normalized GM contractions at different speeds. In
particular, the swing-side EMG contracts just prior to the midpoint of swing
phase regardless of speed; in addition, as speed increases, so does the
relative magnitude of the swing-side EMG. One possibility that needs further
study is whether the braking action of the swing-side GM on the thigh also
helps passively extend the knee.

Comparative function and evolution of the GM

The above results indicate that the reorganization and relative enlargement
of the GM in humans does not give the muscle a major role in level bipedal
walking. While we cannot discount the hypothesis that the GM was important for
walking over uneven terrain (see above), the results of this study indicate
that the GM has several critical functions that improve running performance.
These data, combined with other results
(Marzke et al., 1988) on
bipedal postural control, raise several questions about the evolutionary
origins of the unique anatomy of the human GM. To address these questions, it
is useful to begin with a comparison of what is known about GM function in
humans versus non-human primates, especially apes, in relation to
their anatomical differences.

Non-human GM activity during locomotion has been examined using EMG in both
chimpanzees (Tuttle et al.,
1975; Stern and Susman,
1981) and in macaques
(Hirasaki et al., 2000). These
studies indicate that GM activity is generally similar during bipedal walking
and vertical climbing in apes (Stern and
Susman, 1981), both of which differ from activity during
quadrupedal walking. In apes, the GMIF (which is absent in humans) and the
middle and anterior portions of GMP (broadly homologous with the more cranial
fibers of the human GM) are active during stance phase of both bipedalism and
vertical climbing (Tuttle et al.,
1975; Stern and Susman,
1981). Hirasaki et al. also noted GM activity during stance phase
of climbing in Japanese macaques (Hirasaki
et al., 2000). GM activity during swing phase is somewhat more
variable in non-human primates, although the GMIF is active in apes at the end
of swing during bipedal walking but not during vertical climbing
(Stern and Susman, 1981).
These results suggest three major functions of the non-human primate GM.
First, the GMIF primarily acts as a thigh extensor during the stance phase in
both climbing and walking (Stern,
1972; Tuttle et al.,
1975; Stern et al.,
1981). Second, the non-human primate GMP probably functions
primarily as a thigh rotator (Tuttle et
al., 1975; Stern and Susman,
1981), preventing the flexed femur from collapsing into lateral
rotation during bipedal stance phase. Finally, the GMIF also helps decelerate
the limb during swing phase in terrestrial locomotion (it is probably
unnecessary to decelerate the limb during climbing).

As noted (Stern, 1972),
evidence that the human GM and the ape GMIF both act primarily as hip
extensors during the stance phase explains much of the derived configuration
of human GM anatomy in terms of the reorganization of the human pelvis for
bipedalism. In particular, apes use the more caudal fibers of the muscle, the
GMIF, to extend the thigh during climbing and bipedal walking, and humans use
the functionally equivalent cranial portion of the GM for bipedal running, and
to a much lesser extent in walking. In addition, the ape GMIF and the human GM
are both active towards the middle or end of swing phase, suggesting a shared
role in swing-limb deceleration. The major functional contrast between humans
and apes is that the ape GMP is primarily a medial rotator of the hip to
counteract the tendency of the thigh to collapse into lateral rotation, and it
may act additionally as an abductor of the thigh to prevent the tendency of
the stance-side hip to collapse into adduction
(Stern and Susman, 1981).
Since GM activity is quite low during human bipedal walking on level surfaces,
to the point of being absent in some subjects
(Sutherland et al., 1960), it
is reasonable to conclude that the expansion of the cranial portion of the GM
is probably mostly related to its most dominant function in humans, the
control of trunk pitch (Marzke et al.,
1988). In order to test this hypothesis more fully, however,
additional data are needed on the amount of work done by the muscle during hip
extension (which would result in positive work), versus trunk flexion
(which would result in negative work). It would also be useful to assess GM
activity during walking and running on uneven substrates, although preliminary
EMG data (unreported) during walking on uneven ground indicates no measurable
increase in activity.

Another relevant point is that the human GM acts in conjunction with the
erector spinae to control flexion of the trunk at two different joints. The
erector spinae, which attaches to the sacrum and iliac crests, filling the
trough between the left and right iliac tuberosities, extends the sacroiliac
joint. The human GM shares part of the same area of attachment and aponeurosis
as the erector spinae (Standring et al.,
2005), but primarily extends the hip. Both muscles thus act in a
complementary, combined fashion to control flexion of the trunk at the hip and
the sacroiliac joint. Therefore, expansion of the human GM, which is
essentially an expansion of the ape GMP, likely helped permit an important
functional linkage across the two joints between the thigh and the lower back
that is necessary to stabilize trunk pitch in a biped.

Another, related question is when the expansion and reorganization of the
human GM occurred. Unfortunately, it is difficult if not impossible to
reconstruct reliably the relative size and precise configuration of any
muscle, including the GM, from its origin and insertion markings in fossils
(Zumwalt, 2006). Although a
human-like configuration of the pelvis is apparently present by at least 1.9
million years ago in Homo erectus
(Day, 1973;
Rose, 1984;
Ruff, 1995), there is much
disagreement over the organization of gluteal musculature in australopithecine
species such as Australopithecus afarensis and A. africanus.
Some researchers have suggested that muscle attachment markings on pelves of
australopithecines are human-like
(Lovejoy, 1988;
Haeusler, 2002). In fact,
Haeusler suggests that the australopithecine GM not only originated primarily
from the ilium, but that it could have been as large as that of modern humans
(Haeusler, 2002). While
several fragmentary pelves, notably AL 288-1 (A. afarensis) and Sts
14 (A. africanus), have roughened surfaces along the posterior iliac
crests that may indicate an expansion of the GMP onto the iliac crest, the
muscle's region of origin in these specimens appears to be limited to the
medial third of the crest nearest the sacroiliac joint
(Aiello and Dean, 1990). In
several H. erectus innominates, as in modern humans, the attachment
is much more extensive, comprising a widened, rough surface along the superior
iliac crest that extends from the sacroiliac joint to the midpoint of the
crest in some individuals. This expansion suggests a relatively larger cranial
portion of the muscle in the genus Homo. Further evidence, however,
is necessary to test the hypothesis that the australopithecine GMP was as
expanded as in Homo (Toussaint et
al., 2003).

Although the cranial origin of the GM in australopithecines may have been
smaller and more ape-like than the expanded origin in Homo, the
femoral insertion of the GM in Australopithecus appears to be similar
to that of humans and derived from the ape pattern. Most notably, Lovejoy et
al. pointed out that the insertion of the GM on the Maka femur (Mak-VP-1/1),
attributed to A. afarensis, was restricted to the gluteal ridge on
the proximal portion of the lateral femur
(Lovejoy et al., 2002). As
noted (Stern, 1972), this
reorganization makes sense given the various derived adaptations of the pelvis
for bipedalism that permit the GM to function as a hip extensor, and to
accommodate differences in fiber resting lengths brought about by upright
posture. It therefore seems likely that australopithecines lack a GMIF similar
to that of non-human primates. However, the extent to which the GMIF was
reduced or absent is not entirely clear and requires further study.

A final line of evidence comes from biomechanical models of hip muscle
function in fossil hominids. The lines of action of the gluteal muscles on the
pelvis of Lucy (AL 288-1, A. afarensis) were compared
(Berge, 1994) using both more
ape-like and human-like reconstructions. Berge concluded that an ape-like
gluteal pattern, in which the caudal portion of GM is relatively large and the
cranial portion is relatively small, would have provided australopithecines
with the best leverage for powerful extension of the thigh, and would have
allowed for the full range of thigh movements. Had australopithecines a
human-like gluteal configuration, the GM would have had little leverage for
extension of the femur, an important function in both human and ape locomotion
(Berge, 1994;
Berge and Daynes, 2001). In
another modeling study (Nagano et al.,
2005), it was estimated that if australopithecines had modern
human-like gluteal attachments, then the GM would have needed to produce 30%
higher forces than those of modern humans during walking. Although Nagano et
al. primarily modeled the GM as an extensor of the hip
(Nagano et al., 2005), they
attributed its higher force production to its role as a hip abductor needed to
maintain lateral trunk stability on a relatively wide pelvis. In view of the
earlier analyses (Berge, 1994;
Berge and Daynes, 2001), such
estimated increases in GM activity during walking could also be attributed to
the muscle's poor mechanical advantage as an extensor. In addition, none of
the above studies explicitly considered the muscle's role as a trunk pitch
stabilizer.

Considered together, the comparative and fossil evidence for the evolution
of the GM suggests that australopithecines probably had an intermediate
configuration between that of apes and humans. They clearly resembled humans
and differed from apes in lacking expansion of the caudal GMIF portion of the
muscle, but possibly did not have the same degree of cranial expansion evident
in humans. It is therefore reasonable to hypothesize that australopithecines
did not rely as heavily on the GM for trunk stabilization, either because
they, like all other primates including chimpanzees, did not habitually run
for long distances (Bramble and Lieberman,
2004), or because they compensated for the lack of strong cranial
GM fibers with other muscles such as the erector spinae. Expansion of the
cranial portions of the GM, however, would have been useful to
australopithecines if they included a substantial portion of tree-climbing in
their locomotor repertoires.

Future experimental and paleontological research is necessary to clarify
the functional and evolutionary history of the human GM. Based on the above
results, we offer several alternative scenarios that merit further study. As
noted above, one possibility is that australopithecines had an intermediate
configuration of the GM (Berge,
1994; Berge and Daynes,
2001), retaining some kind of caudal portion but with a less
expanded cranial portion than is evident in Homo. If so, then the
caudal portion would likely have been an effective extensor of the femur
during climbing and perhaps walking, and the cranial portion would have helped
to stabilize the sacrum, but probably would not have been a strong trunk
stabilizer. An implication of this scenario is that the expansion of the
cranial portion of the GM is a derived trait of Homo that would have
been selected for control of trunk flexion during endurance running
(Bramble and Lieberman, 2004)
and/or foraging (Marzke et al.,
1988). An alternative possibility, however, is that the
configuration of the GM in Australopithecus was much like that of
Homo in terms of the loss of the GMIF. Either the australopithecine
GM as a whole was relatively smaller, as many researchers suggest, or possibly
as large as in humans (Haeusler,
2002). As shown above, the GM in either case is unlikely to have
played much of a role in level terrain walking, and is unlikely to have been
selected for running given that the genus lacks many other features associated
with running capabilities (Bramble and
Lieberman, 2004). According to this scenario, the derived anatomy
of the GM in Australopithecus was probably a reconfiguration of the
gluteal musculature for climbing, or a novel adaptation for foraging tasks
such as digging that involve flexion of the trunk
(Marzke et al., 1988). We
cannot discount the hypothesis that expansion of the GM might have been useful
for walking on uneven terrain. However, it is clear that expansion of the GM
in Homo would have benefited any activity that requires trunk
stabilization, especially running. Regardless of which scenario is correct,
the expansion of cranial portion of the GM is a uniquely hominid
characteristic, perhaps distinctive to the genus Homo, which played a
vital role in the evolution of human running capabilities.

List of abbreviations

EMG

electromyographic

FF

foot flat

GM

gluteus maximus

GMIF

gluteus maximus ischiofemoralis

GMP

gluteus maximus proprius

GRF

ground reaction force

HO

heel-off

HS

heel strike

IZ

innervation zone

MS

mid-stance

TO

toe-off

ACKNOWLEDGEMENTS

We are grateful to the subjects who participated in the experiment, NSF
(BCS 044033) for funding, two anonymous reviewers for their comments, and to
the many colleagues with whom we have had many enjoyable discussions about the
gluteus maximus and its function.

Jonkers, I., Stewart, C. and Spaepen, A.
(2003b). The complementary role of the plantarflexors, hamstrings
and gluteus maximus in the control of stance limb stability during gait.
Gait Posture17,264
-272.

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