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Electromyography of back muscles during quadrupedal and bipedal walking in primates.

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Electromyography of Back Muscles During Quadrupedal and
Bipedal Walking in Primates
Department of Anthropology, University of Texas at Austin, Austin, Texas
78712 (L.J.S.) and Department of Anatomical Sciences, SUNY at Stony
Brook, Stony Brook, New York 11794 (W.L.J.)
EMG, Quadrupedalism, Bipedalism, Hominoids,
Baboon, Erector spinae, Multifidus
Despite the extensive electromyographic research that has
addressed limb muscle function during primate quadrupedalism, the role of
the back muscles in this locomotor behavior has remained undocumented. We
report here the results of an electromyographic (EMG) analysis of three intrinsic back muscles (multifidus, longissimus, and iliocostalis) in the baboon
(Pupio unubis), chimpanzee (Pun troglodytes), and orangutan (Pongo pygrnueus) during quadrupedal walking. The recruitment patterns of these three
back muscles are compared to those reported for the same muscles during
nonprimate quadrupedalism. In addition, the function of the back muscles
during quadrupedalism and bipedalism in the two hominoids is compared.
Results indicate that the back muscles restrict trunk movements during quadrupedalism by contracting with the touchdown of one or both feet, with more
consistent activity associated with touchdown of the contralateral foot. Moreover, despite reported differences in their gait preferences and forelimb muscle EMG patterns, primates and nonprimate mammals recruit their back
muscles in an essentially similar fashion during quadrupedal walking. These
quadrupedal EMG patterns also resemble those reported for chimpanzees,
gibbons and humans (but not orangutans) walking bipedally. The fundamental similarity in back muscle function across species and locomotor behaviors
is consistent with other data pointing to conservatism in the evolution of the
neural control of tetrapod limb movement, but does not preclude the suggestion (based on forelimb muscle EMG and spinal lesion studies) that some
aspects of primate neural circuitry are unique. 0 1994 Wiley-Liss, Inc.
Much study has been devoted to investigating primate quadrupedalism in comparison to that of nonprimate mammals (e.g.,
Prost, 1965; Hildebrand, 1966, 1967;
Kimura et al., 1979; Rollinson and Martin,
1981; Vangor and Wells, 1983; Reynolds
1985a)b;Vilensky and Larson, 1989; Larson
and Stern, 1987, 1989; Demes et al., 1994;
see Vilensky, 1987, 1989 for reviews). As a
result, numerous aspects of primate quadrupedalism have been proposed to be unique
among mammals, including their preferred
gait pattern (Muybridge, 1899; Prost, 1965;
Hildebrand, 1966, 1967; Rollinson and
Martin, 1981), mechanisms of propulsion
(Kimura et al., 1979), and muscle activity
patterns (Larson and Stern, 1987,1989).
The difference between primates and
nonprimates with respect to footfall patterns in symmetrical gaits is well documented. Primates preferentially (though not
exclusively) use a diagonal-sequence gait
(LhRfRhLf, Lh = left hind limb, Rf = right
forelimb, etc.) rather than the lateral-sequence gait (LhLfRhRf) utilized by nonpri-
Received March 18,1993; accepted October 21,1993
Address reprint requests to Liza Shapiro, Dept. of Anthropology, University of Texas at Austin, Austin, TX 78712-1086.
mate mammals (Muybridge, 1899; Prost,
1965;Hildebrand, 1966,1967;Rollinson and
Martin, 1981). Primates also have been
singled out among mammals for their “frontsteering, rear-driving” rather than “frontsteering, front-driving’’ propulsive mechanism (Kimura et al., 1979). Both of these
presumably unique aspects of primate quadrupedalism traditionally have been explained in terms of morphology. For example, it has been suggested that a diagonalsequence gait is more stable for primates
than is a lateral-sequence gait if the center
of gravity is more posteriorly located in primates than in nonprimate mammals (Rollinson and Martin, 1981). Morphological explanations also hold that the posterior
propulsive mechanism is associated with
the fact that primates support most of their
weight on their hind limbs (Kimura et al.,
1979; see also Reynolds, 1985a,b; Vilensky
1987, 1989; Vilensky and Larson, 1989;
Demes et al., 19941, and thereby “free” the
forelimbs for other behaviors.
More recently, however, doubt has been
cast on the notion that primates are unique
or even consistent in employing a hind-limb
propulsive mechanism. For instance, propulsive forces on primate hind limbs may be
asymmetrical (e.g., on leading vs. trailing
limbs in a gallop; Demes et al., 1992, 1994),
and it has been demonstrated that both primates and nonprimates propel themselves
predominantly with their hind limbs
(Demes et al., 1992, 1994; see also Pandy et
al., 1988; Vilensky, 1989). Moreover, Vilensky (1987, 1989) and Vilensky and Larson
(1989)present convincing evidence that neither a more posteriorly located center of
gravity nor increased hind-limb weight can
adequately explain the primate preference
for diagonal sequence gaits. These authors
point out that the location of the center of
gravity should not affect stability at most
speeds and gaits chosen by primates, and
even so, “the actual difference in CG locations between for example, cats and primates appears to be slight” (Vilensky, 1989:
358). Vilensky and Larson (1989) also note
that although diagonal-sequence gaits are
preferred, lateral-sequence gaits are not uncommon among primates. Accordingly,
these authors offer a neurological rather
than morphological explanation for primates’ overall preference for diagonal-sequence gaits, as discussed below (see also
Larson and Stern, 1989).
Electromyographic analyses have contributed substantially to characterizing the nature of primate quadrupedalism, as well as
permitting detailed comparisons between
primate and nonprimate quadrupedalism
with respect to muscle function. These studies have revealed overall similarity in hindlimb muscle function between primates and
nonprimate mammals (particularly domestic cats) when they walk quadrupedally
(e.g.,Jungers et al., 1983;Vangor and Wells,
1983), notwithstanding some exceptions
(e.g., Jungers et al., 1980; Jungers and
Anapol, 1985; Vilensky, 1987). The continuity of hind-limb muscle activity patterns
across mammalian groups (and between
mammals and other tetrapods) is suggestive
of an evolutionary conservatism in locomotor neural circuitry (Peters and Goslow,
However, EMG studies also have revealed
dissimilarity between quadrupedal primates and nonprimates with respect to the
recruitment patterns of forelimb muscles
(e.g., Larson and Stern, 1987, 1989). It has
been suggested that both the unique forelimb EMG patterns exhibited by primates
and their preference for diagonal-sequence
gaits are not simply due to biomechanical
factors, but are likely to be the result of
changes in primate neural control mechanisms. That is, neural control of quadrupedalism may depend more on supraspinal
input in primates than in nonprimate mammals (Eidelberg et al., 1981).This evolutionary change in primate neural control is
thought to be associated with the superior
manipulative abilities of primate forelimbs
and their tendency to be released from locomotor function (Vilensky, 1987, 1989; Vilensky and Larson, 1989; Larson and Stern,
Although primates do not appear to be
unique in hind-limb muscle function during
quadrupedalism, the contrasting results for
forelimb muscles suggest that further investigation of muscle function during primate
quadrupedalism in a comparative context is
warranted. A thorough comparison of mus-
cle function during primate vs. nonprimate
quadrupedalism should include a consideration of all muscle groups important to locomotion, i.e., axial as well as appendicular
muscles. Research on back function in the
cat has demonstrated that during quadrupedal walking, multifidus, longissimus, and iliocostalis contract bilaterally with touchdown of each foot; i.e., there are two “bursts”
of muscle activity during each step cycle
(Carlson et al., 1979; English, 1980; Zomlefer et al., 1984).Tokuriki’s (1973a)data on
longissimus in a dog (at the level of the
fourth lumbar vertebra) also indicate that
this muscle contracts in association with
touchdown of each foot during walking. Taylor (1978),referring to unpublished observations, noted that the lumbar iliocostalis of
dogs is inactive during walking. Back-muscle function during primate quadrupedalism
remains undocumented. The purpose of the
study reported here is to examine the recruitment patterns of multifidus, longissimus, and iliocostalis in primates walking
quadrupedally and to compare the results to
those reported for nonprimate mammals.
In a previous study, we collected EMG
data on the same back muscles for a chimpanzee and two gibbons walking bipedally,
and compared the results to human backmuscle activity during bipedalism (Shapiro
and Jungers, 1988). Results indicated a basic similarity in back-muscle recruitment
patterns between the nonhuman hominoids
and humans, reminiscent of the “conservative” nature of hind-limb muscle function
characterizing primates and nonprimates
walking quadrupedally. This “conservation”
of back-muscle function across species
raises the question of whether or not backmuscle function is also maintained across
locomotor behaviors. Therefore, in the current study, the recruitment patterns of
selected axial muscles in primates (chimpanzee, orangutan, and baboon) walking
quadrupedally are not only compared to
those characterizing nonprimate quadrupedalism, but are also compared to our previous data on bipedalism. In addition, new
data on back-muscle function in bipedalism
are presented here for the orangutan.
The aims of the study can be summarized
as follows:
1. To describe and compare the recruitment patterns of several back muscles during quadrupedalism in three primate species. This aspect of the study allows us to
test whether or not the function of primate
back muscles during quadrupedalism is consistent across species, as was reported for
bipedalism (Shapiro and Jungers, 1988).
This represents the first attempt known to
use to investigate primate back-muscle
function in quadrupedalism.
2. To test whether or not there are any
differences in back-muscle function between
primates and nonprimate mammals walking quadrupedally, given their reported differences in forelimb muscle activity as well
as their differences in footfall sequence preferences. Nonprimate back-muscle EMG
data were taken from the literature.
3. To compare back-muscle function in
primates during quadrupedalism to backmuscle function during bipedalism in nonhuman hominoids and humans. Are the
muscle activity patterns utilized in quadrupedalism called upon in bipedalism, or does
the role of the back muscles change as the
trunk is subjected to new biomechanical demands?
The experiments were performed in a
large enclosure (7.3 m x 3.7 m x 2.7 m). Details of the experimental environment can
be found elsewhere (Stern et al., 1980;
Jungers et al., 1983). Each subject was encouraged to walk quadrupedally andlor bipedally for food rewards. During quadrupedalism, all subjects walked with a diagonalsequence gait. The subjects included one
male chimpanzee (Pan troglodytes), two
orangutans (Pongo pygmaeus), and one
male baboon (Papio anubis). We also collected quadrupedal and bipedal data for a
second chimpanzee. The results for the two
individuals were consistent, but data from
only one individual are presented here. This
chimpanzee is the same individual whose
bipedalism was investigated in Shapiro and
Jungers (1988). For one of the orangutans
(“Solok), most of the quadrupedal step cycles were irregular, leaving only one or two
digitizable step cycles. Even after training,
the other orangutan (“Tombak) was rarely
able to walk bipedally without hand support
from the trainer. Therefore, the quadrupedal data presented here are from one of the
orangutans (Tombak), and the bipedal data
are from the other (Solok).
cle revealed no tail contraction, verifying
that the electrode was not placed in the extensor caudae lateralis.
In the hominoids, the electrode was placed
in longissimus at the lower thoracic level,
about 4-5 cm lateral to the spinous proExperimental technique
cesses. In the baboon, the electrode was
The technique employed was telemetered
placed about 1cm lateral to the spinous proelectromyography with simultaneous video
cesses at the level of the last rib. In all subrecording as described in Stern et al. (1977,
jects, electrode placement was verified by
1980). Each animal was placed under
stimulation, revealing the contraction of the
halothanelnitrous oxide anesthesia, after
craniocaudally oriented fibers characterizwhich fine-wire bipolar electrodes were ining longissimus.
serted into multifidus, longissimus, and iliocostalis. Dissections of cadavers of compara- Iliocos tal is
ble size to each of the experimental subjects
In the hominoids, the electrode was placed
were performed in order to determine relevant musculoskeletal landmarks and the lo- in iliocostalis at a point along a vertical line
cation at which each muscle is most accessi- passing through the midpoint of the iliac
ble for electrode insertion (see Figs. 1and 2 crest, at the level of the last two ribs. In the
baboon, the electrode was placed about 3.5
in Shapiro and Jungers, 1988).
cm lateral to the spinous processes at a level
approximately midway between the ribs and
iliac crest. Again, electrode placement
In the hominoids, the electrode was inserted just medial t o the most posteromedial was verified for all subjects by stimulation,
aspect of the iliac crest (i.e., the “posterior revealing the contraction of the craniolatersuperior iliac spine”).Multifidus is the most ally oriented fibers characterizing iliocostawell developed here, and although it is a lis.
relatively deep muscle, at this level only
Data analysis
skin, fascia and erector spinae aponeurosis
lie superficially. For this reason, confidence
Details of the method used here can be
in the accuracy of electrode placement was found in Stern et al. (19801, Jungers et al.
high. Electrode placement was verified by (19831, and Larson and Stern (1986); only a
sending a small stimulating current back brief summary follows. In order to quantify
through the electrode, revealing the contrac- the results, the videotape recording of each
tion of the craniomedially oriented fibers animal with the EMG signals superimposed
characterizing multifidus.
was played back frame by frame. The exact
The existence of the tail in the baboon timing of behavioral events with respect to
made electrode placement a bit more diffi- the EMG signals was noted and transposed
cult. Just medial to the iliac crest and lateral onto a hard copy of the video image. This
to multifidus lies the lumbar portion of the was possible because at the end of each twoextensor caudae lateralis (i.e., the “lumbo- second sweep of the oscilloscope beams, the
coccygeus”; see Bogduk, 1973, 1980), which image of the animal is deleted, leaving only
is relatively large in the baboon. Therefore, an image of the EMG signals.
placement of the electrode just medial to the
Behavioral “events” refer to the onset or
iliac crest would most likely be located in cessation of step cycles. Although the hands
this tail extensor, rather than in multifidus. as well as the feet contact the substrate durTo avoid this problem, in the baboon the ing quadrupedal walking, the feet were choelectrode was placed deeply at a level just sen as the point of reference for consistency
above the iliac crest, and just lateral to the with both the bipedal data and with the litspinous processes. Stimulation of the mus- erature on nonprimate back muscle function
during quadrupedalism (e.g., Tokuriki,
1973a; CarIson et al., 1979; English, 1980;
Zomlefer et al., 1984). That is, “touchdown77
of the foot (TD) marks the beginning of support phase, and “toe-off of the foot (TO)
marks the beginning of swing phase. We
also identified the midphases (M) of support
and swing (the points at which the hip and
ankle are aligned vertically). Since touchdown of the opposite or contralateral foot
was important in the interpretation of back
muscle function in bipedalism, we also included this reference point ( C ) in the analysis of quadrupedalism (e.g., Fig. 1).
In order to quantify the data, the duration
and relative amplitude of the raw EMG signals were digitized in conjunction with the
behavioral events, and transformed into a
matrix representation. The matrix indicates
the percent frequency of muscle activity at a
given amplitude and at a given point in the
locomotor cycle (Stern et al., 1980; Jungers
et al., 1983; Larson and Stern, 1986). The
relative intensity of EMG activity was estimated by comparing signal amplitude to a
designated maximum burst for each muscle
during each experiment. For all results except iliocostalis in Papio, activity referred to
as “consistent” occurred at least 67% of the
time; activity occurring between 33% and
67% of the time was considered to be frequent but less predictable (e.g., Fig. 1).
The EMG data presented for the baboon’s
multifidus and longissimus were collected
in a single experiment, during which the signal for iliocostalis was lost. A second experiment on the same three muscles in the same
individual was only successful in providing
data for multifidus and iliocostalis. In this
second experiment, the frequency of muscle
activity was lower overall than in the first
baboon experiment and when compared to
the other primate subjects. Despite the differences in frequency, the muscle activity
patterns of multifidus were similar in the
two experiments, and results are presented
here from the first experiment. For Papio’s
iliocostalis, however, activity from the second experiment is depicted which occurred
between 30% and 40% of the time and between 5% and 30% of the time.
Although walking speed was not measured directly, the baboon clearly exhibited
Multifidus: Quadrupedalism
Fig. 1. Quantified muscle activity patterns of multifidus (right side) during quadrupedal walking in Papio,
Pan, and Pongo. TD = touchdown of the ipsilateral
(right) foot, marking the beginning of support phase.
M = midphase of support or swing, when the hip and
ankle form a line perpendicular to the substrate.
C = touchdown of the contralateral (left)foot. TO = toeoff of the ipsilateral (right) foot, marking the beginning
of swing phase. Blackened areas indicate consistent activity; that is, activity occurring at least 67% of the time.
Striped areas indicate frequent, but less predictable activity; that is, activity occurring between 33%and 67%
of the time. The numbers in each box represent the number of step cycles analyzed for each support or swing
phase. Amplitude is scaled to the maximum activity observed in each muscle.
a variety of speeds. Nevertheless, the baboon's slow and moderately paced step cycles were combined after separate examination of results revealed similar patterns of
muscle activity at each speed (this pertains
to the results for multifidus and longissimus
only; speed differences were less noticable in
the separate experiment from which the ilio- Papio
costalis data were generated).
tongissimus: Quadrupedalism
Primate quadrupedalism
Multifidus activity in all three primates
generally resembles that reported for the
cat: there are two bursts of multifidus activity during the step cycle, one associated with
touchdown of the ipsilateral foot (TD), and
the other associated with touchdown of the Pan
contralateral foot (C; Fig. 1). The latter
burst is clearly centered around contralateral touchdown and is more consistent in
pattern among the three primates, while the
ipsilateral burst is somewhat more variable
in pattern among the three.
In all three primates, longissimus (like
multifidus) is consistently active as the contralateral foot touches down (Fig. a), a pat- Pongo
tern resembling that reported for cats and
dogs, However, the ipsilateral burst displayed by the nonprimates is more variable
in pattern among the primates. For examTD
ple, in the chimpanzee, longissimus shows
Fig. 2. Quantified muscle activity patterns of longissivariable activity throughout swing phase,
with a slight increase in amplitude just be- mus (right side) during quadrupedal walking in Papio,
Pun, and Pongo. See Figure 1for abbreviations and confore ipsilateral touchdown, and brief but ventions.
consistent activity at touchdown. There is
some activity surrounding ipsilateral touchdown in the orangutan, but it is not consistent. Overall, the results for the baboon tivity is associated with ipsilateral and espemore closely resemble those reported for cially contralateral touchdown (Fig. 3). This
nonprimates in that there are two consis- pattern resembles that of the other two mustent bursts of activity, one at contralateral cles (Figs. 1,2) and also resembles results
touchdown and the other just after ipsilat- reported for cats. If anything, it is likely that
eral touchdown.
we have underestimated the frequency of iliocostalis activity at touchdown in the baIliocostalis
Iliocostalis is recruited differently in the
Despite the lower frequency and relative
inconsistency of iliocostalis activity recorded chimpanzee (Fig. 3) than are multifidus and
for Papio, when iliocostalis is active, its ac- longissimus (Figs. 1,2). Unlike the latter two
Iliocostalis: Quadrupedalism
wing Phase
rppoti Phase
the only consistent activity is a burst centered around touchdown of the contralateral
foot, and there is variable activity just before
and at ipsilateral touchdown. Its “double
burst” pattern is also quite similar to the
activity exhibited by multifidus (Fig. 1).
Primate us. nonprimate quadrupedalism
As the results reported above make clear,
there is a general (but not identical) resemblance between primates and nonprimates
in terms of back-muscle recruitment patterns during quadrupedalism. The baboon’s
back-muscle activity more closely resembles
that of cats and dogs than does that of
the two hominoids. Importantly, the chimpanzee’s deviations from the nonprimate
quadrupedal pattern (e.g., variable activity
of longissimus throughout swing phase, Fig.
2; absence of ipsilateral activity of iliocostalis, Fig. 3) are the same patterns that
produce the resemblances between this
hominoid’s quadrupedal and bipedal EMG
patterns (see below).
Quadrupedulism us. bipedalism
Fig. 3. Quantified muscle activity patterns of iliocostalis (right side) during quadrupedal walking in Papio,
Pun, and Pongo. For Pupio only, blackened areas indicate activity occurring between 30%and 40% of the time
and striped areas indicate activity occurring between
5%and 30%of the time (see text for explanation). Otherwise, abbreviations and conventions are as in Figure 1.
muscles, iliocostalis exhibits no ipsilateral
touchdown activity at all. However, like
multifidus and longissimus, iliocostalis contracts consistently a t contralateral touchdown, followed by variable swing phase activity. The recruitment pattern for the
orangutan’s iliocostalis (Fig. 3) is essentially
identical to that for its longissimus (Fig. 2):
Figure 4 reveals that the chimpanzee uses
the three muscles quite similarly during
both quadrupedalism and bipedalism, despite the different mechanical demands
placed on the back in these two locomotor
behaviors. During both behaviors, multifidus and longissimus respond to touchdown
of each foot (with an emphasis on the contralateral burst), and iliocostalis responds
almost solely to contralateral touchdown in
both behaviors. In other words, control of
the trunk in bipedalism is accomplished
with the same basic patterns that are utilized during quadrupedalism. In fact, the
recruitment of longissimus and especially
iliocostalis when a chimpanzee walks quadrupedally is more similar to that of a chimpanzee walking bipedally than it is to that of
a cat walking quadrupedally.
In the orangutan, iliocostalis exhibits the
same recruitment pattern during bipedalism that it does in the chimpanzee, gibbon,
and human (Shapiro and Jungers, 1988);its
activity is associated with touchdown of the
contralateral foot and restriction of excessive movement of the trunk in that direction
Fig. 4. Comparison of EMG activity during quadrupedal and bipedal walking in the chimpanzee for all
three back muscles. Mult. = Multifidus; Long. = Longissimus; Ilio. = Iliocostalis. See Figure 1 for other
abbreviations and conventions.
(Fig. 5). However, whereas multifidus and
longissimus contract bilaterally with touchdown of each foot in the chimpanzee, gibbon,
and human, these two muscles in the orangutan respond to contralateral touchdown
only (resembling the pattern for iliocostalis).
The three primates included in this study
exhibit an overall similarity to each other in
the recruitment patterns of each of the three
muscles during quadrupedalism. In addition to the consistency among the primate
species, the results for the primates reveal a
basic similarity to those reported for nonprimate mammals. That is, in both primates
and nonprimates, each of these muscles
(with the exception of iliocostalis in the
chimpanzee) contracts bilaterally with or
just before touchdown of each foot.
Zomlefer et al. (1984) reported that when
“high decerebrate” cats (whose back muscle
activity closely resembles that reported for
“intact” cats) walk, back muscle contractions associated with the contralateral foot
are of longer duration and higher amplitude
Fig. 5. Comparison of EMG activity during quadrupedal and bipedal walking in the orangutan for all
three back muscles. See Figures 1 and 4 for abbreviations and conventions.
than those associated with ipsilateral touchdown. The authors concluded that the primary role of the back muscles during walking is unlikely to be one of increasing step
length through lateral flexion of the trunk
(as suggested for dogs by Tokuriki, 1973a).
Rather, during quadrupedal walking, the
back muscles act not to initiate movements,
but to “compensate for andor minimize the
movements of the trunk at each step” (Zomlefer et al., 1984:259; see also Carlson et al.,
1979).This, in turn, stabilizes the pelvis and
provides a rigid origin for muscles acting on
the hind limb (English, 1980; see also Carrier, 1987). Zomlefer et al.’s (1984) con-
clusion is consistent with other evidence
demonstrating that during quadrupedal
walking in cats, the range of angular movements of the lumbar spine in the sagittal
and frontal planes is small (Goslow et al.,
1973; Carlson et al., 1979; English, 1980).
Despite the overall similarity between
primate and nonprimate back-muscle EMG
during quadrupedalism, a t least two differences are notable. First, the chimpanzee
does not recruit iliocostalis at ipsilateral
touchdown. This difference becomes important when quadrupedalism is compared to
bipedalism (see below). Second, when there
is both an ipsilateral and contralateral burst
of muscle activity during primate quadrupedalism, the bursts differ little in amplitude
or duration (in contrast to the cat data).
Nevertheless, the back-muscle activity of
both primates and cats exhibits an emphasis
on the response to contralateral touchdown.
In cats, this emphasis is expressed by higher
amplitude and longer duration (Zomlefer et
al., 1984). Among the primates, it is expressed by the fact that more consistent activity occurs at contralateral than at ipsilateral touchdown, especially in the hominoids.
In other words, although the primatenonprimate EMG is not identical in pattern,
the results are similar enough to suggest
that like cats and dogs, it is likely that backmuscle activity during quadrupedal walking
in primates is associated primarily with the
restriction of movements of the trunk. Similarity in recruitment patterns between primates (Ateles, Lagothrix, and Erythrocebus)
and nonprimates during quadrupedal walking has also been reported with respect to
hind-limb muscle function (Vangor and
Wells, 1983). Thus, despite certain functional specializations that have been associated with primate quadrupedalism (e.g., distribution of weight between forelimbs and
hind limbs, footfall pattern; EMG of forelimb muscles), neither hind limb nor backmuscle function during quadrupedalism appears to clearly or consistently distinguish
primates from other mammals (at least
those few mammals for which we have
The reason why the chimpanzee recruits
iliocostalis solely at contralateral touchdown in quadrupedalism remains to be explained. While speed was not recorded in
this study, this type of muscle recruitment
pattern does not appear to be clearly related
to walking speed. In nonprimate mammals
in which speed has been measured, back
muscles are inactive at very slow walking
speeds. Otherwise, burst duration is inversely correlated with speed during walking, but the biphasic pattern of back-muscle
activity remains intact even at a trot. It is
only higher speeds accompanied by a change
in gait to a gallop that produce a markedly
different muscle activity pattern from the
walkhot pattern (Tokuriki, 1973a,b, 1974;
Taylor, 1978; Carlson et al., 1979; English,
1980; Zomlefer et al., 1984). Therefore, it is
unlikely that the chimpanzee’s absence of
iliocostalis activity at one foot touchdown
but not the other is attributable to its walking speed. Alternatively, the chimpanzee’s
distinctive pattern may be related to the fact
that in hominoids, the iliac blade is mediolaterally expanded, and accordingly, iliocostalis (which originates on the iliac crest) is
situated more laterally than in monkeys or
in cats (Reynolds, 1931). Its EMG pattern in
chimpanzees could then be viewed as a reflection of its efficient leverage for lateral
flexion, which is emphasized when counteracting movements of the trunk brought
about by contralateral touchdown (in quadrupedalism as well as bipedalism). This hypothesis is supported by the orangutan’s iliocostalis activity in quadrupedalism. In the
orangutan (whose iliocostalis is also laterally situated), ipsilateral activity is present
but not a t all consistent, while there is a
consistent burst centered around contralateral touchdown. Finally, the difference between chimpanzees (and to some extent
orangutans) on the one hand, and cats and
baboons on the other, might be related to
overall body shape differences (e.g., thoracic
widtwdepth proportions) or t o currently undocumented kinematic differences in walking pattern between these two groups.
The primate results become even more illuminating when quadrupedalism is compared to bipedalism. Unlike quadrupedalism, bipedalism requires balance of the
trunk in the sagittal and frontal planes
(Thorstensson et al., 1982,1984).During bipedalism in chimpanzees, gibbons and humans, the more medially placed multifidus
and longissimus contract bilaterally with
each step, controlling movement in the sagittal plane. The more laterally placed iliocostalis contracts unilaterally in response to
contralateral touchdown only, controlling
movement of the trunk in the oblique and
frontal planes (Shapiro and Jungers, 1988).
In the chimpanzee, this “bipedal” pattern is
maintained from the same basic pattern
characterizing quadrupedalism. In fact, although the chimpanzee differs from the cat
with respect to a lack of ipsilateral activity
in iliocostalis during quadrupedalism, this
same lack of ipsilateral activity occurs when
the chimpanzee walks bipedally. In other
words, the recruitment patterns used in
quadrupedalism for control of the trunk or
stabilization of the pelvis appear to serve
equally well for control of the fore-aft and
lateral movements of the trunk associated
with bipedalism (Thorstensson et al., 1982,
Unlike the bipedal patterns of the other
hominoids, all three back muscles in the
orangutan respond solely to contralateral
touchdown. The results for the orangutan
are consistent with its awkward and “unnatural” form of bipedal walking (orangutans
have not been observed walking bipedally in
the wild; Sugardjito, 19821, and indicate
that for this hominoid, the maintenance of
balance requires almost exclusively side to
side control of the trunk (i.e., in the frontal
plane). The more human-like bipedalism
employed by the chimpanzee and gibbon is
characterized by control of movements in
both the sagittal and frontal planes. In
chimpanzees, gibbons, and humans, however, back-muscle activity associated with
contralateral touchdown is of higher amplitude than that responding to ipsilateral
touchdown (for those muscles with adequate
lateral leverage; longissimus and iliocostalis). This suggests that one of the most demanding mechanical requirements of bipedalism in hominoids is the necessity to
prevent the trunk from swaying in the frontal plane (Keith, 1923)- the response to
which is most exaggerated in the least natural biped, the orangutan. The uniqueness of
the orangutan’s back-muscle activity in bipedalism also accounts for the fact that
back-muscle recruitment patterns differ between quadrupedal and bipedal walking in
this highly specialized/suspensory hominoid
(unlike the results for the chimpanzee; cf.
Figs. 4,5).
Vangor and Wells (1983) found that for
several hind-limb muscles in Ateles, Lagothrix, and Erythrocebus, the phasic activity
patterns characterizing quadrupedalism
were very similar to those associated with
bipedalism in the same animals. In other
words, the functions of those particular
hind-limb muscles in bipedal gait were “conserved” from quadrupedal walking. In addition, for those muscles, the patterns for qua-
drupedal and bipedal walking were also
used by Ateles and Lagothrix during vertical
climbing. For other hind-limb muscles, recruitment patterns used in bipedal walking
were found to be different from those observed during quadrupedal walking, but
similar to those used during vertical climbing. Vangor and Wells (1983) concluded
from their results that “vertical climbing,
therefore, rather than quadrupedal walking, may establish a phasic activity pattern
for a particular muscle which is conserved
when the primate undertakes bipedal walking” (pp. 133-134). In other words, they considered climbing to be “preadaptive” for bipedalism (see also Prost, 1980; Fleagle et al.,
1981). Finally, Vangor and Wells (1983)
found no specific or consistent resemblance
to human bipedalism in the phasic activity
patterns of various hind-limb muscles during nonhuman primate quadrupedalism, bipedalism, or vertical climbing. The implication of their results is that “the ancestor of
bipedal humans. . . had to undergo much
change in muscle function with the evolution of bipedal gait, whether or not it was
originally human-like in gross structure or
gross locomotor behavior” (Vangor and
Wells, 1983:134).
The overall similarity in back-muscle activity reported here for quadrupedalism,
nonhuman bipedalism and human bipedalism is noteworthy. It suggests that, contrary
to Vangor and Wells’ (1983) statement regarding hind-limb muscle function, the ancestor of bipedal humans would not have
had to undergo major change in back-muscle
function with the evolution of bipedal gait.
Notwithstanding the similarity in back
function during quadrupedalism and bipedalism, similar back-muscle EMG patterns
in vertical climbing and bipedalism would
lend further support to the notion that
climbing is preadaptive for bipedalism. We
are currently investigating back-muscle
function in vertical climbing and other suspensory behaviors in nonhuman primates
(see also Hurov, 1982).
The suggestion that primate “spinal circuitry” differs from that characterizing
nonprimate mammals (as a result of the evolution of primates’ emphasis on grasping
and manipulative abilities of the forelimb)
has been based largely on the observed differences in forelimb muscle EMG patterns
between primates and other mammals (Larson and Stern, 1987; Vilensky, 1987, 1989;
Vilensky and Larson, 1989; Larson and
Stern, 1989). If primate neural circuitries
diverged from that of other mammals, it is
possible that this evolutionary specialization may be reflected only in forelimb muscle function, since this is the part of the body
on which “neural evolution”has presumably
directly acted. Therefore, the lack of pronounced differences between primates and
nonprimate mammals in back (and hindlimb) muscle function neither adds support
nor weakens this neurological hypothesis.
This study represents the first time the
EMG of back muscles during quadrupedalism in primates has been documented. The
results can be summarized as follows:
1.In Pan, Pongo, and Papio, back muscles
restrict movements of the trunk by responding to touchdown of one or both feet during
quadrupedalism, with an emphasis especially in the hominoids on the response to
contralateral touchdown. Recruitment patterns during quadrupedalism are generally
consistent across species, as was reported
for bipedalism (Shapiro and Jungers, 1988).
2. Nonprimate mammals (i.e., cats and
dogs) and primates recruit their back muscles in a generally similar fashion (but not
identically) during quadrupedal walking despite the differences between these two
groups in footfall sequence and forelimb
muscle recruitment patterns. The discrepancies in back-muscle EMG patterns that
were observed between hominoids on the
one hand and cats and monkeys on the other
most likely reflect differences in muscular
arrangement, general body shape andlor
kinematic differences in walking between
these two groups.
3. There is a fundamental similarity in
back-muscle activity patterns during quadrupedalism (nonprimate and primate) and
bipedalism (including humans), despite the
differences in mechanical demands placed
on the back in these two behaviors.
In conclusion, back-muscle activity patterns demonstrate a basic conservatism
across animals and locomotor behaviors.
This finding contrasts with EMG studies on
the primate forelimb (Larson and Stern,
1987, 19891, but does not preclude the suggestion that aspects of primate neural circuitry for locomotion are unique. Regardless, the results reported here are consistent
with other electromyographic data pointing
to considerable conservatism in the evolution of the neural control of tetrapod limb
movement (Peters and Goslow, 1983 and
references therein).
The EMG data could not have been collected without the help of Susan Larson,
Jack Stern, Hillary Johnston, Malcolm McClinton, Aaron Blaisdell, and Marianne
Crisci. Daniel Schmitt deserves special
thanks for his help in data analysis, and
thanks also go to George Boykin and
Charles Garrison for their patience and generosity concerning dissection materials. The
paper was improved by the suggestions of
two anonymous reviewers, and John Fleagle, Jack Stern, and Farish Jenkins provided useful comments and discussion on an
earlier version of the manuscript. This research was supported by NSF grants to Jack
Stern: BNS 8519747, BNS 8606781, BNS
8819621, BNS 8823083, and DBS 9209004,
and by the University of Texas at Austin
Research Institute.
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muscle, primate, electromyography, bipedal, quadrupedal, back, walking
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