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Gait characteristics of two squirrel monkeys with emphasis on relationships with speed and neural control.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 68:429-444 (1985)
Gait Characteristics of Two Squirrel Monkeys, With Emphasis on
Relationships With Speed and Neural Control
JOEL A. VILENSKY AND M. CHARLENE PATRICK
Departments ofAnatomy ( J A . I?) and Physiology (M.C.i?),Indiana
University School of Medicine, Fort Wayne, Indiana 46805
KEY WORDS
Primates, Squirrel monkeys, Gait, Locomotion,
Speed, Neural control
ABSTRACT
Two adult squirrel monkeys (one of each sex) were trained to
locomote on a motor-driven treadmill at seven fixed speeds within 0.89-2.58
&second. Subsequently, the animals were filmed while locomoting at these
speeds, with the films then being used to determine gait parameters. The
female monkey exhibited lateral-sequence symmetrical gaits at slow speeds,
and transverse and rotatory gallops at fast speeds. The male used lateralsequence symmetrical gaits at all speeds. The squirrel monkeys exhibited
typical relationships between temporal gait parameters and increased speed,
with these relationships continuing across the run-gallop transition. An analysis of footfall intervals (delays) and support patterns indicated that during
symmetrical gaits these monkeys emphasized lateral support. During galloping, one delay, the trailing hindlimb to trailing forelimb, was found to be very
stable, both across speeds and for both types of galloping. Also during galloping, swing duration was found t o be more variable than stance duration.
These findings are interpreted with regard to understanding the neural
control of locomotion in tetrapods, and more specifically, in primates. The
latter part of this discussion revolves around three basic differences between
primate and non primate gaits: (1) utilization of diagonal-sequence gaits by
primates (although the squirrel monkeys were atypical in this regard); (2)
absence of a running trot in primates; and (3) absence of stepping following
spinal cord transection in primates. These three differences reflect greater
supraspinal control of locomotion in primates, and possibly intrinsic differences in the coupling of spinal locomotor generators.
The patterns exhibited between changes in pear to progress directly from a diagonalspecific gait parameters and increasing speed sequence, diagonal-couplets run into a gallop
have been successfully used by investigators (Rose, 1977; Vilensky, 1983). Finally, and
to infer neural mechanisms of locomotor con- perhaps most importantly, in most mammals
trol in quadrupeds, most commonly cats (6. stepping movements can be elicited following
Wetzel and Stuart, 1976; Grillner, 1981),but spinal transection. Such is not the case for
only by Vilensky (1983) for primrtes. Al- primates (Eidelberg et al., 1981). Eidelberg
though a priori it would seem that the re- (1981)suggested this may indicate that spinal
sults from other quadrupeds would be step generators in primates either require
directly applicable to primates, there is rea- greater tonic facilitatory input from sources
son to expect some differences. Most impor- outside the cord, or that the generators are
tantly, primates typically use diagonal- superseded by other neural control mechasequence gaits while almost all other quadgaits*Additionr'peds use
Received March 21, 1985; revised July 2,1985 accepted July
ally, primates typically do not have a gait 8, 1985.
to the running trot Of most M.Charlene Patrick's current address is: Department of Biolcursors (Hildebrand, 1967). Rather, they ap- ogy, Purdue University, w.Lafayette, IN 47907.
0 1985 ALAN R. LISS, INC.
430
J.A. VILENSKY AND M.C. PATRICK
nisms. Thus, the neural control of locomotion
may differ between primates and other mammalian quadrupeds.
In Vilensky’s (1983) report, gait data and
the implications of these data were presented
for two macaques (with many more data
available for one of the two animals) across a
wide variety of speeds including the run-gallop transition. In this paper, we present a
similar report on the gait of two squirrel
monkeys. However, in contrast to the first
report, gait data are available for both animals across all speeds and more than one
stride is available for every speed. Additionally, some of these data are compared with
previously compiled data on cats (cf. Vilensky and Patrick, 1984).
MATERIALS A.ND METHODS
Two adult squirrel monkeys (Saimiri sciureus), one male (0.63 kg) and one female
(0.57 kg), were the subjects of this study.
They were trained to locomote on a motordriven treadmill (1.17 m x 0.43 m belt) which
was enclosed in a Plexiglas cage. Each training session generally consisted of a 10-20minute episode with food rewards being used
to induce the desired behavior (steady-state
locomotion on the treadmill belt). These sessions were conducted daily (including weekends) for approximately 3 weeks, by which
time both monkeys appeared comfortable on
the treadmill and locomoted readily at a variety of speeds. The monkeys were then
filmed with a motor-driven camera operating
a t 100 frameslsecond while locomoting on the
treadmill. This filming rate was verified by
timing markers located on the film at 0.01second intervals. The treadmill speeds used
during filming were 0.89, 1.17, 1.44, 1.72,
1.99, 2.28, and 2.58 rrdsecond (+ 0.02 d s e c ond). This approximate range and assortment of speeds had previously resulted in
good comparative data in a study of cat locomotion (Vilensky and Patrick, 1984). The
filming trials consisted of 10-20-second bouts
a t each speed.
After the films were developed, each stride
(defined as left-hind limb [Lh] contact to the
following Lh contact) was evaluated to determine its suitability for analysis. The most
critical factor in distinguishing a “good” from
a “no good” stride was whether the animal
maintained a n invariant position on the
treadmill belt. This was determined by comparing tracings of the animal’s rump a t con-
secutive Lh footfalls. A stride was considered
“good” when the rump was in nearly the
identical location (within 3 cm actual distance) at these footfalls. Thus, for “good”
strides it could be assured that the animal
was locomoting at, or very close to, the speed
shown on the treadmill speedometer (which
was visible to the camera). In addition to
movement relative to the belt, unusual actions such as the animal turning its trunk or
touching part of the Plexiglas cage during a
stride resulted in a “no good” stride. When
more than one gait was utilized within a
specific trial (e.g., running and galloping),
this trial was subdivided with the strides
comprising each gait considered separate
trials. A maximum of ten “good” strides were
analyzed for each speed. The minimum number of “good” strides available for any specific trial was four, and the mean for all trials
was 9.5.
Following the “good” vs. “no good” determination, Hildebrand (1966) gait diagrams
were constructed for all “good” strides. The
diagrams for each trial were then normalized
and averaged using methodology previously
described (Vilensky and Patrick, 1984).Thus
a mean or “typical” stride was computed for
each trial. These strides permitted comparisons across speeds, between the two individuals, and between the squirrel monkey and
cat data.
RESULTS
Footfall patterns and delay periodssymmetrical gaits
Figures 1 and 2 depict mean Hildebrand
(1966)gait diagrams for each monkey at each
speed. The variability about these mean diagrams is not depicted in the figures because
of the added complexity. However, the maximum standard deviation for cycle duration
was 27 msec (male, 1.44 dsecond; see also
Fig. 41,while that for any single limb’s absolute swing or stance duration was 31 msec
(male, Lf, swing, 1.44 dsecond).
It is apparent from Figure 1 that the male
monkey used symmetrical gaits with a n
LhLfRhFtf footfall sequence at all speeds. At
the lower speeds he employed a lateral-sequence, lateral-couplets walk (terminology in
accordance with Hildebrand) and progressed
to a lateral-sequence, single-foot run a t
speeds above 1.17 dsecond. Figure 1 also
illustrates a general decrease in cycle and
stance durations with increasing speed (see
below).
431
GAIT CHARACTERISTICS OF SQUIRREL MONKEYS
SPEED (MIS)
Lh
Lf
Rf
Rh
Lh
Lf
Rf
Rh
Lh
Lf
Rf
Rh
Lh
Lf
Rf
Rh
Lh
Lf
Rf
Rh
.89
1.17
1.44
1.72
1.99
Lh
Lf
Rf
Rh
2.28
Lh
Lf
Rf
Rh
2.58
I
I
I
.10
I
.20
I
.30
I
.40
.do
CYCLE DURATION (SEC)
Fig.1. Gait diagrams (Hildebrand,1966) for the male monkey at each speed.
Table 1details the absolute and relative (%
of cycle duration) delay intervals (time between limb footfalls) for the male monkey
using the left limbs as standards. Because
the male used only symmetrical gaits, the
right comparable delays were similar. The
table shows that across all speeds the absolute delay between ipsilateral hind-fore limbs
(Lh-LO ranged only between 60 and 80 msec;
however, a good inverse relationship with
speed was evident. The values for the reciprocal ipsilateral delays (Lf-Lh) were much
greater at all speeds, but showed a similar
inverse relationship with speed. The diagonal (Lh-Rf; Lf-Rh) and homologous (Lh-Rh;
Lf-Rf) absolute delays also exhibited notable
decreases with increased speed, as well as
very high correlation coefficients. Analysis
of the relative values presented in Table 1
reveals little change in any of the delays
across speed, the maximum range being approximately six percentage points (Lf-Rh
delay).
Figure 2 presents gait diagrams for the
female. For 1.44,2.28, and 2.58 &second two
diagrams are presented because two types of
gait were used at each of these speeds (cf.
Materials and Methods). The female used a
lateral-sequence, lateral-couplets walk at
0.89 mlseconds and a lateral-sequence, sin-
J.A. VILENSKY AND M.C. PATRICK
432
TABLE 1. Absolute (msec) and relative (%) mean delays for the male at each speed, with correlation
coefficients for the absolute delays
Speed (mid
Absolute
0.89
1.17
1.44
1.72
1.99
2.28
2.58
r value*
Relative
0.89
1.17
1.44
1.72
1.99
2.28
2.58
Lh-Lf
Lh-Rh
Lh-Rf
Lf-Rh
Lf-Lh
Lf-Rf
80
75
70
65
70
65
60
- .9:3
220
190
170
160
160
145
130
- .98
310
270
260
230
220
220
200
- .98
140
I115
95
95
90
80
70
- .98
385
325
305
275
255
265
205
- .96
230
195
185
165
150
150
140
- .99
17.2
18.7
19.9
19.0
21.7
19.8
20.4
47.3
47.3
45.1
46.8
49.7
44.1
44.2
66.7
67.2
69.0
67.3
68.3
66.9
68.0
30.1
28.6
25.2
27.8
28.0
24.3
23.8
82.8
81.3
80.1
81.0
78.3
80.2
79.6
49.5
48.5
49.1
48.2
46.6
45.6
47.6
*Correlation coefficient be1.ween log speed and log delay.
gle-foot walk a t 1.17 and 1.44 (,‘A’’ diagram)
dsecond. However, at the higher speeds and
at 1.44 (“B” diagram) dsecond, she used
asymmetrical gaits (gallop; see below). For
symmetrical gaits the absolute delay between the Lh-Lf footfalls increased slightly
with increasing speed, ranging between 80
and 110 msec, while all the other delays calculated (i.e., those depicted in Table l) decreased. Expressed in relative values, the
ipsilateral Lh-Lf delay again displayed a n
increase as speed increased, ranging between
16.6 and 29.8% of the cycle, while the Lf-Lh
delay showed a complementary decrease. The
relative delays between homologous limb
pairs showed no relationship with speed,
ranging between 45 and 55% of the cycle.
The Lh-Rf diagonal delay increased with
speed from 66 to 75% of the cycle, while the
Lf-Rh delay decreased from 29 to 19%.
ration and these relative values are also included in the table.
Homologous delays: The absolute delay between the trailing forelimb (FT) and leading
forelimb (FL)as well as the reciprocal delay
(FL-FT)generally decreased with increasing
speed. In both cases the rotatory gallops C‘B”
speeds) showed slightly higher values than
the transverse gallops at the same speed.
The relative values of these delays are fairly
stable with one set being the complement of
the other.
The absolute delay between the trailing
hindlimb (HT) and leading hindlimb (HL)as
well as its reciprocal, HL-HT, generally decreased with speed for the transverse gallops.
The rotatory gallop delays were notably high
for the HL-HT interval and notably low for
the HT-HL interval. The relative HT-HL delay showed a tendency to decrease while its
complement, HL-HT, increased.
Trailing fore-hind delays: The FT-HTabsoFootfall patterns and delays-asymmetrical
lute delay decreased (with the rotatory galgaits
lops showing high values) while the HT-FT
The gait diagrams for the galloping strides delay was very consistent, ranging over only
15 msec. In relative terms the FT-HTdelay
of the female (Fig. 2) indicate that a t 1.44 (€3)
and 1.72 dsecond she used a right lead decreased with speed while the HT-FTdelay
transverse gallop, while left lead transverse increased.
Leading fore-hind delays: The FL-HLabsogallops were used at 1.99, 2.28 (A), and 2.58
(A) dsecond. Rotatory gallops were used as lute delay decreased with speed while the
well at the two highest speeds (B diagrams), HL-FLinterval was almost constant, but the
rotatory gallops had higher values than the
both with Rh and Lf leads.
Absolute delays between trailing and lead- transverse gallops. In relative terms, the FLing footfall combinations during galloping HL delay decreased with the rotatory gallops
were calculated from the female’s gait dia- showing lower values. The complementary
grams. These data are presented in Table 2. pattern was evident for the relative HL-FL
Each value was then normalized to cycle du- delay.
433
GAIT CHARACTERISTICS OF SQUIRREL MONKEYS
SPEED (MIS)
Lh
Lf
.89
Rf
Rh
Lh
Lf
Rf
Rh
1.17
Lh
Lf
Rf
Rh
1.44(A)
Lh
Lf
Rf
Rh
Lh
Lf
Rf
Rh
1.44(8)
1.72
1.99
2.28 (A)
2.28 (B)
2.5 8 (A)
CYCLE DURATION (SEC)
Fig 2. Gait diagrams (Hildebrand, 1966)for the female monkey at each speed At 1 44.2 28,
and 2.58 &second two types of gait were recorded (A and B; see text)
J.A. VILENSKY AND M.C. PATRICK
Fore trailing-hind leading delays: The FTHL absolute delay showed a dramatic decrease with speed, with the rotatory and
transverse gallops exhibiting consistent values. The reciprocal delay (HL-FT) increased,
with the rotatory gallops having higher values. In relative terms, the FT-HL delay
showed a notable decrease while the HL-FT
delay increased.
Fore leading-hind trailing pairs: The FLH T and the HT-FLdelays both tended to decrease with speed although for the HT-FL
delay the rotatory gallop values were high.
In relative terms, the FL-HTdelay decreased
while the HT-FLdelay increased.
To further analyze the female's asymmetrical gaits we computed the duration that
one or both hindlimbs contacted the ground
during a cycle (total hindlimb support) and
the interval between the midpoint of forelimb stance and the midpoint of hindlimb
stance (midtime lag), both expressed as a percentage of total stride duration (cf. Hildebrand, 1977). These values are plotted in
Figure 3. For the transverse gallops total
hindlimb support decreased and midtime lag
increased, as speed increased. Values for the
rotatory gallops are located together, showing the same midtime lag value as the trans-
*transverse
o ro t o t o ry
90
80
70
60
50
40
TOTAL HINDLIMB SUPPORT (%)
Fig. 3. Plot of midtime lag (interval between the
midpoint of the forelimb stance and midpoint of the
hindlimb stance) vs. total hindlimb support (both as percentages of cycle duration) for the galloping speeds of
the female (cf. Hildebrand, 1977). The arrowhead indicates the direction of increasing speed along the dashed
line connecting the points for the transverse gallop at
each speed. The points for the two rotatory gallops are
indicated separately.
435
GAIT CHARACTERISTICS OF SQUIRREL MONKEYS
.5-
I
+
.4-
A
-
2:
.3-
Z
0
I-
s
.5-
3
n
A
u
symmetrical
transverse g a l l o p
rotatory g a l l o p
-1
*
U
U
.a-
.3-
I
I
1.o
2.0
3: 0
SPEED (MIS)
Fig. 4. Plot of mean cycle duration vs. speed for the female (A) and the male (B). The bars
indicate the range about each mean.
verse 2.28 dsecond gallop, but less total
hindlimb support.
creased with increasing speed for all the
limbs. The absolute value of the correlation
coefficients for this relationship (computed
Cycle duration
using the log of the mean absolute stance
value
for all the limbs at each speed vs. log
Figure 4 depicts mean cycle durations at
each speed for both monkeys, with bars indi- speed) were greater than .99 for both moncating the range for each trial. Cycle dura- keys. Interestingly, the drop in mean absotion clearly decreased with increasing speed. lute stance duration across the speeds over
The correlation coefficients (computed with which the female galloped was very similar
log values) for this relationship were high: for both animals, approximately 70 msec.
In addition to revealing the relationship
-0.98 for the male and -0.96 for the female.
It is noteworthy that across the speeds of the between absolute stance duration and speed,
galloping trials (1.44 to 2.58 &second) the Figure 5 indicates that the hindlimbs generfemale exhibited a decrease in mean cycle ally had greater stance values at all speeds.
duration of 50 msec, while the male’s de- This was also true for the female. However,
crease in cycle duration over this same range statistical comparisons of slopes and interusing symmetrical gaits was 80 msec. From cepts between regression equations relating
the data for the female presented in Figure forelimb stance duration with speed and
4, it is also apparent that the rotatory gallop hindlimb stance duration with speed yielded
strides were longer than the transverse gal- no significant differences (method of Kleinbaum and Kupper, 1978).
lops at the same speed.
Relative: Similar t o absolute stance, relaStance durations
tive stance duration showed a very strong
Absolute: Figure 5 displays mean absolute inverse relationship with speed. For both anstance durations for each limb at each speed imals the correlation coefficients (absolute
for the male. Stance duration clearly de- value) for this relationship were greater than
.98 (linear fit).
J.A. VILENSKY AND M.C. PATRICK
436
.3(
A
.2!
Lha
L f rn
I
=zf
Rhr
Rf
.2(
YI
V
A
Z
a
a
Iv)
u
:
I-
3
2m
.I!
a
A
a
m
'
t
.1(
2.0
1.0
3.0
SPEED (MIS)
Fig. 5. Plot of absolute stance duration vs. speed for the four limbs of the male.
Swing durations
Figure 6 depicts mean absolute swing durations for the female's forelimbs and hindlimbs (left and right values were pooled) at
each speed. It is apparent from this figure
that there was no overall trend with speed.
However, the figure does indicate that the
forelimbs had greater swing durations than
the hindlimbs at every speed. Furthermore,
a t test between the mean forelimb and mean
hindlimb swing values for all speeds indicated a significant difference ( P < .05). Figure 6 also reveals that the swing durations
during rotatory gallops (B diagrams at 2.28
and 2.58 dsecond) were greater than during
any other speed or gait.
The absolute swing duration data from the
male were similar to those of the female in
that no trend was evident with speed and a
significant difference (P< .02) was evident
between the mean fore and hindlimb values.
Relative swing duration is the reciprocal of
relative stance and thus this parameter increased as speed increased (see above).
Support patterns
Table 3 depicts the limb combinations contributing to each animal's support at each
speed. Each support pattern listed includes
GAIT CHARACTERISTICSOF SQUIRREL MONKEYS
437
Hindlimb
Forelimb
-
z
.22
I
2 .21
Z
0
c
<
w
=)
n
0
.20
z
3
.19
v)
.18
.17
89
J
144[Al
2.28[A)
SPEED [MIS)
Fig. 6. Histogram showing mean forelimb and mean hindlimb swing durations for the
female at each speed. A and B sets of bars at 1.44, 2.28, and 2.58 &second correspond to
different gaits at these speeds (see text).
fore, the utilization of only lateral-sequence
symmetrical gaits by both squirrel monkeys
was unexpected. Considering this result, we
questioned whether the treadmill had somehow induced an “artificial” gait in these animals. We concluded this to be unlikely
because the macaques described in Vilensky
(1983) used only diagonal-sequence symmetrical gaits on a treadmill. Similarly, recently
filmed vervet monkeys locomoting on the
identical treadmill used by the squirrel monkeys, predominantly utilized diagonal-sequence gaits. Finally, Prost and Sussman
(1969) reported that a footfall pattern of
LhLfRhRf (lateral-sequence) was preferred
(used 63% of the time) by a female squirrel
monkey walking on level ground, while the
LhRfRhLf pattern (diagonal-sequence) was
used more frequently on inclined surfaces.
Clearly, the lateral-sequence gaits utilized
by our subjects are typical for Saimiri during
walking on level surfaces. The question thus
DISCUSSION
raised is why squirrel monkeys are unlike
Footfall patterns
most other primates. According to Rollinson
Primates, in contrast to most other quad- and Martin (1981) diagonal-sequence gaits in
rupeds, typically utilize diagonal-sequence primates result from a more posteriorly losymmetrical gaits (Hildebrand, 1967). There- cated center-of-gravity (CG) compared to
all limb combinations making up that group
(e.g., triplets refers to all four, three-legged
combinations).Neither periods of full suspension (i.e., “no foot” support) nor of four limb
support were exhibited by either monkey,
and thus these categories are not listed in
the table. It is apparent that support by triplets was only evident at the slower speeds,
not being present past 1.72 dsecond. Support by diagonals also decreased with speed
and was not evident at all during the rotatory gallops. Fore-hind pair support was only
evident during galloping and generally decreased with increasing speed. With one
small exception (female, 2.28B), support by
lateral pairs was only apparent during symmetrical gaits and also decreased with increased speed. Finally, support by single
limbs increased as speed increased and was
notably greater during rotatory gallops, than
during identical speed transverse gallops.
438
J.A. VILENSKY AND M.C. PATRICK
TABLE 3. Support patterns for the male and female monkeys at each speed expressed as percent of cycle’
Speeds ( d s )
Male
0.89
1.17
1.44
1.72
1.99
2.28
2.58
Female
0.89
1.17
1.44 (A)’
1.44 (B)
1.72
1.99
2.28 (A)
2.28 (B)
2.58 (A)
2.58 (B)
Triplets
Diagonals
Fore-Hind
Laterals
Singles
24
10
4
0
0
0
0
22
32
30
22
20
14
12
0
0
0
0
0
0
0
54
58
50
50
44
34
36
0
0
16
28
36
52
52
28
6
8
16
2
0
0
0
0
0
20
34
42
32
30
26
16
0
4
0
0
0
0
28
32
30
24
24
22
16
52
54
36
0
0
0
0
2
0
0
0
6
14
24
36
44
60
74
74
84
‘Triplets refer to all possible three-legged combinations; Diagonals to Lh/Rf or Rh/Lf; fore-hind to LfRf or Lh/Rh; laterals
to LIuLf or Rh/Rf; singles to any individual limb.
‘At 1.44, 2.28, and 2.58 m i for the female, two types of gait were recorded (A and B; see text).
other mammals. Specifically, they imply that
in primates the CG is located closer to the
hip joint, while in nonprimates it’s located
closer to the shoulder joint. Thus, if squirrel
monkeys have a more anteriorly located CG
relative to other primates (i.e., closer to the
shoulder joint), their utilization of lateralsequence gaits might be explained. Unfortunately, no direct CG measurement exists for
Saimiri; however, their relatively large
brains and skulls (Hill, 1960) might account
for a more forward CG location. Rollinson
and Martin employ this argument with reference to the use of lateral-sequence gaits in
very young primates.
In terms of asymmetrical gaits, the female
squirrel monkey utilized both transverse and
rotatory gallops. These two types have also
been reported to occur in other primate species (Prost, 1969; Wells, 1974; Rose, 1977).
Thus, squirrel monkeys are not atypical with
regard to asymmetrical gaits. However, the
lack of galloping by the male is incongruous.
Although the trot (run; see below)-gallop
transition has been reported to occur at
speeds which scale as a function of body size
(Heglund et al., 19741, the predicted trot(run)gallop transition speeds for the male and female monkeys differed only by 0.03 mlsecond. Furthermore, the female’s actual transition speed (1.44 &second) was close to the
predicted value (1.33 dsecond). Thus the
male’s lack of galloping is apparently best
related to “psychological” factors rather than
physiological ones. That is, the treadmill and/
or training conditions somehow inhibited his
switching gaits. We have recently observed a
similar situation in a young vervet monkey.
Therefore, the data from the higher speeds
for the male may be considered to be somewhat anomalous. Nevertheless, these data
are very useful for comparative purposes,
both interspecifically (following paragraph)
and intraspecifically (below).
Figure 7 depicts a comparison of the male
monkey’s footfall patterns (B) with those of a
cat (A) a t identical speeds. The cat, similar to
the male monkey, used symmetrical gaits a t
these speeds (although she galloped as well
at the faster of these speeds in different
trials). The patterns from both animals have
been normalized. The cat data are from a n
animal used for a report on cat locomotion
(Vilensky and Patrick, 1984). Figure 8 presents the same data on a modified version of
Hildebrand’s (1966)basic gait graph with the
arrowheads indicating the direction of increasing speed. At 0.89 and 1.17 mlsecond
the footfall patterns of the two animals are
nearly identical (Fig. 71, both being lateralsequence, lateralcouplets walks. However, at
1.44 mlsecond the cat switched (note sharp
drop in Fig. 8) to a lateral-sequence, diagonal-couplets walk, and to a running trot a t
higher speeds (except a t 1.99 mlsecond when
a lateral-sequence, diagonal-couplets run was
GAIT CHARACTERISTICSOF SQUIRREL MONKEYS
439
A
Lh
Lf
Rf
Rh
Lh
Lf
Rf
Rh
Lh
Lf
Rf
Rh
Lh
Lf
Rf
1.72
Rh
Lh
If
1.99
Rf
Rh
Lh
Lf
Rf
Rh
Lh
Lf
Rf
Rh
0
40
20
60
80
100
70OF TOTAL CYCLE
0
20
40
60
80
TOOF TOTAL CYCLE
100
Fig. 7. Normalized gait diagrams mildebrand, 1966)for a cat (A) and the male monkey (B)
at identical speeds.
c---.cat
L
4
50
70
0
60
I
50
Lh STANCE
I
40
I
30
(%I
Fig. 8. Plot of the Lh-Lf footfall interval (delay) vs.
Lh stance duration (both as percentages of cycle duration) for the male monkey and for the cat depicted in
Figure 7. Each point represents the values at a particular speed with the arrows indicating the direction of
increasing speed. This diagram is a modification of Hildebrand’s (1966) basic gait graph.
used). In summary, at 1.44 &second the cat
underwent a transition to a trotlike gait, and
as speed increased the “trot” tended to become more synchronized. No such transition
was apparent for the monkey. This difference
may be important with regard to the neural
control of locomotion in primates (see below).
Finally with regard to footfall patterns, an
examination of the female squirrel monkey’s
gait diagrams (Fig. 2) between 0.89 and 1.44
dsecond shows a definite trend toward galloping with the transverse gallop at 1.44 (B)
&second being the culmination of this trend.
Specifically,at 0.89 dsecond the Lf-Rh delay
was large, but as speed increased this interval rapidly decreased; finally, at 1.44 (B) d
second Rh footfall occurred before Lf footfall.
Thus it appears as if the female’s symmetrical gaits were changing in such a way that
galloping would be facilitated. Although the
Lf-Rh delay in the male also decreased over
these speeds, the rate of decrease was less; at
1.44 dsecond the two footfalls were still separated by 95 msec (Table 1). This difference
explains why the Lh-Lf absolute delay remained relatively constant in the male but
increased in the female.
440
J.A. VILENSKY AND M.C. PATRICK
Cycle, stance, and swing durations
The decrease in cycle duration with speed
reported for the squirrel monkeys is well documented for other quadrupeds, as well as for
humans (cf. Vilensky and Ghelsen, 1984).Interestingly, in contrast to Heglund et al.
(1974)this decrease continued across the galloping speeds in the female. Others have also
indicated cycle duration continues to decrease once galloping is initiated (Norgren et
al., 1977; Vilensky, 1983). However, the rate
of decrease in cycle duration was smaller
across the female’s galloping speeds than
across the male’s similar speed symmetrical
gaits. In contrast, absolute stance duration
appeared to decrease at the same rate regardless of the gait being used (i.e., both
monkeys showed approximately the same decrease across the galloping speeds).
The noted differences in the swing and
stance durations of the forelimbs and hindlimbs of the squirrel monkeys (hindlimbs
generally having greater stance and shorter
swing durations) are opposite to those reported for cats (cf. Afelt and Kosicki, 1975;
Halbertsma, 1983; Vilensky and Patrick,
1984). However, the squirrel monkey pattern
is not consistent across primate species (cf.
Hildebrand, 1967) and probably relates to the
relative lengths of the fore and hindlimbs.
Finally, the almost linear increase in midtime lag as speed increased during galloping
in the female (Fig. 3) is noteworthy. Such
data are not available for any other animal
and thus inter or intraspecific comparisons
are precluded. Based on this animal, it is
clear that as speed increased there was
greater separation of the hindlimb and forelimb propulsive strokes. This undoubtedly
relates to the greater overall force requirements accompanying increases in speed.
Delays and support patterns
Previous reports on primates have emphasized the utilization of diagonal support
(Prost, 1965, 1969; Rollinson and Martin,
1981; Vilensky, 1983). In contrast to these
previous reports, but in accordance with their
use of lateral-sequence gaits, the squirrel
monkeys emphasized lateral support during
symmetrical gaits. That is, the Lh-Lf footfall
interval (an ipsilateral delay) was generally
short regardless of speed while the “next”
delay in the lateral footfall sequence, Lf-Rh
(a diagonal delay), was notably longer a t most
speeds (Table 1). Furthermore, during all
symmetrical gaits except 1.44 (A) &second
for the female, support by “laterals” was
greater than support by “diagonals” (Table
3).
The emphasis on lateral support during
slower speeds by both squirrel monkeys is
apparently similar to the situation in the cat
(Fig. 7) and by inference, to most quadrupeds.
Obviously, the advantages of lateral-sequence gaits (cf. Gray, 1944) supersede any
problems caused by lateral support (e.g., rolling tendencies). However, as speed increases
most quadrupeds begin to trot. This gait emphasizes diagonal support, which would seem
to be more stable. With regard to the monkeys, the female galloped once speed reached
1.44 dsecond; however, the male continued
to use what would appear to be a very unbalanced gait. Obviously, since he was able to
locomote quite well using this gait, mechanical optimization is not the only concern of a
locomoting animal.
The absolute and relative delays for the
female during asymmetrical gaits are meaningful with reference to comparable data for
cats (Eisenstein et al., 1977; Norgren et al.,
1977; Wetzel et al., 1977). For cats the FT-FL
delay was reported to occupy approximately
25% of the cycle across all types of galloping.
The monkey was remarkably similar in this
measure (Table 2). During transverse and
rotatory galloping, the HT-HLinterval in cats
ranged between 11 and 37%,with some indication of it being longer during the transverse type. This again is fairly consistent
with our results. With regard to fore-hindlimb interactions, the main conclusion from
the cat studies was that the HT-FT interval
is more stable than any other delay, lasting
approximately 100 msec, or about one-third
of cycle duration. In the squirrel monkey the
HT-FT delay was also very stable, with the
values across all speeds and both types of
galloping ranging only from 150 to 165 msec,
or about 50%of the cycle. This 15-msecrange
was the least of all the delays. Thus, our
results and those for cats are similar. Based
on their findings, Wetzel et al. (1977) concluded that the HT-FT interval is the most
likely delay to be associated with the transmission of neural signals between the cervical and lumbar parts of the spinal cord during
galloping (see below).
Neurologic considerations: quadrupeds
Locomotor studies of intact as well as “reduced” animals have been used to infer the
basic patterns and constraints under which
GAIT CHARACTERISTICS OF SQUIRREL MONKEYS
the locomotor control system operates. These
patterns and constraints have in turn been
used to infer basic characteristics of the locomotor generators and the pathways connecting them (cf. Grillner, 1981). The data
presented in this paper contribute t o both of
these endeavors.
Cycle, stance, and swing durations: Our
most significant finding regarding the temporal components of locomotion in relation to
neural control is, that cycle duration, and
more importantly, absolute stance duration,
continue to decrease across the trot(run)-gallop transition. Furthermore, there does not
appear to be any marked discontinuity in the
rate of decrease in absolute stance at this
transition. Thus, although obviously the central pattern generators (CPGs) controlling
each limb (cf. Grillner, 1981) interact differently during symmetrical and asymmetrical
gaits, the afferents which trigger limb liftoff
appear to respond to changes in speed in the
same manner whether the animal is walking, running, or galloping. This relationship
is best represented by a power curve (cf. Goslow et al., 1973).
Additional evidence for stance duration following a rather strict program is that for the
two speeds at which both rotatory and transverse gallops were observed this parameter
was virtually identical for both types of galloping at each speed, while swing durations
were markedly different (Fig. 6). Thus, as
suggested above, the specific gait used by an
animal (whether symmetrical or asymmetrical) has virtually no effect on stance duration. On the contrary, our data support
previous reports indicating a high degree of
flexibility in swing duration during galloping (cf. Vilensky and Patrick, 1984).
Although it is reasonable to suggest that
our findings on the relationships between
temporal gait parameters during symmetrical and asymmetrical gaits and speed are
general (i.e., apply to most tetrapods), it is
possible that the differences between primate and nonprimate locomotion (see below)
may render them somewhat unique. This
caution is reinforced by Vilensky’s (1980) observation that the trot(run)-galloptransition
in a macaque did not occur at the predicted
stride rate (cf. Heglund et al., 1974). Similarly, the female squirrel monkey’s stride
rate at 1.44 dsecond was substantially less
than predicted by the equation presented by
Heglund et al. (1974).
Gait transitions: The transition between
walking and trotting in vertebrates is consid-
441
ered t o be continuous, while that between
trotting and galloping to be discrete (Wetzel
and Stuart, 1976). Although there is no clear
distinction between walking and trotting,
Figure 8 indicates that the transition between them may be more discontinuous than
previously believed (cf. also Vilensky and
Patrick, 1984). Furthermore, our finding that
neither squirrel monkey used a running trot,
and previous reports indicating that primates in general don’t use this gait (6.Hildebrand, 1967; Dagg, 1977; Rose, 1977; Vilensky, 19831, also support the view.
With regard to the trot-gallop transition,
Eisenstein et al. (1977) suggested that the
transverse gallop is the single gait that allows a smooth, rather than an abrupt trotgallop transition. It is clear from Figure 2
that a transverse gallop can similarly be
smoothly achieved directly from the footfall
pattern used during a lateral-sequence, single-foot walk. Obviously, therefore, the coupling patterns used by the CPGs of the limbs
do not necessarily have to pass through a
trotting phase to achieve transverse galloping.
Delays: In terms of delays, the most notable finding was that in squirrel monkeys and
cats the HT-FTinterval is remarkably stable
across different types of galloping, and across
speeds. Wetzel et al. (1977) suggested that
this stability is in accordance with evidence
(cf. Wetzel and Stuart, 1976) indicating that
touchdowns are moments of strong afferent
input. Thus, it is possible that this interval
is central to galloping; i.e., all other intervals
are based on this one. Obviously more data
need be accumulated for this to be assured.
Neurologic considerations: primates
There appear to be three major distinctions
between most primates and most nonprimate
tetrapods with regard to locomotor patterns:
(1) the difference in footfall sequence (diagonal vs. lateral-sequence);(2) the absence of a
running trot in primates; and (3) the lack of
stepping by spinalized primates (see beginning of paper). Each of these distinctions is
discussed below with appropriate neurological considerations.
The utilization of diagonal rather than lateral-sequence gaits by most primates is
thought to be related to physical (i.e., weight
distribution) rather than physiological (or
neurological) considerations (cf. above). Although this explanation is plausible and has
experimental backing (Tomita, 1967eited in
Kimura et al., 1979), there are some “nag-
442
J.A. VILENSKY AND M.C. PATRICK
ging” problems with it. For example, using
segment weights and CGs (Vilensky, 1979a)
we calculated the actual location of the total
body CG of a “typical” rhesus monkey standing with forelimbs vertically below the shoulder joint and hindlimbs vertically below the
hip joint. The results indicated a location
midway between the two joints rather than
closer to the hip joint. Furthermore, the CG
of the body undergoes anterior-posterior a s
well as ventral-dorsal movements during a
locomotor cycle (Vilensky, 1979b).Finally, although Rollinson and Martin (1981) cite evidence indicating more body weight support
on the hindlimbs in primates during static
postures, they fail to note that in two of the
monkeys tested by Kimura et al. (1979) the
maximum vertical force during locomotion
was approximately equivalent on the foreand hindlimbs. It was however notably
greater on the forelimbs in dogs. Interestingly, spider monkeys, which Rollinson and
Martin cite as often using lateral-sequence
gaits, apparently have much greater maximum vertical force on their hindlimbs than
forelimbs (Kimura et al., 1979). Thus the relationship between CG location, vertical support force, and gait utilization is still obscure.
Despite this obscurity, there seems little
doubt that primates are “hindlimb dominated” with regard to propulsion (cf. Kimura
et al., 1979; Rollinson and Martin, 1981).
However, this deduction also does not readily
explain the utilization of diagonal-sequence
gaits in primates. Clearly, highly hindlimb
dominated forms are predominantly saltatory (e.g., rabbits). However, when rabbits do
walk, they apparently use lateral-sequence
gaits (cf. Dagg, 1977). Additionally, the slow
loris is reported to use lateral-sequence gaits
(Tomita, 1973-cited in Kimura et al., 1979)
although its legs are “more powerful” (Napier and Napier, 1967). Thus, at this point,
we also question any direct relationship between “hindlimb dominance” and the utilization of diagonal-sequence gaits in primates.
Based on the above, it does not appear
likely that the braidbody ratio of squirrel
monkeys explains their use of lateral-sequence gaits. Additionally, Cebus, with a
similarly high braidbody ratio (Elias, 1977),
apparently uses diagonal-sequence gaits
(Tomita, 1973-cited in Kimura et al., 1979).
It is conceivable, however, that capuchin
monkeys, if tested on level surfaces or on a
treadmill, would use lateral-sequence gaits
because Prost and Sussman (1969) reported
Saimiri to prefer diagonal-sequence gaits on
inclined (arboreal?) surfaces. Finally, it
should be noted that the female squirrel
monkey was observed to use diagonal-sequence footfall patterns during acceleration.
In conclusion, the physical and/or physiological basis of the use of diagonal-sequence
gaits in primates is still uncertain and awaits
further testing under varied conditions in
many different species.
The absence of spinal stepping in monkeys
(cf. opening section) clearly must reflect differences in motor control between primates
and other tetrapods. This, in turn, probably
reflects anatomical differences in descending
pathways (cf. Kuypers, 1973) as well as in
intrinsic connections. From a functional
standpoint it is reasonable to infer (in accord
with Eidelberg, 1981) that motor control in
primates is simply under greater supraspinal
control (and requires more supraspinal input) than in nonprimates. In addition to Eidelberg et aL’s (1981)results, there are other
data to support this view.
Spinal shock is the period immediately
after spinal injury during which there are
few spontaneous movements, and few reflexes can be elicited from the caudal portion
of the body. The amount of time spinal shock
lasts appears to increase with phylogenetic
“level,” i.e., being maximal in humans (lasting weeks) to only briefly in frogs. Similarly,
behavioral recovery following spinal cord
transection is greater in “lower” animals (cf.
Stelzner, 1982). Stelzner argued that despite
these differences, the actual intrinsic spinal
circuitry is very similar among different
classes of vertebrates. He suggested that the
absence of descending influences following a
lesion suppresses the remaining circuitry
within the isolated spinal cord, with spinal
shock being indicative of that effect. Furthermore, once present, descending connections
are necessary to fully maintain the intrinsic
functioning of the cord. Thus, if we extrapolate t o primates, it would appear that although all the basic circuitry is present in
the spinal cord of primates to produce stepping, once having become “overcome” by descending (supraspinal) influences, the intrinsic circuitry can no longer function without this influence.
Clearly, Stelzner’s (1982) hypothesis adequately explains and supports Eidelberg et
al.’s (1981) results. Similarly Haines et al.
(19751, using Tupaia and Galago as neuroanatomical models of Paleocene and Eocene pri-
GAIT CHARACTERISTICSOF SQUIRREL MONKEYS
mates, respectively, suggested primate locomotor evolution is characterized by progressive cortical control over axial and appendicular musculature. This control is brought
about through new connections being formed,
with the more primitive connections (e.g.,
spinal reflex pathways) still being maintained.
Although both Stelzner’s (1982)and Haines
et al.’s (1975)hypotheses are reasonable, they
do not explain the noted absence of trotting
in primates. That is, if spinal cord mechanisms are basically similar across vertebrates, then prior to galloping a trotting
phase should be evident. Furthermore, the
absence of trotting in the male squirrel monkey suggests that the absence of this gait in
primates is not simply the result of the use
of diagonal-sequence footfall patterns. At
present we can suggest no reason for the
absence of trotting in primates except to propose some anatomical andlor functional differences in the linkage of CPGs relative to
other tetrapods.’
Obviously, the neuronal andlor mechanical
basis of primate quadrupedalism is far from
clear. Thus, many more data from both primate and nonprimate species are necessary
to understand this perplexing aspect of primate biology.
ACKNOWLEDGMENTS
We are grateful to the Fort Wayne Children’s Zoo for loaning the monkeys; to Mr.
G. Duncan for technical assistance during
filming; to Mr. S. Stoddard-Apter for computer software; to Ms. C . Bishop for the illustrations; to Ms. E. Gankiewicz and Ms. C.M.
Hockensmith for assistance during training;
and to Ms. E. Wilson for typing the many
drafts of this manuscript.
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