Gait characteristics of two squirrel monkeys with emphasis on relationships with speed and neural control.код для вставкиСкачать
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. LITERATURE CITED Melt, Z, and Kasicki, S (1975)Limb coordination during locomotion in cats and dogs. Acta Neurobiol. Exp. 35:369-378. Ankel, F (1972) Vertebral morphology of fossil and extant primates. In R Tuttle (ed): The Functional and Evolutionary Biology of Primates. Chicago: AldineAtherton, pp. 223-240. Dagg, A1 (1977) Running, Walking and Jumping: The Science of Locomotion. London: Wykeham Publications. ’Dagg (1977)suggested another possibility. She proposed that primates do not trot because they “may have a spine that is not straight and rigid enough’’ (p. 69). No data are presented t o support this view. Furthermore, considering the rather unspecialized nature of the primate vertebral column (Ankel, 1972) and the apparent flexibility of the cat vertebral column (e.g., during galloping), Dagg’s argument does not seem valid. 443 Eidelberg, E (1981) Consequences of spinal cord lesions upon motor function, with special reference to locomotor activity. Prog. Neurobiol. 17:185-202. Eidelberg, E, Walden, JG, and Nguyen, LH (1981) Locomotor control in macaque monkeys. Brain 104:647663. Eisenstein, BL, Postillion, FG, Norgren, KS, and Wetzel, MC (1977) Kinematics of treadmill galloping by cats. II. Steady-state coordination under positive reinforcement control. Behav. Biol. 21:89-106. Elias, M (1977) Relative maturity of cebus and squirrel monkeys at birth and during infancy. Dev. Psychobiol. 10:519-528. Goslow, GE Jr, Reinking, RM, and Stuart, DG (1973) The cat step cycle: Hind limb joint angles and muscle lengths during unrestrained locomotion. J. Morphol. 141:l-42. Gray, J (1944) Studies in the mechanics of the tetrapod skeleton. J. Exp. Biol. 20:88-116. Grillner, S (1981) Control of locomotion in bipeds, tetrapods, and Ash. In VB Brooks (ed): Handbook of Physiology Sect. 1: The Motor System Vol. I 1 Motor Control, Part 2. Bethesda: Am. Physiological Society, pp. 11791236. Haines, DE, Goode, GE, Albright, BC, and Murray, HM (1975)Some neuroanatomical aspects of primate locomotor evolution. J. Hum. Evol. 4~103-111. Halbertsma, JM (1983) The stride cycle of the cat: The modelling of locomotion by computerized analysis of automatic recordings. Acta Physiol. Scand. [Suppl.] 521: 1-75. Heglund, NC, Taylor, CR, and McMahon, TA (1974)Scaling stride frequency and gait to animal size: Mice to horses. Science I86:1112-1113. Hildebrand, M (1966) Analysis of the symmetrical gaits of tetrapods. Folia Biotheoretica 6:9-22. Hildebrand, M (1967) Symmetrical gaits of primates. Am. J. Phys. Anthropol. 26:119-130. Hildebrand, M (1977)Analysis of asymmetrical gaits. J. Mammal. 58:131-156. Hill, WCO (1960) Primates: Comparative anatomy and taxonomy. Vol. IV,Part A Cebidae. Edinburgh Edinburgh University Press. Kimura, T,Okada, M, and Ishida, H (1979) Kinesiological characteristics of primate walking: Its significance in human walking. In ME Morbeck, H Preuschoft, and N Gomberg (eds): Environment, Behavior and Morphology: Dynamic Interactions in Primates. New York Gustav Fischer, pp. 297-311. Kleinbaum, DG and Kupper, LL (1978) Applied Regression Analysis and other Multivariable Methods. Scituate, MA: Duxbury. Kuypers, HGJM (1973) The anatomical organization of the descending pathways and their contribution to motor control especially in primates. In JE Desmedt (ed): New Developments in Electromyography and Clinical Neurophysiology. Vol. 3. Basel: Karger, pp. 38-68. Napier, JR,and Napier, PH (1967)A Handbook of Living Primates. New York: Academic. Norgren, KS, Seelhorst, E, and Wetzel, MC (1977)Kinematics of treadmill galloping by cats. I. Steady state coordination under aversive control. Behav. Biol. 2m-88. Prost, JH (1965) The methodology of gait analysis and gaits of monkeys. Am. J. Phys. Anthropol. 23:215-240. prost, JH (1969) a replication study on monkey gaits. Am, J. phys, ~ ~ ~30:2~~-208. h ~ ~ ~ ~ l fiost, JH,and Sussman, Rw (lg69) Monkey locomotion on inclined surfaces. Am. J. Phys. Anthropol. 31.5358. . 444 J.A. VILENSKY AND M.C. PATRICK Rollinson, J, and Martin, RD (1981) Comparative aspects of primate locomotion, with special reference to arboreal cercopithecines. Symp. Zool. SOC. Lond. No. 48, pp. 377-427. Rose, MD (1977) Positional behavior of olive baboons Papi0 anubis) and its relationship to maintenance and social activities. Primates 1859-116. Stelzner, D J (1982) The role of descending systems in maintaining intrinsic spinal function: A developmental approach. In B Sjolund and A Bjorklund (eds): Brain Stem Control of Spinal Mechanisms. New York: Elsevier, pp. 297-321. Vilensky, JA (1979a) Masses, centers-of-gravity,and moments-of-inertia of the body segments of the rhesus monkey (Macaca mulatta). Am. J. Phys. Anthropol. 5057-66. Vilensky, JA (197913) A Biomechanical Analysis of Rhesus Monkey (Macaca mulatta) Locomotion. Ph.D. thesis, University of Wisconsin, Madison. Vilensky, JA (1980) Trot-galloptransition in a macaque. Am. J. Phys. Anthropol. 53347-348. Vilensky, JA (1983) Gait characteristics of two macaques, with emphasis on relationships with speed. Am. J. Phys. Anthropol. 61.255-265. Vilensky, JA and Gehlsen, G (1984) Temporal gait parameters in humans and quadrupeds: How do they change with speed? J. Hum. Movement Studies 10:175188. Vilensky, JA, and Patrick, MC (1984) Inter and intratrial variation in cat locomotor behavior. Physiol. Behav. 3S733-743. Wells JP (1974) Positional behavior of Cercopithecus aethiops sabueus (the green monkey): A functional biomechanical analysis. Ph.D. thesis, University of Massachusetts, Amherst. Wetzel, MC, Anderson, RC, Brady, TH, Jr, and Norgren, KS (1977) Kinematics of treadmill galloping by cats. III. Coordination during gait conversions and implications for neural control. Behav. Biol. 21:107-127. Wetzel, MC, and Stuart, DG (1976) Ensemble characteristics of cat locomotion. h o g . Neurobiol. 7:1-98.