Stabilization and mobility of the head and trunk in wild monkeys during terrestrial and flat-surface walks and gallops
1 Department of Anatomy and Caribbean Primate Research Center, University of
Puerto Rico Medical School, PO Box 365067, San Juan, PR 00936-5067,
USA
2 Department of Archaeology, Deccan College Post-graduate and Research
Institute, Pune 411006 (Maharashtra), India
3 Department of Cell Biology & Anatomy, University of Calgary, 3330
University Drive NW, Calgary, AB T2N 4N1, Canada
4 Département STAPS, Centre Universitaire de Recherche en
Activités Physiques et Sportives (CURAPS), Université de La
Réunion, Site du Tampon, 117 rue du Général Ailleret,
97430 Le Tampon, France
* Author for correspondence (e-mail: ddunbar{at}rcm.upr.edu)
Accepted 31 December 2003
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Summary |
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Key words: natural locomotion, kinematics, segmental stabilization, sensorimotor control, spatial orientation, reference frames, graviceptors, vestibular apparatus, vestibulo-ocular reflex, inertia, free-ranging monkeys, hanuman langur, bonnet macaque, Semnopithecus entellus, Macaca radiata
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Introduction |
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Laboratory studies have produced a wealth of information on how the vestibular system works. The success of many of these studies, however, has required protocols that severely restrict the natural range of movement patterns practised by the animal and human subjects. Thus, much remains to be learned about vestibular function during natural or volitional movements, especially under real-world conditions. One major gap in this knowledge concerns the mechanical or environmental requirements of the vestibular system for perceiving and transmitting sensory information about the orientation of the body in space (i.e. relative to gravity verticalearth horizontal). Specifically, are there restrictions on how the head-fixed vestibular apparatus can be positioned or reoriented via head movements without deteriorating the nervous system's perception of spatial orientation?
Behavioural studies of humans and birds that focus on head orientation and
stabilization provide evidence that tolerable movements of the head-fixed
vestibular apparatus are restricted. During resting postures and other
activities, human head orientation pitches the horizontal semicircular canals
upwards slightly at 16° above earth horizontal
(Graf et al., 1995
). When
humans perform a variety of locomotor tasks (walking, running, hopping), both
with and without vision, the head rotates through no more than 20° in the
pitch (sagittal) plane, and the horizontal semicircular canals remain closely
aligned with earth horizontal (Pozzo et
al., 1990
). Furthermore, the head rotates through fewer degrees
than the trunk when rotating in the roll (frontal) plane to maintain single
limb stance on a narrow cylindrical beam or rocking platform, except when the
trunk rotates through less than 3°
(Pozzo et al., 1995
). Birds
stabilize the head during walking
(Erichsen et al., 1989
;
Troje and Frost, 2000
),
perching, standing (Erichsen et al.,
1989
) and flying (Brown,
1948
,
1951
,
1952
), even when trunk
orientation changes. This stabilization, controlled in large part by
vestibulocollic and optocollic reflexes (Gioanni,
1988a
,b
),
appears critical to the physiological or optical requirements of the eyes
(Dunlap and Mowrer, 1930
;
Fitzke et al., 1985
;
Friedman, 1975
;
Frost, 1978
;
Hodos and Erichsen, 1990
;
Troje and Frost, 2000
). Head
orientation in birds is also related to the control of posture, locomotion and
gaze direction (Green,
1998a
,b
;
Green et al., 1992
). This
orientation maintains the horizontal semicircular canals near earth
horizontal, being tilted upward slightly by
10° during the behaviours
discussed above (Erichsen et al.,
1989
).
Under natural conditions, however, head movements are frequently necessary,
particularly for redirecting gaze through a greater number of degrees than is
permitted of the eyes in the orbits alone. Slight pitch-plane rotations may
correct for vertical translations in order to maintain gaze on a fixed target
(Pozzo et al., 1990),
anticipatory yaw-plane rotations occur when turning a corner while walking
(Grasso et al., 1996
,
1998
) or driving a car
(Land and Lee, 1994
) and large
rotations in multiple planes are commonly practised when walking to increase
panoramic vision of the immediate surroundings. Thus, if the brain requires a
stabilized head to correctly interpret information from the vestibular
apparatus, how can large head movements occur without interfering with this
interpretation?
The above studies of head stabilization are restricted to bird flight and
to human subjects and birds performing upright bipedal or monopedal tasks.
Does head stabilization also occur in quadrupeds? If so, when and to what
degree? If not, what segmental movement patterns do occur? Quadrupedal mammals
are similar to bipeds in that the cervical column is held relatively upright
during resting postures and many voluntary activities but, during locomotion,
at least some species (cats, guinea pigs) reorient the column more
horizontally (Graf et al.,
1995; Vidal et al.,
1986
). As in birds (Erichsen
et al., 1989
), the horizontal semicircular canals in many species
are most commonly pitched up by 510° during rest, but in some
mammals, such as guinea pigs, this orientation is closer to 20°
(Graf et al., 1995
).
Furthermore, a study of natural and volitional locomotion by jackrabbits
reveals, in qualitative terms, that the head is commonly stabilized
rotationally in space (Bramble,
1989
).
Studies in the wild (Dunbar and Badam,
1998) and in captivity (Strait
and Ross, 1999
) reveal that the head in several primate species is
commonly stabilized rotationally in space during natural and volitional
quadrupedal locomotion. Preliminary evidence indicates, however, that the head
frequently rotates through several degrees in the pitch and yaw planes during
quadrupedal walks but rotates through less than 20° in the pitch plane and
only minimally in any other plane during gallops
(Dunbar and Badam, 1998
).
Thus, head movements are more restricted under some conditions than
others.
In the present paper, we further pursue the issue of potential restrictions
in orientation and movement of the vestibular apparatus in quadrupeds by
investigating, in both qualitative and quantitative terms, the kinematics of
head and trunk movements by wild, free-ranging monkeys practising volitional
locomotor behaviours in natural habitats. Two species representing different
primate subfamilies are investigated in an attempt to distinguish among those
aspects of head and trunk movement patterns that are common across gaits or
species or both. The specific question asked is how do the head and trunk
segments rotate during quadrupedal walks and gallops on the ground and flat
surfaces? Aspects of this study have been presented previously in abstract
form (Dunbar, 1998;
Dunbar and Badam, 1995
; D. C.
Dunbar, presented at satellite conference of Neuronal Control of Movement
Society, Mexico, 1977 and the 13th Symposium of International Society
for Postural and Gait Research, Paris, 1997).
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Materials and methods |
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The hanuman group lived in a large city whereas the bonnet group lived in an agricultural village. Both groups followed particular pathways through their geographic home range or territory, making it possible to predict when and where the monkeys could be found. The present study focused on walks and gallops by adults of either sex on flat and continuous surfaces along which the monkeys followed a rectilinear course; the hanumans practised these gaits on the flat top of a straight stonewall. The bonnets, by contrast, walked on the ground, following the edge of a straight irrigation ditch. Hanuman wall locomotion was compared with available ground locomotor cycles in this species in order to determine if the two substrate designs had notably different impacts on movement patterns. No clear influence on locomotor kinematics could be identified. Thus, comparisons between bonnet ground locomotion and hanuman wall locomotion were considered valid.
Data collection, definitions and variables
Cine recordings of the monkeys were made at a frequency of 100 Hz with a
tripod-mounted and levelled super-8 movie camera (Mekel Engineering, Inc.,
Covina, CA, USA) equipped with an 1170 mm video zoom lens (Canon, USA
Inc., Lake Success, NY, USA). The camera lens was oriented perpendicular to
the linear pathway to provide a lateral view and was not panned or tilted. Ten
walk and 10 gallop cycles per species were retained for further analysis. Film
sequences were chosen in which segmental and whole-body movements remained in
the same perpendicular plane, minimizing subsequent parallax measurement
error. The walk samples were collected from three hanuman (two males, one
female) and four bonnet (two males, two females) subjects, and the gallop
samples were collected from four hanuman (two males, two females) and six
bonnet (two males, four females) subjects.
Head and trunk rotations were considered in terms of a three-axis coordinate system: pitch, yaw and roll. Rotations about the pitch axis were in the sagittal (pitch) plane, rotations about the yaw axis were in the transverse (yaw) plane, and rotations about the roll axis were in the coronal (roll) plane. Filming in lateral view only allowed quantitative measurements of rotations about the pitch axis. Yaw-axis rotations were analyzed in qualitative terms using locomotor cycles that were separate from the cycles used for quantitative analysis of pitch-axis rotations. Roll-axis rotations were not included in the study because accurate analysis was unreliable.
Owing to the complexity of segmental movements and associated forces during
locomotion, no segment will be completely stabilized (0° rotation). How
much rotation can occur, however, before a segment is no longer considered
stabilized? To answer this question requires the selection of a threshold
value. Rather than make an arbitrary decision, we adopted the 20° of
pitch-plane rotation already known for human subjects
(Pozzo et al., 1990) as the
threshold value. We feel justified in extrapolating this value to monkeys
because they are closely related phylogenetically to humans and preliminary
evidence indicates that pitch-plane rotations in these species are often less
than 20° (Dunbar and Badam,
1998
). Furthermore, the neural mechanisms controlling locomotion
and posture, at least in terms of limb movements, appear to be conservative
among tetrapods in general (Dunbar et al.,
1986
; Jenkins and Goslow,
1983
; Jenkins and Weijs,
1979
; Peters and Goslow,
1983
; Vilensky and Gehlsen,
1984
).
The following body landmarks were digitized (Numonics Corp.,
Montgomeryville, PA, USA) frame by frame (10 ms sampling rate): tip of mouth,
ear (external auditory meatus), shoulder joint and hip joint. These landmarks
were used to create head (mouth apexear) and trunk (shoulder
jointhip joint) axes in order to measure (SigmaScan SPSS Inc., Chicago,
IL, USA) head and trunk rotations in the pitch plane relative to earth
horizontal throughout the locomotor sequence
(Fig. 1). Head axis-to-trunk
axis angles () were calculated from these head-to-space (
) and
trunk-to-space (ß) angles. The base of the tail was also digitized for
subsequent calculation of locomotor velocity. The raw data were then smoothed
with a 10 Hz cut-off frequency to minimize measurement error.
|
The variables of interest included pitch axis displacements and velocities of the head and trunk relative to space and of the head relative to the trunk, mean head and trunk positions (mean angle) relative to space, estimated mean position of the horizontal semicircular canals relative to space, vertical linear displacement and velocity of the head, and peak frequencies of linear and angular head displacements. Preferred locomotor velocities and cycle durations were also collected to lend context to the head and trunk variables. The 100 Hz sampling rate and objects of known size along the locomotor pathways provided time and scaling variables, respectively, for velocity calculations.
The mean position in space of the horizontal semicircular canals during
gait cycles was estimated from the mean head position values as follows.
Measurements on rhesus monkey (Blanks et
al., 1985) Macaca mulatta is closely related to
bonnets and hanuman (Spoor and
Zonneveld, 1998
) skulls reveal that the horizontal semicircular
canals are pitched upward anteriorly at 22°, on average, to the Frankfort
plane or line. This imaginary line passes through the external auditory meatus
and the inferior orbital margin. Our measurements on rhesus and hanuman skulls
further revealed that the measured head axis in both species is approximately
20° below the Frankfort horizontal plane. Combining the above information,
we estimated that the horizontal semicircular canals in both species were
pitched up by 42° from the measured head axis.
Finally, Fourier frequency analyses were conducted on both the smoothed angular and linear displacement data for the head in order to determine peak frequencies for each species during walks and gallops. Owing to constraints of the research protocol, individual locomotor performances of long enough duration for meaningful frequency analyses could not be recorded. Average frequency profiles, however, were derived for each gait type and species by performing a frequency analysis of each individual cycle and then averaging the frequency spectra across these cycles. This technique produced clear average peak frequencies. Harmonics, however, were not clearly produced and, thus, were not included in the analysis.
Statistics
Variables were compared across gaits (quadrupedal walks vs
gallops) and across species (hanumans vs bonnets) using two-way
analysis of variance. The following statistical procedure determined what mean
percentage variance in head-to-trunk angle was explained by head position and
by trunk position. Pearson's product moment correlation coefficients were
obtained for head-to-space and trunk-to-space angle against head-to-trunk
angle for each gait cycle. The mean percentage of the variance explained was
calculated from the mean of the z-transformed correlations. The
correlation coefficients for each cycle were compared using a test of
homogeneity (Sokal and Rohlf,
1981) in order to ascertain whether head or trunk positions were
significantly different determinants of head-to-trunk angle. The joint
probabilities for these individual comparisons were then calculated to
determine the significance of the difference in the mean percentage of the
head-to-trunk variance explained by head and trunk positions. In addition,
Spearman's coefficients of rank correlation were calculated to determine how
angular and vertical linear displacement of the head co-varied. Coefficients
were obtained for each trial and then z-transformed to determine the
average correlations and standard deviation by gait type and species.
P-values less than or equal to 0.05 were considered significant for
all statistical tests.
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Results |
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Qualitatively, the trunk in both species remained in an essentially fixed horizontal position during walks. Only minimal pitch, yaw and roll rotations occurred in response to the sequential limb movements. Vertical linear displacements of the head were also minimal. Head rotations, however, were variable. At times, the head would be held in a relatively static position, as when the monkeys focused gaze on the upcoming support surface and on a specific or distant target. At other times, by contrast, the head commonly rotated through several degrees about the pitch and yaw axes, as the monkeys visually scanned their physical surroundings.
When subjected to quantitative analysis, both similarities and differences between hanuman and bonnet walks emerged, as revealed in Table 1. Compared with bonnets, hanumans walked slower, but with longer cycle durations, and experienced larger head and trunk rotational displacements about the pitch axis. Nevertheless, the basic kinematic pattern was comparable in both species, in that head rotations were greater than trunk rotations (Fig. 3), and the mean pitch-plane rotational ranges of both segments were less than 20°. Note, however, that whereas these rotations were always less than 20° for the trunk in both species, head rotations often approached 25° in bonnets and 30° in hanumans (Fig. 3). Furthermore, yaw-plane head rotations, while not measured directly, often approached 180° as the hanumans and bonnets looked to the right and left (Fig. 2A).
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Vertical head translations were not significantly different between the two species during walks, although both the mean and maximal instantaneous velocities of these translations were higher in hanumans than in bonnets. Vertical head movements were not strongly correlated with rotations about the pitch axis (hanuman r2=0.16, S.D.=0.35; bonnet r2=015, S.D.=0.42). Whereas the direction of rotation at times paralleled vertical displacements (i.e. head rise with upward rotation, head drop with downward rotation), this relatively inphase pattern was interrupted with periods during which vertical translation and rotation were nearly 180° out of phase (Fig. 4A,B). Out-of-phase periods occurred primarily near touchdown of a hand when the forelimbs were also nearly 180° out of phase and one hind limb was near midsupport. The resultant whole-body deceleration, combined with decreased cranial trunk height, caused the head to pitch and drop downward. The head compensated for the downward pitch and drop, however, by rotating upward. This upward rotation, often anticipatory, peaked at or near maximal vertical descent. Occasionally, a downward compensatory head rotation also occurred near peaks in vertical ascent (Figs 2, 4). Any particular association between vertical and angular head displacements could apparently be largely overridden voluntarily, however; as when the monkeys visually inspected their surroundings (Fig. 4A).
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Pitch-plane rotations of the head relative to the trunk during walks were
larger in hanumans than in bonnets (Fig.
5). In both species, however, head-to-trunk angles were more
highly correlated with head-to-space angles (r2=0.74 for
hanuman and 0.85 for bonnets) than with trunk-to-space angles
(r2=0.33 for hanuman and 0.10 for bonnets), verifying that
the head was rotating on the trunk rather than the trunk on the head. All
combined probabilities (Sokal and Rohlf,
1981) were significantly different at the 0.001 level.
|
Mean instantaneous rotational velocities of the head about the pitch axis relative to space did not differ significantly between the species during walks. The maximal instantaneous velocities, however, were significantly higher in hanumans than in bonnets. In both species, mean instantaneous rotational velocities of the trunk relative to space were much lower than those of the head. These mean velocities were greater in hanumans than in bonnets, however, as were maximal instantaneous trunk pitch velocities. Both mean and maximal instantaneous rotational velocities of the head relative to the trunk were also greater in hanumans than in bonnets (Fig. 5), as were both mean and maximal instantaneous velocities of head vertical translations.
Mean peak (fundamental) frequencies of pitch-plane rotations and vertical displacements of the head during walks were 0.98±1.82 Hz (mean ± S.D.) and 1.95±0.32 Hz in hanumans and 1.17±1.52 Hz and 0.78±1.09 Hz in bonnets, respectively. These frequencies did not differ significantly between rotational and vertical displacements or between species.
Mean angular head position in the pitch plane relative to space during walks differed slightly between species (Fig. 6A,C). When the measured values were adjusted by +42° (see Materials and methods), the estimated mean position of the horizontal semicircular canals was pitched upward rostrally above earth horizontal by +7° in hanumans and by +4° in bonnets. Mean angular trunk position in the pitch plane relative to space revealed that the shoulder joints were lower than the hip joints (indicated by negative values in Table 1) in both species. This mean angular position was greater in hanumans, however, than in bonnets (Fig. 6B,D). By contrast, mean head-to-trunk angular position formed a significantly smaller angle in hanumans than in bonnets.
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Gallops
Gallops differ from quadrupedal walks in that limb movements are
asymmetrical (i.e. unequal timing between footfalls and handfalls), each limb
is in contact with the support surface for less than 50% of the gait cycle
time, and the cycle includes an airborne phase
(Alexander, 1982;
Hildebrand, 1977
). The
hanumans used two different types of gallops, as defined by Hildebrand
(1977
). In transverse gallops,
touchdown of the leading hind limb the second hind limb to contact the
support surface was followed by touchdown of the contralateral
forelimb. In rotary or rotatory gallops, touchdown of the leading hind limb
was followed by touchdown of the ipsilateral forelimb
(Fig. 7A). The bonnets were
observed using only the transverse gallop
(Fig. 7B).
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Qualitatively, the pattern of head and trunk movements during gallops was in marked contrast to the pattern during walks. Neither the head nor the trunk ever appeared to rotate about the roll or yaw axes (Fig. 7). The trunk, however, made large rotations about the pitch axis that were necessary for the mechanics of gallops. Specifically, in the initial portion of the gait cycle, the cranial end of the trunk raised upward to lift the forelimbs and allow the feet to completely support body weight. Subsequently, the caudal end of the trunk rose upward to lift the hind limbs, while the cranial end dropped downward to lower the forelimbs, enabling the hands to completely support body weight. Finally, near the end of the cycle, the hands lifted off the support surface to allow a brief airborne phase as the caudal end of the trunk lowered once again to bring the feet into contact with the support at the beginning of the next cycle. The head, in contrast to the trunk, rotated minimally about the pitch axis, but those rotations that did occur were usually in the same direction as the trunk. The head, however, did experience large vertical translations due to the rise and fall of the cranial end of the trunk. Near peak ascent or descent of the trunk, the head appeared to rotate downward or upward, respectively, suggesting an adjustment in head orientation.
Quantitatively, gallops differed from walks and hanuman gallops differed from bonnet gallops in several aspects (Table 1). In both species, mean gallop (diagonal and rotary combined) velocities were faster and mean cycle durations were shorter than in walks. Hanumans, however, galloped faster and with longer cycle durations than bonnets.
In both species, rotations of the trunk about the pitch axis relative to space were larger than head rotations during gallops and larger than trunk rotations during walks. Trunk rotations were larger in hanumans, however, than in bonnets (Fig. 3). The ranges of head rotation relative to space were less than 20° but slightly larger in hanumans than in bonnets. These head rotations were comparable within each species, however, to the average rotations found during walks (Fig. 3). Head rotations about the pitch axis relative to the trunk were also larger than during walks in both species and were larger in hanumans than in bonnets.
Mean vertical head translations and both mean and maximal vertical head velocities during gallops were larger than during walks in both species and were larger in hanumans than in bonnets. Vertical head movements were positively correlated with pitch-plane rotations of this segment in both species, but more strongly in bonnets (r2=0.73, S.D.=0.37) than in hanumans (r2=0.37, S.D.=0.31). This finding indicated that the direction of head rotation and vertical displacement were in phase to a greater degree in gallops than in walks (Fig. 4). Nevertheless, the direction of head rotation was at times out of phase with vertical translations. Unlike during walks, head rotations during gallops were most affected by the large pitch-plane rotations of the trunk, characteristic of this gait, and by hind limb touchdowns (Figs 4, 7). Specifically, during ascent or descent of the cranial trunk, the head made intermittent, adjusting pitch rotations in the downward or upward direction, respectively. In addition, following touchdown of the leading hind limb and prior to touchdown of the trailing forelimb, the head pitched upward with the extending trunk, as the latter segment countered the downward pitch of the body and increased stride length (Fig. 7A2,A7,B2).
Head-to-trunk angles were more highly correlated with trunk-to-space angles
(r2=0.91 for hanumans and 0.81 for bonnets) than with
head-to-space angles (r2=0.18 for hanumans and 0.28 for
bonnets), verifying that the trunk was effectively rotating on the head rather
than the head on the trunk (Fig.
8). All combined probabilities
(Sokal and Rohlf, 1981) were
significantly different at the 0.001 level.
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Mean instantaneous rotational velocities of the head about the pitch axis relative to space during gallops did not differ between species or from mean head rotational velocities during walks. Whereas the maximal head-to-space velocities also did not differ from the velocities that occurred during walks in either species, these maximal velocities were higher in hanumans than in bonnets. Mean rotational velocities of the trunk relative to space were higher in gallops than in walks for both species and were higher in hanumans than in bonnets (Fig. 8). Maximal trunk-to-space rotational velocities were also higher in gallops than in walks but did not differ significantly between species. Mean head-to-trunk rotational velocities were higher in gallops than in walks in both species, and were higher in hanumans than in bonnets. By contrast, maximal head-to-trunk rotational velocities did not differ significantly between species. In addition, whereas maximal head-to-trunk rotational velocities were greater during gallops than during walks in bonnets, these velocities did not differ significantly between gallops and walks in hanumans.
Mean peak frequencies of pitch-plane rotations and vertical displacements of the head during gallops were 1.56±0.71 Hz and 2.15±0.22 Hz for hanumans and 1.37±1.01 Hz and 1.17±0.70 Hz for bonnets, respectively. These mean peak frequencies did not differ significantly between rotational and vertical displacements, from walks or between species.
The mean head angular position in the pitch plane relative to space during gallops differed between species (Fig. 6A,C). When adjusted by +42°, the estimated mean position of the horizontal semicircular canals was pitched slightly upward rostrally above earth horizontal by +9° in hanumans and by +2° in bonnets. Mean trunk angular position relative to space was more steeply pitched (shoulders down) in hanumans than in bonnets (Fig. 6B,D). Furthermore, as during walks, the mean head-to-trunk angular position during gallops formed a smaller angle in hanumans than in bonnets. Nevertheless, during gallops, the mean angular positions of the head and the trunk relative to space, and the head relative to the trunk, were not significantly different from the mean positions during walks within each species.
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Discussion |
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Comparisons between gaits and species
Those measured variables that differ significantly between gaits
(P0.05; Table 1)
can be attributed primarily to differences in the mechanics of walks and
gallops. These variables include locomotor velocity, cycle duration and the
characteristics of trunk pitch rotation required to achieve these velocities
and durations. By contrast, those measured variables that are comparable
between gaits (P>0.05) are more likely to reflect morphological or
physiological constraints or both. These variables are associated with the
head, including mean pitch displacement, velocities and peak frequencies.
Note, however, that although the head pitch-plane rotations are comparable
on average between gaits of the measured sample, rotations greater
than 20° are commonly practised by both species during walks but not
during gallops. Furthermore, although not measured directly, head yaw-plane
rotations are also known to be frequently large during walks but minimal or
absent during gallops.
Interspecific differences in the measured variables are likely to be
attributed, in large part, to morphological and behavioural differences
between hanumans and bonnets. Hanumans are greater in size and mass than
bonnets (Roonwal and Mohnot,
1977). Furthermore, as in comparisons between langurs and macaques
in general (e.g. Napier and Napier,
1967
; Schultz,
1930
; Washburn,
1942
), the ratio of hind limb to forelimb length is greater in
hanumans than in bonnets, as reflected in the mean trunk position values
(Table 1). Behaviourally, the
two species move differently through human habitats
(Roonwal and Mohnot, 1977
; D.
C. Dunbar, personal observation). Hanumans appear confident, but aloof, and
interact minimally with people as they move through human communities. By
contrast, bonnets appear less confident but interact with and react to human
activity around them. The slower average preferred walk velocity of hanumans
reflects these differences (Table
1). Gallop behaviours also differ. Bonnets will gallop only when
necessary (e.g. to avoid danger), preferring to walk whenever possible. By
contrast, hanumans often prefer to gallop, using a slow lope at the running
walk velocities of bonnets. Furthermore, hanuman segmental movements during
gallops appear fluid and graceful, whereas bonnet movements appear rigid and
tense. Thus, differences in morphology and psychology appear to contribute to
species differences in locomotor kinematics. Some of the measured kinematic
differences, however, may become reduced at more closely matched locomotor
velocities. Nevertheless, regardless of differences due to morphology,
behaviour or locomotor velocity, head position and displacement remain
comparable across gaits in both species.
Mechanisms of segmental stabilization
Stabilization of the head or trunk or both can be attributed to the
intrinsic mechanics of the musculoskeletal system (stiffness, viscoelasticity,
joint design, segmental inertia) and the sensorimotor nervous system
(reflexive and voluntary control). Studies attempting to flesh out the
relative contributions of these variables have focused primarily on head
stabilization (Bizzi et al.,
1978; Goldberg and Peterson,
1986
; Keshner and Peterson,
1995
; Keshner et al.,
1992
,
1995
,
1999
). Kinematic and
electromyographic studies of human head stabilization reveal that the relative
contribution of mechanical versus neural mechanisms varies with the
plane and frequency of head movement
(Keshner and Peterson, 1995
;
Keshner et al., 1992
,
1995
,
1999
). For rotations in the
yaw plane, voluntary control mechanisms dominate head stabilization at lower
frequencies, whereas mechanical mechanisms dominate at higher frequencies.
Reflexes (vestibulocollic, cervicocollic) smooth the transition from voluntary
to mechanical control and damp the mechanical resonance that occurs at higher
frequencies. For rotations in the pitch plane, by contrast, reflexes are
significant at both low and high frequencies. This extended reflex role may
allow voluntary control mechanisms to focus on compensating for perturbations
or stimuli from the surrounding environment
(Keshner et al., 1995
).
The protocol of the current study allows us to consider the role of inertia
in hanuman and bonnet head stabilization during locomotion. As its resonant or
natural frequency is approached, the head's inertial properties will cause it,
for example, to rotate in the pitch plane approximately 180° out of phase
to the direction of vertical displacement under passive (e.g. minimal
neuromuscular activity) conditions. Thus, inertia effectively stabilizes the
head through compensatory rotations. Among humans, inertia is likely to play a
dominant role in head stabilization during runs and hops but much less so
during walks (Pozzo et al.,
1990,
1991
). Is inertia the primary
stabilizer of the head during hanuman and bonnet locomotion or does it play a
less important role than other mechanisms?
Inertia is predicted to become a significant factor influencing head
stabilization in cats at 5 Hz
(Peterson and Goldberg, 1981
).
Using the cat frequency as a reference point, Guitton et al.
(1986
) calculate a 24
Hz frequency range within which inertia becomes a major factor for human head
stabilization. This range was obtained by applying the following mathematical
equation, based on dimensional similarity between species
(Jones and Spells, 1963
):
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Segmental stabilization and mobility
Several muscles that traverse the head and neck, neck and trunk or both the
head and trunk can stabilize one segment in order to allow the other segment
to move effectively (Gowitzke and Milner,
1988). Owing to differences in mass between the segments, the
activity pattern of the same group of muscles will probably change, depending
upon whether the head moves on the trunk (walks) or the trunk moves on the
head (gallops). In support of this hypothesis, Horak et al.
(1994
) found for bipedal
humans that, depending upon which segment moves and which is stabilized (body
on head versus head on body), the electromyographic activity pattern
for the same muscle group changes.
Segmental stabilization and spatial reference frames
Laboratory studies provide evidence that the body depends upon different
segments (head, trunk, feet) to function as reference frames for supplying
sensory information about spatial orientation
(Berthoz, 1991;
Mayne, 1974
; Mergner et al.,
1983
,
1991
;
Nashner, 1985
; Pozzo et al.,
1990
,
1991
;
Wilson and Melvill Jones,
1979
). However, which segment provides the spatial coordinate
system during a wide range of natural postural and locomotor activities with
differing segmental trajectories and velocities is unclear. The
choice of reference frame apparently depends upon the segment being
spatially oriented and the task requiring this orientation. The hind limbs
(and forelimbs when quadrupedal), through tactile and proprioceptive inputs,
can supply information about earth horizontal during quiet stance and small
postural disturbances when physical contact with the support surface is
continuous (Berthoz, 1991
;
Nashner, 1985
). During
locomotion, by contrast, limb contact with the support surface is intermittent
and often brief. Thus, the head and trunk segments are more likely to provide
spatial reference frames during most locomotor activities.
Head mobility and stabilization
The ranges of head pitch-plane displacement during gallops by these two
monkey species correspond to the ranges found in human subjects performing a
variety of locomotor tasks (Pozzo et al.,
1990), suggesting that the head has a preferred range of movement
in the pitch plane that is restricted to 20° or less. Whereas head
rotation appears to be restricted in this or any other plane during gallops,
the same restrictions do not apply during quadrupedal walks. Head rotations
larger than 20° do occasionally occur in the pitch plane and frequently in
the yaw plane, with no apparent effect on stability. Why head excursions are
larger and more common in the yaw plane than in the pitch plane during walks
is unclear. One possibility may be related to differing osteoligamentous
constraints on motion at the atlantoaxial joint, which allows at least
180° of yaw-plane rotation, and at the atlantooccipital joint,
which restricts motion to
13° of pitch-plane rotation in monkeys. To
increase pitch-plane rotation requires flexion and extension of the entire
headneck complex at the cervicothoracic joints between the 6th cervical
and 3rd thoracic vertebrae (Graf et al.,
1995
). A second possibility is that, unlike yaw-plane rotations,
large pitch-plane rotations may stimulate unwanted sensory inputs from the
utricular maculae. Rapid changes in tilt may result in imprecise estimation of
linear motion from the maculae (Pozzo et
al., 1990
), and perhaps even trigger sensations of disequilibria
during walking. A third possibility is that in urban and rural India, dangers
(e.g. dogs, cars) usually approach in the horizontal plane, whereas dangers
from overhead (e.g. birds of prey, snakes) are infrequent and require less
vigilance.
What would be the benefit of a rotationally stabilized head? The
headneck system contains sensory receptors (vestibular, visual,
stretch) and neural pathways (vestibulocollic, vestibuloocular,
vestibulospinal) that influence muscles controlling eye, head, neck, trunk and
limb movements. Large head rotations combined with the large trunk rotations
essential for gallops may create conditions under which the brain's
interpretation of sensory information about body orientation in space would be
exceedingly complex and overly vulnerable to error. A stabilized head with the
horizontal semicircular canals closely aligned with earth horizontal, however,
can function as a reference frame or inertial guidance system by simplifying
the brain's interpretation of information provided by sensory receptors about
balance, and segmental and whole-body orientation relative to space
(Berthoz, 1991;
Mayne, 1974
; Pozzo et al.,
1990
,
1991
).
Head movements, gaze stabilization and vision
The small head rotations that do occur about the pitch axis may serve to
actively counter vertical body displacements in order to reduce the degree of
eye rotation necessary for maintaining gaze on a fixed object or point in
space (Fuchs, 1981;
Peterson et al., 1985
; Pozzo
et al., 1990
,
1991
;
Robinson, 1981
). When human
subjects focus gaze on a target while performing bipedal locomotor tasks, the
head makes compensatory movements by rotating downward when it rises
vertically, and rotating upward when it falls vertically (Pozzo et al.,
1990
,
1991
). The phase relations of
these rotational and translational movements are variable during walks but are
nearly 180° out of phase during runs. What phase relations do hanumans and
bonnets display during walks and gallops, and are these relations the same as
in humans?
Similar to human bipedal walks, the phase relation between pitch-plane rotation and vertical translation of the head during quadrupedal walks varies from being nearly in phase to being 180° out of phase. For both human and monkey walks, head rotations probably do not need to correct for vertical translations during much of the cycle because the amount of vertical displacement is small enough for corrections to be achieved by eye rotation alone. Head pitch-plane rotations and vertical translations are most often nearly 180° out of phase, however, during the two periods when the forelimbs are also nearly 180° out of phase (Figs 2, 4). At these times, when the trunk pitches downwards and the head drops the greatest distance, a rotational adjustment of the head is probably required to assist the eyes in maintaining a stable gaze.
In contrast to that seen during quadrupedal walks and during human bipedal walks and runs, pitch-plane rotations and vertical displacements of the head are largely in phase during quadrupedal gallops (Figs 4, 7). Specifically, when the head drops, it rotates downward, and vice versa. Those few correctional or adjusting counter-rotations that do occur are in response to the maximal rise and fall of the head or to specific kinematic features of quadrupedal gallops (e.g. horizontally oriented trunk experiencing large pitch rotations, asymmetrical four-limb footfall and handfall pattern, trailing hind limb touchdown, trunk extension).
The finding that head rotations are not typically 180° out of phase
during either quadrupedal walks and gallops or bipedal walks leads us to
question the importance of fine-tuned angular adjustments for gaze
stabilization and maintenance in monkeys or even humans, as suggested by Pozzo
et al. (1990). Based on the
relatively stable orientation of the head that always occurs during gallops
and is common during walks, the monkeys appear to focus gaze on so distant a
target that the change in eye-to-target angle would probably be minimal, even
when head rotation corresponds to trunk rotation. Furthermore, the human
locomotor tasks in which head pitch is most out of phase with head translation
(i.e. running and hopping) are also the two tasks in which inertial properties
of the head are most likely to dominate head stabilization
(Pozzo et al., 1990
). Thus, we
suggest that adjusting head rotations about the pitch axis are associated less
with gaze stabilization and more with maintaining vestibular pitch orientation
near earth horizontal and within the 20° threshold range.
Experiments with monkeys running in a circular path, however, reveal that
correctional head rotations compensate for trunk movements about the yaw axis,
indicating that gaze stabilization requires both eye and head nystagmous in
the horizontal plane (Solomon and Cohen,
1992). Specifically, gaze velocity is able to compensate for body
velocity, suggesting that compensatory head rotations about the yaw axis are
required to maintain gaze.
Head velocities during locomotion become relevant here because, at least
among human subjects, the vestibulo-ocular reflex (VOR) saturates at around
350 deg. s1 (Pulaski et
al., 1981). The retinal slip that occurs above this threshold
velocity results in interruptions in visual input. The VOR threshold for
monkey head movements during natural locomotion is unknown but, considering
phylogenetic closeness and experimental evidence supporting a common neuronal
organization controlling gaze and its associated reflexes in quadrupeds and
bipeds (Vidal et al., 1986
),
the thresholds may be similar. If so, then VOR saturation is not a problem for
either hanumans or bonnets because both the mean and maximal velocities of
head rotations and translations remain below 350 deg. s1
during both walks (Fig. 5) and
gallops (Fig. 8). A more
definitive statement cannot be made, however, until VOR saturation velocities
are determined experimentally for monkeys.
Trunk stabilization
During quadrupedal walks, visual inspection of the physical surroundings is
common, requiring large rotations of the head and frequent changes in gaze
direction. The potential problem for the brain to correctly interpret
vestibular information on spatial orientation while the head rotates may be
overcome by trunk stabilization, which is characteristic of this gait.
Psychophysical studies on human subjects indicate that the trunk provides a
spatial reference frame. In a series of studies investigating the
perception of head and trunk rotations and object motion in the
horizontal plane, Mergner et al.
(1983,
1991
,
1992
) demonstrate that a
stabilized trunk can provide information about body orientation relative to
space by combining vestibular information with proprioceptive information from
the neck. They also provide evidence that the central nervous system uses a
hierarchy of coordinate systems for controlling segment-to-segment and
whole-body orientation in space. Specifically, the trunk (combined vestibular
and nuchal signals), not the head, provides the reference frame for
orientation in external space, and the coordinate systems for the head (nuchal
signals) and eyes (visuo-oculomotor signals) are dependent upon the
trunk-in-space coordinate system. Proprioceptors within the human trunk are
also critical to the perception of verticality
(Jakobs et al., 1985
;
Mittelstaedt, 1988
) and
rotation of the trunk (Taylor and
McCloskey, 1990
). Furthermore, non-proprioceptive receptors
located within the trunk can provide the brain with information about trunk
posture relative to space (Mittelstaedt,
1995
,
1996
,
1997
,
1998
;
Vaitl et al., 1997
). Together,
these latter studies have revealed that the mass of the kidneys, and possibly
other organs, as well as shifts in blood mass within major vessels, function
as somatic graviceptors for position sense and for the perception of angular
velocity. The human trunk, however, experiences only small rotations during
bipedal locomotion. If and how these graviceptors provide postural information
about the trunk during quadrupedal locomotion, particularly during gallops
when the trunk experiences large pitch rotations, is unknown.
Head and trunk mean position
Mean positions of the head and trunk relative to space (earth horizontal)
and the head relative to the trunk are comparable between walks and gallops,
indicating that the head and trunk are making symmetrical pitch rotations
about these mean positions. In addition, the mean pitch position of the head
closely aligns the horizontal semicircular canals with earth horizontal. The
estimated mean position of the horizontal semicircular canals is pitched
slightly above earth horizontal rostrally in both species. This mean
horizontal canal alignment with absolute space corresponds closely to that
reported for several vertebrate species at rest
(Vidal et al., 1986) and
during voluntary movements (Graf et al.,
1995
). Furthermore, when converted to the measurement system used
in the present study, the mean head positional values of three macaque species
(M. mulatta, M. fuscata and M. fascicularis) walking on
wooden beams under zoo conditions (Strait
and Ross, 1999
) fall within the ranges of motion for hanumans and
bonnets. That the values from this zoo study do not correspond to the
mean positional values for hanumans and bonnets more likely reflects
differences in methodology than species.
Neck
The shortness of the neck in monkeys, combined with the technical
limitations of filming wild animals under natural conditions, makes accurate
kinematic analysis of this segment fall beyond the scope of the current
protocol. The neck, forming the physical link between the head and trunk and
containing essential somatosensory receptors, is nevertheless a significant
segment in the mechanics and neural control of head and trunk movements. Thus
far, head and trunk movements have been studied primarily in short-necked
primates (monkeys, humans). Details of contributions by the neck to head and
trunk movements during natural locomotion may be best revealed, however,
through investigations of long-necked species (e.g. horses, giraffes).
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