Stabilization and mobility of the head and trunk in vervet monkeys (Cercopithecus aethiops) during treadmill walks and gallops
Department of Anatomy and Caribbean Primate Research Center, School of Medicine, University of Puerto Rico, PO Box 365067, San Juan, PR 00936-5067, USA
e-mail: ddunbar{at}rcm.upr.edu
Accepted 15 September 2004
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Summary |
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Key words: spatial reference frames, pitch, yaw, roll, gaze, visual input, optic flow, blinks, vestibular input, proprioception, sensory reweighting, quadrupedal locomotion
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Introduction |
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Previous studies of natural locomotion on the ground and flat surfaces by
monkeys (Macaca radiata and Semnopithecus entellus) in the
wild (Dunbar and Badam, 1998;
Dunbar et al., 2004
) and under
semi-natural conditions (Macaca mulatta)
(Dunbar and Badam, 1998
)
reveal that movement patterns of the head and trunk differ between gaits.
During quadrupedal walks, which are characterized by a symmetrical footfall
pattern, the trunk rotates through 10° or less in the pitch or sagittal
plane. The head, however, is free to rotate in the pitch (>20°) and yaw
or transverse (up to 180°) planes during quadrupedal walks without any
apparent disturbance to balance or spatial orientation. By contrast, the
relative degree of segmental mobility reverses during quadrupedal gallops, a
gait that incorporates an asymmetrical footfall pattern and an airborne phase.
The trunk experiences large pitch rotations of up to 50°. The head,
however, experiences only small rotations (<20°) in the pitch plane and
minimal rotations in any other plane. Thus, using 20° as a threshold angle
(for rationale, see Dunbar et al.,
2004
), the head rotates on a stabilized trunk during walks, but
the trunk effectively rotates on a stabilized head during gallops.
The above findings were interpreted to indicate that the nervous system
requires either the head or the trunk to be rotationally stabilized to provide
a reference frame for determining body orientation relative to space (e.g.
gravity vertical or gravitoinertial acceleration vector). During
gallops, a stabilized head in a face-forward, downwardly pitched orientation
that aligns the horizontal semicircular canals near earth-horizontal allows
the eyes and vestibular apparatus to provide the brain with redundant
reference frames for gaze (Berthoz and
Pozzo, 1988; Clément et
al., 1988
; Grossman et al.,
1988
; Owen and Lee,
1986
; Pozzo et al.,
1990
), and spatial orientation and heading
(Gdowski and McCrea, 1999
;
Mayne, 1974
;
Pozzo et al., 1990
). Evidence
continues to accumulate that the vestibular apparatus functions as an inertial
navigational system (Berthoz and Pozzo,
1994
; Dunbar et al.,
2004
; Mayne, 1974
;
Pozzo et al., 1990
) within the
stable platform of the head (Pozzo et al.,
1990
), and is sensitive to the gravitoinertial acceleration
vector (Imai et al., 2001
).
Together, these visual and vestibular cues can also determine locomotor
velocity (speed of approach) and acceleration
(Bertin et al., 2000
;
Prokop et al., 1997
;
Telford et al., 1995
;
Varraine et al., 2002
). During
walks, by contrast, a stabilized trunk can provide information about spatial
orientation by combining signals from the vestibular apparatus and neck
proprioceptors (Mergner et al.,
1983
,
1991
,
1992
), and from proprioceptors
(Jacobs et al., 1985; Mittelstaedt,
1988
; Taylor and McCloskey,
1990
) and nonproprioceptive receptors (Mittelstaedt,
1995
,
1996
,
1997
;
Vaitl et al., 1997
) in the
trunk itself.
Visual, vestibular and somatosensory inputs are also important for
eliciting body sway when necessary to correct posture
(Allum, 1983;
Berthoz et al., 1979
;
Bronstein, 1986
;
Day et al., 1997
;
Jeka et al., 1997
;
Kavounoudias et al., 1999
;
Lackner and DiZio, 1993
;
Lee and Lishman, 1975
;
Lestienne et al., 1977
;
Nashner and Wolfson, 1974
),
and to initiate neuromuscular activity during free-fall or at the appropriate
time before touchdown to prepare the limb for absorbing the force of impact
and supporting the body against the effects of gravity
(Dietz and Noth, 1978
;
Dufek and Bates, 1990
;
Engberg and Lundberg, 1969
;
Greenwood and Hopkins, 1976
;
Lacour and Xerri, 1980
;
Liebermann and Goodman, 1991
;
McKinley and Pedotti, 1992
;
McKinley and Smith, 1983
;
Melvill Jones and Watt,
1971a
,b
;
Santello and McDonagh, 1998
;
Santello et al., 2001
;
Vidal et al., 1979
;
Watt, 1976
). The relative
contributions of the different sensory inputs can change or become
`re-weighted', however, depending upon the environmental conditions. In a
posture control study, Peterka
(2002
) found that
proprioceptive inputs concerning the support surface dominate when subjects
correct for small perturbations without vision. As the size of the postural
disturbance increases, however, the gain for gravity-related (vestibular)
feedback increases while the gain for surface-related (proprioceptive)
feedback decreases.
Even under natural conditions, all sources of sensory information are not
constantly available. Visual input in particular is normally interrupted,
albeit briefly, by blinks. These rapid and stereotyped eyelid movements serve
to protect the cornea (Porter et al.,
1993). Whether blinks occur only intermittently in response to
corneal irritation or also at specific times during eye or head movements is
unclear. The latter case would suggest that blinks serve an additional role in
filtering visual input.
The nervous system's ability to interpret correctly sensory information on
spatial orientation, balance, locomotor velocity, correct limb placement and
antigravitational support has evolved in the context of the animal moving
relative to its environment (e.g. overground). The issue then arises as to
whether a stabilized segment is necessary for interpreting this information
when the body remains stationary relative to its surroundings (i.e. in-place).
One major difference between these two conditions concerns visual and
vestibular input, especially the presence or absence of optic flow and otolith
stimulation, respectively. This present study, therefore, addresses the
following two questions: (1) are head and trunk movements during treadmill
locomotion the same as, or different from, those movements occurring during
overground locomotion? (2) During head movements, do blinks occur at
particular times and, if so, when? The African vervet monkey
(Cercopithecus aethiops L. 1758), which has been studied
previously in captivity during overground
(Hurov, 1985;
Larson and Stern, 1989
),
wooden beam (Strait and Ross,
1999
), treadmill (Vilensky and Gankiewicz,
1990a
,b
;
Vilensky et al., 1990
), and
jump-down (Dyhre-Poulsen and Laursen, 1984;
Laursen et al., 1978
)
locomotion, will be the investigated species. I hypothesize that (1) head and
trunk rotations during treadmill walks and gallops will be comparable to the
rotations reported for overground locomotion
(Dunbar et al., 2004
), and (2)
blinks that do occur will be associated with rapid head movements.
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Materials and methods |
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The cine camera (Redlake, San Diego, CA, USA) was mounted on a tripod and
recorded the treadmill gaits from lateral view at a 100 Hz (frames
s1) filming rate. Both the cine camera and treadmill were
leveled before filming, aligning the filmed image of the treadmill belt
surface with earth horizontal. A digital speedometer mounted on the treadmill
and within the field-of-view of the camera lens indicated instantaneous belt
speeds. A total of 10 walk cycles (3 cycles from monkey 1; 3 cycles from
monkey 2; 4 cycles from monkey 3) and 10 gallop cycles (4 cycles from monkey
1, 3 cycles from monkey 2; 3 cycles from monkey 3) were extracted for
quantitative analysis of pitch plane movements. For inclusion in this sample,
head and trunk orientation and movements had to remain in approximately the
same (pitch) plane and perpendicular to the camera lens. This perspective
minimized parallax measurement error and allowed meaningful comparisons with
overground gait cycles in the wild (Dunbar
et al., 2004). In addition, a total of 60 (20 cycles/monkey) walk
cycles and 60 (20 cycles/monkey) gallop cycles, which were separate from the
cycles for quantitative analysis above, were analyzed for yaw and roll
rotations and orientations of the head. Blinks (down-phase and up-phase of the
eyelid combined) were also analyzed during these head yaw rotation cycles, as
well as during 12 performances of one walking monkey turning around on the
treadmill in response to reversals in belt direction (referred to in this
study as `turn-arounds'). The pale eyelids and dark eyes of this species made
it possible to determine when blinks occurred.
Analysis followed previously described procedures
(Dunbar et al., 2004).
Briefly, a three-axis (pitch, yaw, roll) coordinate system defined rotations
in the sagittal (pitch), transverse (yaw) and coronal (roll) planes,
respectively. Each cycle was analyzed frame by frame with a digitizer
(Numonics Corp., Montgomeryville, PA, USA) and computer. Head and trunk
pitch-plane rotations were measured (SigmaScan, SPSS Inc., Chicago, IL, USA)
quantitatively relative to earth-horizontal, using the treadmill belt surface
as the reference. The head axis passed through the ear (external auditory
meatus) and the tip of the mouth, with the ear serving as the apex for head
angle (Fig. 1). The trunk axis
passed through the hip and shoulder joints, with the hip serving as the apex
for trunk angle. Head-to-trunk angles were then calculated from these
head-in-space and trunk-in-space measurements. The head or trunk was
considered to be rotationally stabilized when pitch displacements were 20°
or less (for rationale, see Dunbar et al.,
2004
). The pitch displacement data were used to derive angular
velocities. At each processing step, data were smoothed with engineering
software (MATLAB, The Math Works, Inc., Natick, MA, USA), using a low-pass
filter cut-off frequency of 10 Hz to minimize measurement error. The mean
position or orientation of the head and trunk relative to earth horizontal
were calculated from the maximum and minimum positional values measured
throughout each cycle. A negative value indicated that the head axis (mouth
down) or trunk axis (shoulders down) was tilted downward below earth
horizontal (0°). The orientation of the horizontal semicircular canals
relative to space, unknown in vervets, was estimated by adjusting the mean
head positional angles by +40°, a corrective value that was derived from
other monkey species (for rationale, see
Dunbar et al., 2004
).
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The following quasi-quantitative observational system classified head yaw rotations: head facing forward = 0°, head facing laterally into or directly away from camera lens = 90°, head facing backwards over shoulder = approaching 180°, head facing halfway between forward and laterally = 45°, and head facing halfway between laterally and backwards over shoulder = 135°. Measurements of blink duration were based on the number of elapsed cine film frames.
Quantitative variables were compared between gaits with Student's
t-test. To determine what mean percentage of head-to-trunk angular
displacements were contributed by changes in head-to-space angle versus
trunk-to-space angle, the following procedure was used
(Dunbar et al., 2004).
Pearson's product moment correlation coefficients were obtained for
head-to-space and trunk-to-space angles against head-to-trunk angles for each
cycle, and the mean percentage of variance was calculated from the means of
the z-transformed correlations. For each cycle, a test of homogeneity
(Sokal and Rohlf, 1981
) was
used to compare the correlation coefficients, and to reveal if head and trunk
positions were significantly different determinants of head-to trunk angle.
Finally, joint probabilities for each comparison were calculated to determine
the significance of the differences in the mean percentage of head-to-trunk
angle that were explained by head-to-space angle versus trunk-to-space angle.
For all statistical tests, P-values less than or equal to 0.05 were
considered significant.
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Results |
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Treadmill walks
The vervet monkeys usually walked with a diagonal sequence pattern (i.e.
hind limb followed by opposite forelimb)
(Fig. 2A), although lateral
sequence patterns (i.e. hind limb followed by ipsilateral forelimb) also
occurred. Head angular motions occurred in the yaw and pitch planes. Yaw-plane
rotations were usually 45° and 90° as the monkeys looked toward or
directly into the camera lens, but in 13 episodes lasting 1 to 3 cycles these
rotations approached 180° as they looked over the shoulder at the trainer
standing behind the treadmill. The latter head rotations included a noticeable
roll component as the monkeys looked backward and upward.
|
Blink activity varied depending upon the degree and direction of head yaw rotation. Blinks did not occur when the head turned up to 90° backwards (from anterior to posterior) or forwards (from posterior to anterior). Blinks also did not occur when the head rotated backwards to nearly 180°. By contrast, in 4 out of 7 behavioral episodes when the head rotated forwards rapidly and without delay back into the pitch plane, a blink of approximately 50 ms in duration occurred beginning at 90° and ending at 45°. Furthermore, in 6 out of 12 sequences during which one of the monkeys performed a turn-around, a 50 ms blink also occurred at comparable angles during forward head turns. In 7 of the 9 remaining episodes (head rotation only + turn-arounds) in which the eyes did not blink on the forward return, the head stopped momentarily at 90° before completing its forward rotation.
The mean ranges of pitch rotations from the quantitative sample
(Table 1) reveal that, although
both the head and trunk were usually stabilized (<20°) during walks,
the head rotated significantly more than trunk (Figs
3A,
4A). Head-to-trunk angles were
more highly correlated with head-to-space angles
(r2=81.92%) than with trunk-to space angles
(r2=14.05%), verifying this head-on-trunk rotational
pattern. All combined probabilities (Sokal
and Rohlf, 1981) were significantly different at the 0.01 level.
The head, however, was commonly observed to pitch through a much larger range
32° in one cycle as the monkeys looked overhead or down at
the treadmill belt. By contrast, the trunk remained rotationally stabilized in
all planes. Paralleling the displacement values above, mean and maximal pitch
velocities were much larger for the head than the trunk during walks, and
head-to-trunk pitch velocities were closer to those of the head than the trunk
(Fig. 4C,E,G).
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|
Whereas mean trunk position was closer to earth horizontal
(Fig. 3D), mean head position
was pitched downward (31°) (Fig.
3C). When this value is adjusted by +40° (see Materials and
methods), the predicted orientation of the horizontal semicircular canals
would be 9° above earth horizontal (upward tilt rostrally). The monkeys,
however, commonly fixed gaze on objects immediately above the treadmill or on
the treadmill belt immediately before them, requiring the head be held in
positions of upward (e.g. 30°) or downward (e.g.
90°)
pitch, respectively. These head positions moved the horizontal semicircular
canals into more vertical orientations relative to space. The head was also
commonly rotated and held in a position of yaw (
90°) to fix gaze on
the cine camera located to one side (Fig.
2A), and in a combined position of yaw (approaching 180°) and
roll in order to fix gaze on the trainer standing behind the treadmill.
Treadmill gallops
The vervet monkeys galloped with either a transverse (i.e. leading hind
limb followed by contralateral forelimb) or rotary (i.e. leading hind limb
followed by ipsilateral forelimb) pattern
(Fig. 2B,C). As during walks,
head rotations were most commonly at 45° and 90°, but in 7 episodes,
which also lasted 13 cycles, these rotations approached 180° to
look over the shoulder (Fig.
2C). Blink activity also corresponded to that during walks and
turn-arounds, but was even more consistent. In 6 out of 7 cycles in which one
of the monkeys looked backwards over its shoulder, no blink occurred when the
head turned from forwards to backwards, but a 50 ms blink occurred beginning
at 90° and ending at 45° when it turned from backwards to forwards.
During the one cycle in which the blink did not occur, the head stopped
turning momentarily at 90° to fix gaze on the camera lens before
completing the forward rotation, as was observed during walks and
turn-arounds.
In the quantitative sample in which the head remained in the pitch plane
(Table 1), pitch rotations of
the trunk relative to space during gallops were much larger than during walks,
but mean head pitch rotations relative to space were equivalent (Figs
3A,
4B). Head-to-trunk pitch
rotations were closer to those of the trunk relative to space than to the head
relative to space, and significantly larger than during walks. Head-to-trunk
angles were more highly correlated with trunk-to-space angles
(r2=78.39%) than with head-to space angles
(r2=20.99%). Thus, in contrast to walks, when the head was
restricted to the pitch plane, the trunk effectively rotated on the head. All
combined probabilities (Sokal and Rohlf,
1981) were significantly different at the 0.01 level. The relative
magnitudes of the segmental velocities, once again, paralleled those of the
displacement data above (Fig.
4D,F,H). Both mean and maximal pitch velocities of the trunk
relative to space were greater than those of the head, and greater than during
walks. These velocities for the head relative to the trunk were closer to
those of the trunk relative to space and also greater than during walks. The
mean and maximal pitch velocities for the head, however, were comparable to
those during walks.
There were notable exceptions to the mean pitch rotational pattern of treadmill gallops described above. Head rotations of more than 20° occurred in the pitch plane, even though trunk rotations were also more than 20° (Figs 3A, 5A). These pitch excursions, however, were of a much smaller magnitude than those in the yaw plane, falling near the stabilization threshold defined in this study. Specifically, with increases in head pitch rotation of more than just a few degrees beyond 20°, trunk pitch rotations diminished. For example, cycles with head pitch rotations of 21° and 22° had trunk pitch ranges of 30° and 27°, respectively (Fig. 5A). By contrast, a cycle with a head pitch rotation of 28° had a trunk pitch rotation of only 17° (Fig. 5B). The latter gallop cycle is distinctive in that it presented a walk-like rotational pattern consisting of a head rotating on a stabilized trunk and this walk-like pattern extended to the velocity profiles (Fig. 5D,F,H).
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Mean trunk position during treadmill gallops was at a slightly, but significantly, steeper pitch angle to earth horizontal than during walks (Fig. 3D). Mean head position relative to space, however, was comparable to the position during walks (Fig. 3C). In this position, the horizontal semicircular canals would be tilted upward rostrally at approximately 6° above earth horizontal. As described above for walks, however, the head was frequently held in positions requiring large rotations in the pitch, yaw and roll planes.
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Discussion |
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Regarding proportions, relative differences in forelimb to hind limb
lengths between vervets and the other two species could be considered a
potential source of variation in head and trunk displacements during treadmill
versus overground locomotion. To determine the feasibility of this
possibility, measurements of limb segment lengths from the cine films of
representative vervet, bonnet and hanuman individuals were used to approximate
the osteometric intermembral index (humerus + radius length / femur + tibia
length x 100). The resultant indices were 86 for the vervet, 91 for the
bonnet macaque and 83 for the hanuman langur, which fall within the respective
generic index ranges for Cercopithecus (7991), Macaca
(8395) and Presbytis (7384), the former generic
classification of hanuman langurs (Napier
and Napier, 1967). The values indicate that vervets, like hanuman
langurs, have longer hind limbs than forelimbs, suggesting that these
proportions may underlie differences between vervet and bonnet macaque head
and trunk displacements. The proportional differences among all three species
are relatively small compared to those of several other primate species
(Napier and Napier, 1967
),
however and the functional significance of an index that does not consider
foot and hand length, segmental orientation, or soft tissues is doubtful. Much
more likely influences on head and trunk displacements are segmental
orientation, range and coordination of joint rotations, associated
musculotendinous forces and duration of limb contact with the support surface.
Thus, while the reader should be aware that the comparisons between treadmill
and overground locomotion involve different species, the combined evidence
presented above supports a strong likelihood that the fundamental head and
trunk movement patterns of vervet monkeys would be similar to the patterns
found in bonnet macaques and hanuman langurs. The finding that vervet monkeys
can walk and gallop on a treadmill with head and trunk movements that
are comparable to those used by bonnet macaques and hanuman langurs during
overground locomotion (Dunbar et al.,
2004
), only strengthens this likelihood.
Comparison of head and trunk rotations during treadmill versus overground locomotion
Hypothesis 1, which stated that head and trunk rotations during treadmill
walks and gallops will be comparable to the rotations reported for overground
locomotion (Dunbar et al.,
2004), is supported only in part. Treadmill and overground walks
are comparable in that the head commonly rotates in the pitch and yaw planes
on a stabilized trunk. By contrast, treadmill gallops are not always
comparable to overground gallops, in that the head can rotate through several
degrees in the pitch and yaw planes as the trunk rotates simultaneously
through several degrees in the pitch plane. Thus, unlike during overground
gallops (Dunbar et al., 2004
),
the head is not required to be rotationally stabilized. Furthermore, treadmill
and overground locomotion differ in that maximal instantaneous head pitch
velocities occasionally exceed 350° s1 during treadmill
walks (Fig. 4C) and gallops
(Fig. 5D), the threshold
velocity above which, at least in humans
(Pulaski et al., 1981
), the
vestibulo-ocular reflex (VOR) saturates and visual input is disrupted. The
duration of these high velocities is brief, however, falling within the period
of blinks observed in this study and reported for other monkey
(Macaca) species (Baker et al.,
2002
; Porter et al.,
1993
). Other studies comparing treadmill and overground locomotion
in humans and quadrupeds also reveal differences, though less dramatic, in
angular and linear displacements (Alton et
al., 1998
; Barrey et al.,
1993
; Nigg et al.,
1995
; Stolz et al., 1997; Vogt
et al., 2002
), as well as in temporal characteristics (e.g.,
Alton et al., 1998
;
Barrey et al., 1993
;
Buchner et al., 1994
;
Nelson et al., 1972
;
Stolze et al., 1997
;
Wetzel and Stuart, 1976
;
Wetzel et al., 1975
) and
generated forces (White et al.,
1998
).
Simultaneous pitchplane rotations of the head and trunk in excess of
20°, however, only occur when the rotation of head is slightly greater
than 20° (Fig. 5A). When
head pitch rotations become larger, the range of trunk pitch rotation drops
below 20° (Fig. 5B). This
inverse relationship between magnitude of head and trunk pitch excursions most
likely indicates osteoligamentous constraints on motion between the head, neck
and trunk in this plane (Dunbar et al.,
2004; Graf et al.,
1995
). Alternatively, trunk rotations may drop below 20° in
order for it to provide a stable reference frame, as hypothesized for
overground locomotion (Dunbar et al.,
2004
). This latter possibility seems unlikely, however, because
head rotations in the yaw plane commonly far exceed 20° at even the
largest trunk excursions and the head is often held in that rotated position.
If truly detrimental to overground gallops
(Dunbar et al., 2004
), how can
the head and trunk rotate simultaneously during treadmill gallops without
disrupting balance and orientation?
Environmental factors, reference frames, sensorimotor tasks and sensory re-weighting
The environmental differences between treadmill and overground locomotion
have a profound impact on visual and vestibular inputs, with the number of
potential reference frames increasing and sensorimotor tasks decreasing under
treadmill conditions. In contrast to overground locomotion, the treadmill
monkeys are stationary relative to their surroundings. Thus, the fixed
physical surroundings under these artificial conditions provide an external
(extracorporal) spatial reference frame
(Clément et al., 1988;
Owen and Lee, 1986
) that
allows the head (and vestibular apparatus) to rotate through several degrees
during gallops without inducing disorientation. Other potential reference
frames on the treadmill include belt orientation, which largely determines
heading, and sounds and mechanical vibrations during operation, which provide
auditory (Goldring et al.,
1996
; Goossens and Van Opstal,
1999
; see Blauert,
1996
for review) and proprioceptive
(Lackner, 1988
) information,
respectively. The treadmill, however, is not unique in possessing these latter
two sensory cues. While less regular and directionally specific than on the
treadmill, notable auditory and vibrational cues are nevertheless also a
component of natural environments. The comparative data on overground
locomotion (Dunbar et al.,
2004
) was collected in village (bonnet macaque) and urban (hanuman
langur) habitats in which heavy road traffic and industrial machinery produced
ongoing cacophonous sounds near, and vibrations within, many of the locomotor
pathways. Furthermore, vibrations can provide an unreliable reference frame.
Tonic vibration reflexes in skeletal muscles that result from abnormally high
muscle spindle stimulation will induce an illusory sense of motion in a
stabilized (e.g. support phase) limb that resists the reflex contraction
(Goodwin et al., 1972
;
Lackner, 1984
,
1988
). Thus, if vervet monkeys
require a reference frame not available during overground locomotion to rotate
the head during treadmill gallops, the most likely candidate is the fixed
visual surround.
The number of sensorimotor tasks that must be accomplished for successful
locomotion is reduced on the treadmill. Whereas balance must be maintained
during both overground and treadmill locomotion, the tasks of integrating
visual information with vestibular and proprioceptive inputs to propel the
body and maintain a desired trajectory
(Bertin and Berthoz, 2004;
Dietz, 1992
;
Grillner, 1981
;
Schubert et al., 2003
) are
minimized. The need to inspect the surface for obstacles and proper hand and
foot placement, which are primarily visual tasks
(Patla and Vickers, 1997
;
Patla et al., 1991
;
Sherk and Fowler, 2001
), is
reduced because the unnatural smoothness and regularity of the treadmill belt
surface exceeds that of flat surfaces available for overground locomotion,
such as the ground and wall-tops used by the bonnet macaques and hanuman
langurs (Dunbar et al., 2004
).
The trunk can also rotate through fewer degrees while still enabling the hands
and feet to clear the belt surface safely. For example, although galloping at
higher speeds on the treadmill, vervet mean trunk displacements were less than
those of the bonnet macaque on the ground
(Dunbar et al., 2004
) and the
fastest vervet treadmill gallop cycle sampled (3.03 m s1)
had the smallest measured trunk-to-space rotation (17°). In addition, the
need is reduced to constantly monitor visual, vestibular and proprioceptive
inputs to properly adjust the timing of anticipatory extensor muscle activity
in the limbs to accommodate changes in ground elevation, adequately absorb
ground reaction forces at contact (braking) and prevent unwanted joint flexion
due to gravitational force (Dietz and
Noth, 1978
; Dufek and Bates,
1990
; Greenwood and Hopkins,
1976
; Liebermann and Goodman,
1991
; McKinley and Smith,
1983
; Melvill Jones and Watt,
1971a
,b
;
Santello et al., 2001
;
Watt, 1976
). Because the belt
surface is so dependably flat and the sensorimotor tasks of accommodating
surface changes are so reduced, overall limb movements during treadmill
locomotion could be largely determined by efference copy
(von Holst, 1954
;
von Holst and Mittelstaedt,
1950
; see Desmurget and
Grafton, 2000
; Wolpert,
1997
; Wolpert and Ghahramani,
2000
for reviews).
Treadmill locomotion nevertheless creates an incongruity between the
different sensory inputs. Visual and vestibular information indicate that the
body is stationary, but proprioceptive information from the limbs cycling on
the belt indicates that the body is moving forward. This informational
conflict is most likely overcome through a re-weighting (change in relative
importance) of visual and vestibular information on the one hand and the
proprioceptive information on the other, as is known to occur during dynamic
posture control (Peterka,
2002). Specifically, the brain can depend upon proprioceptive
inputs and use the consistently smooth and regular treadmill belt surface as
the spatial reference frame. Thus, the head can rotate in the pitch and yaw
planes without disturbing balance and spatial orientation because the visual
or vestibular inputs are not providing the critical reference frames. If this
sensory re-weighting develops gradually during the period when the monkeys
learn to gallop on the treadmill, it could be considered a training
effect.
Blinks and optic flow
Hypothesis 2, which stated that those blinks that do occur during treadmill
locomotion would be associated with rapid head movements, was supported by the
results. The monkeys blink during head yaw rotations in both treadmill walks
and gallops. Blinks temporarily eliminate optic flow input, the presence of
which in humans is known to have an impact on postural maintenance
(Bronstein and Buckwell, 1997;
Dietz et al., 1994
;
Gielen and van Asten, 1990
;
Stoffregen, 1985
;
Wolsley et al., 1996
) and
locomotor heading (Bardy et al.,
1996
; Pailhous et al.,
1990
; Patla and Vickers,
2003
; Prokop et al.,
1997
; Schubert et al.,
2003
; Warren and Kay,
1997
; Warren et al.,
2001
). Changes in optic flow rate induced by head and eye
rotations elicit lateral body sway, especially when optic flow is artificially
increased by 24 times the normally experienced flow rate to create an
incongruity with somatosensory inputs
(Schubert et al., 2003
). The
50 ms monkey blinks found in this study occur between 90° and 45° of
forward head rotation, the range through which optic flow would be most rapid
and laminar. Removing optic flow input during this brief time period would
therefore avoid the greatest potential for inducing detrimental lateral body
sway. The blinks, which are rapid for monkeys
(Baker et al., 2002
;
Porter et al., 1993
), are most
likely reflexes that are triggered by head or eye movements or some other
stimulus and that have evolved to accommodate large, forwardly-directed gaze
shifts during overground locomotion when the increase in optic flow rate is of
significant magnitude. If and when these blinks occur during overground
locomotion, however, is unknown.
The results of this study reveal that head and trunk kinematics during treadmill and overground locomotion can differ profoundly and that these differences are associated primarily with the presence or absence, respectively, of large head movements during gallops. This comparison not only provides insights into the contributions of vision and other sensory inputs to locomotion, but also demonstrates the value of combining information from the field and laboratory to increase our understanding of biological phenomena.
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