1Department of Clinical Neurosciences and Neuroscience Research Group, The University of Calgary, Calgary, Alberta T2N 2T9, Canada; and 2Balance Disorders Laboratory, Oregon Health Sciences University, Beaverton, Oregon 97006
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ABSTRACT |
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Earhart, Gammon M., G. Melvill Jones, F. B. Horak, E. W. Block, K. D. Weber, and W. A. Fletcher. Forward Versus Backward Walking: Transfer of Podokinetic Adaptation. J. Neurophysiol. 86: 1666-1670, 2001. We asked whether podokinetic adaptation to walking on a circular treadmill transfers to different forms of locomotion. Subjects were blindfolded and asked to walk straight across the floor, in the forward and backward directions, following podokinetic (PK) stimulation that consisted of 30 min of forward walking-in-place on the perimeter of a disk rotating in the clockwise direction. During both forward and backward walking following forward-walking PK stimulation, subjects involuntarily walked along curved trajectories at angular velocities well above vestibular threshold, although they perceived that they were walking along straight paths. The curved paths of forward and backward walking were indistinguishable from one another. Transfer of PK adaptations acquired during forward walking on the turntable to backward walking trials suggests that the PK system controls general locomotor trajectory. Adaptation of the system thus influences forms of locomotion other than that used during acquisition of the adaptation. This transfer also supports the concept that forward and backward walking are controlled by neural networks that share common elements. An interesting feature of the transfer of PK adaptation is that for both forward and backward walking, subjects turned in a counterclockwise direction. As such, the direction of relative rotation between the trunk and feet was maintained for both forward and backward walking. However, the relationship of the lower extremities to the center of rotation was not preserved. The left limb was the inner leg during PK stimulation and forward walking after adaptation, but the left leg was the outer leg during backward walking. These results suggest that PK adaptation affects general locomotor trajectory via a remodeling of the rotational relationship between the trunk and the feet.
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INTRODUCTION |
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Successful locomotion relies on
the ability to adjust locomotor output to meet a variety of
environmental conditions and behavioral goals. Several features of
locomotion can be changed to accommodate the multitude of situations
encountered. For example, one can change the direction of locomotion
and walk forward or backward as desired. Comparisons of forward and
backward walking suggest that kinematic profiles for forward walking
are reversed during backward walking (Grasso et al.
1998; Thorstensson 1986
). Motor patterns for
forward and backward walking support the hypothesis that backward
walking may be produced using muscle synergies similar to those of
forward walking, although the order of muscle activation within
synergies is reversed for the two directions of walking (Buford
and Smith 1990
; Winter et al. 1989
). Kinematic
and myographic evidence indicates that forward and backward walking may
be controlled by common neural circuitry.
In addition to changes in direction, one can also adjust relationships
between sensorimotor elements of locomotor control and perception of
movement. Following forward walking on the perimeter of a rotating
disk, subjects generate curved walking trajectories when asked to walk
forward in a straight line without vision (Gordon et al.
1995). Subjects have no knowledge of this turning, termed podokinetic after-rotation (PKAR), as they perceive that they are
indeed walking along straight paths. PKAR does not depend on a sensory
conflict between somatosensory information indicating that the feet are
turning and visual information indicating that one is stationary with
respect to the environment. Subjects exposed to a rotating disk in the
presence of a rotating visual surround, a situation in which both
somatosensory and visual sources indicate movement, demonstrate PKAR
despite a lack of conflict between sensory inputs (Jürgens
et al. 1999
). Rather, PKAR suggests a remodeling of the
somatosensory signals regarding the relationship between trunk rotation
with respect to the feet and the perception of trunk rotation relative
to space (Weber et al. 1998
).
Our goal in this study was to determine whether, following an adaptive podokinetic (PK) stimulus presented in the context of forward walking, PKAR would be expressed similarly in both forward and backward walking. In light of previous studies reporting similarities between forward and backward walking patterns, we hypothesized that forward walking PK stimulation would result in PKAR during backward, as well as forward, walking. Demonstration of PKAR during backward walking following a forward-walking adaptive stimulus would support the hypothesis that the two forms of locomotion share common circuitry. It would also suggest that adaptations induced through the PK system represent a general adaptation of locomotor trajectory control, rather than a remodeling specific only to the form of locomotion used during the adaptive stimulus.
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METHODS |
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Subjects
Eleven healthy volunteers, 7 male and 4 female, participated in this study. Subjects ranged in age from 19 to 78 yr old. All subjects gave informed consent prior to participation in the study.
Protocol
Each subject participated in two experimental sessions, one to test forward walking and one to test backward walking. The direction of walking for each subject's first session was randomly selected to reduce the potential for order effects. A cadence of 2 Hz was maintained during the entirety of both sessions through use of a metronome attached to the trunk. Each session consisted of control trials, a 30-min period of PK stimulation, and postadaptation trials. Subjects wore a blindfold and earplugs for all control and postadaptation trials but not for the period of PK stimulation. Trials were each 2 min in duration.
FORWARD WALKING SESSION. Each subject performed three control trials during which they were asked to walk straight forward across the floor of a large, quiet television studio with a clear space of approximately 15 m × 20 m. Subjects were then exposed to the adaptive PK stimulus: 30 min of forward walking-in-place on the perimeter of a 76-cm-diam disk rotating at 60°/s in a clockwise direction. After this adaptation, blindfolded subjects were transported by wheelchair to the studio and asked to walk forward in a straight line across the floor. Six postadaptive trials, A1-A6, were performed at 5, 10, 15, 20, 25, and 30 min after termination of the adaptive stimulus. Between trials, and while still blindfolded, subjects were seated in a wheelchair and moved to a different, unknown starting location for the next trial.
BACKWARD WALKING SESSION. The backward walking session was the same as the forward walking session except subjects walked backward during the three control trials and the six postadaptive trials.
Data collection and analysis
As subjects walked, the position of the right foot was marked on the floor with chalk at 10-s intervals. To mark these positions, an experimenter followed each subject closely but made no physical or verbal contact with the subject. For forward walking, the experimenter walked behind the subject and marked the position of the heel, as this was the portion of the foot that made initial contact with the ground. For backward walking the experimenter again trailed the subject (requiring the experimenter to stand facing the backward-walking subject) and marked the position of the toe, as this was the portion of the foot that made initial contact with the ground. For all trials, the experimenter stayed in direct linear alignment with the subject to reduce the potential for directional cues. In addition, subjects wore a blindfold and earplugs, reducing the likelihood that visual or auditory cues influenced subject behavior.
Trajectories for each trial were measured in polar coordinates using a
large compass rose and a tape measure (Gordon et al. 1995). Polar plots of trajectories were produced using
Sigmaplot 5.0 (SPSS, Richmond, CA). Angular velocities were
calculated by measuring the angle between two successive segments of
the plot and dividing by the time between measures (i.e., 10 s).
Clockwise and counterclockwise angular velocities were assigned
positive and negative values, respectively.
We considered the possibility that the vestibular response to real rotation at the start of a trial might result in lower PKAR angular velocities at the beginning of a trial, while higher velocities may be reached by the end of a trial after attenuation of the vestibular signal due to continued rotation. Plots of each angular velocity measurement versus time within the trial were fitted with exponential growth curves to obtain maximum values and rise time constants. Although there was a trend toward increasing angular velocity as a trial proceeded, eliminating the first half of each trial and analyzing only the second minute produced results very similar to those obtained using all the measurements. Thus average angular velocities were calculated using the entire 2 min of data from each trial. Statistical comparisons of forward walking to backward walking values were performed using Friedman repeated measures ANOVAs (P = 0.05).
Mean angular velocities across subjects were plotted versus the start time of each trial (e.g., start time for A1 was 5 min, for A6 was 30 min). These plots were fitted with three-parameter exponential decay functions to determine the initial velocity, time constant of response decay, and a final asymptote value for each direction of walking. Curve fits were extrapolated to zero to obtain y-intercept values for each.
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RESULTS |
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Following 30 min of forward stepping on a disk rotating clockwise (CW) at 60°/s, subjects demonstrated counterclockwise (CCW) podokinetic after-rotation whether tested walking forward or backward. During PK stimulation the left leg was the inner limb and the right leg the outer limb with respect to the center of disk rotation. This relationship was maintained when subjects walked CCW during forward PKAR. However, during backward walking this relationship was reversed. Subjects walked CCW during backward PKAR, with the right lower extremity as the inner and the left as the outer limb relative to the center of rotation.
Figure 1 illustrates the locomotor
trajectories for forward walking (Fig. 1A) and backward
walking (Fig. 1B) in the same subject for trials recorded 10 min after cessation of the adaptive PK stimulus. Note that the paths
taken for the two directions of walking are similar, both turning in
the CCW direction. Average angular velocities (°/s) for the two
trials illustrated were 7.2 ± 0.30 (mean ± SE) and
6.5 ± 0.24 for forward and backward walking, respectively.
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Average angular velocities across all subjects are presented for forward and backward conditions in Fig. 2. Note that control values are low, indicating that subjects walked fairly straight paths prior to PK stimulation. For both forward and backward PKAR, the highest angular velocities were obtained for trial A1, recorded 5 min after cessation of the PK stimulus. Mean velocity for A1 was significantly greater for forward than for backward walking. From the A1 peak, values gradually declined, although some effect was still apparent at A6, recorded 30 min after PK stimulus offset. Values obtained by fitting data with exponential decay curves were similar for forward and backward walking (Table 1).
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In addition to the features of each trial as a whole, we examined
patterns of angular velocity changes within each trial to determine
whether there were differences between forward and backward walking.
Figure 3 shows the angular velocities
measured across the 2-min duration of forward and backward
A1 trials from the same subject. Note that in both forward
and backward PKAR, there is a trend toward increasing angular velocity
as the 2-min trial progresses. This is similar to the 1- to 2-min rise
described previously for the PKAR response (Weber et al.
1998). Rise times and maxima of trials A1-A6 for
forward and backward walking are given in Table
2. The maximum value for
A1-forward was significantly greater than that of
A6-backward, but no other significant differences were noted
for maxima across trials or conditions. There were no significant
differences in rise time across trials or between forward and backward
conditions.
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DISCUSSION |
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PKAR: an adaptive process?
An adaptive process has three defining features: acquisition,
retention, and transfer (Schmid and Jeannerod 1985).
Prior reports of PKAR have demonstrated acquisition, i.e., a change in
response that occurs as the result of a period of stimulation
(Gordon et al. 1995
; Weber et al. 1998
).
Retention, the persistence of a modified response after a period of
rest, has also been documented. PKAR can persist for several hours
following stimulation even when subjects sit quietly for periods of
25-30 min between trials (Weber et al. 1998
). These
results suggest that PKAR may be an adaptive process, as two of the
three defining features have been noted. The present study illustrates
transfer, the expression of a modified response in a situation
different from that used to produce the changes. We report PKAR during
backward walking following PK stimulation during forward walking. This
result, in combination with those of prior studies, supports the
hypothesis that PK modification is an adaptive process characterized by
acquisition, retention, and transfer.
Implications of PKAR transfer from forward to backward walking
We noted substantial PKAR during backward walking following
forward PK stimulation. Anstis (1995), however, reported
no transfer of linear translation aftereffects from one leg to the
other leg after hopping on a linear treadmill. Differences between our
results and those of Anstis may result from several factors. In the
present study, both legs were exposed to the adaptive stimulus and the direction of locomotion was changed, whereas only one leg was exposed
to the stimulus in Anstis' study. Additionally, the circuitry for
control of hopping on one leg may not overlap substantially with the
circuitry controlling hopping on the other leg. There is much evidence,
however, supporting the possibility that common network elements may
control forward and backward walking (Duysens et al.
1996
; Eilam and Shefer 1992
; van Deursen
et al. 1998
). Transfer of PKAR from a forward-walking stimulus
condition to a backward-walking postadaptive condition provides
additional support for this potential sharing of circuitry.
Transfer of PKAR across different forms of locomotion also suggests that the PK system may be a general control system for locomotor trajectory. As such, adaptations obtained during one form of locomotion would result in changes to trajectory for all other forms of locomotion. Based on this hypothesis, one would predict that PK adaptation during forward walking would also influence the trajectory of forward running and skipping. We were not able to test these forms of locomotion due to limitations in the space available for overground locomotor testing and concerns about subject safety.
PKAR transfer from forward to backward walking conditions
provides interesting insights into the parameters being regulated by
the PK system. The relationship of the two legs to the center of
rotation was not maintained across the two directions of locomotion, as
the left limb was the inner leg during forward walking but the outer
leg during backward walking. As such, the left leg moved through a
shorter distance than the right leg during forward walking, but through
a larger distance than the right leg during backward walking. Despite
this change, we propose that the direction of relative rotation between
the trunk and feet was preserved regardless of the direction of
locomotion. During PK stimulation with the disk rotating CW (Fig.
4A), the feet rotate to the
right relative to the space-stable trunk by virtue of their contact
with the rotating disk during stance, i.e., when the foot is firmly
planted on the support surface. When a normal subject walks CCW
overground in either the forward or backward direction (Fig.
4B), the feet again rotate to the right relative to
the trunk, although in this case the feet are space-stable during
stance and the trunk rotates leftward relative to the feet. This
relative rotation of the feet with respect to the trunk can be verified
by slowly walking forward and backward in a CCW direction around a
curved path. This same rotation of the feet with respect to the trunk
is true for an adapted subject performing PKAR in the CCW direction.
Thus the relative rotation between the feet and the trunk
was similar for PK stimulation, forward PKAR, and backward PKAR. These
results suggest that the PK system is primarily controlling relative
rotation between the trunk and feet, rather than relationships between the two limbs. Remodeling of the relationship between trunk rotation and the feet has been proposed previously as the mechanism for PKAR
(Jürgens et al. 1999; Weber et al.
1998
). Control of trunk-in-space with respect to the support
surface is also consistent with recent models of postural orientation
that hypothesize an internal representation of surface in space
resulting from a combination of vestibular and somatosensory
information (Mergner and Rosemeier 1998
).
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Comparison of overground PKAR to in-place PKAR
Most previous experiments examining PKAR have involved
postadaptive tests of stepping-in-place on the turntable, rather than tests of overground locomotion. The clear advantage to this in-place testing is that data can be collected for longer periods of time, as
room size is not a limiting factor. But is this in-place PKAR a
reasonable fascimile of overground PKAR? Our results for forward overground PKAR are similar to those for forward, in-place PKAR in
terms of first-order asymptote and decay time constant values (Weber et al. 1998). Our results are dissimilar in terms
of y-intercept, which had a magnitude of 8.3°/s in the
present study but 16.0°/s for in-place PKAR (Weber et al.
1998
). This difference is not surprising considering the
differences in the adaptation paradigms used. In the present study
subjects walked on the perimeter of a 76-cm disk rotating at 60°/s,
whereas subjects in Weber et al. (1998)
walked over the
center axis of the disk rotating at 45°/s. Walking on the perimeter
involves backward passive motion of both legs, outer more than inner,
whereas walking over the axis involves forward motion of one leg and
backward motion of the other. Additionally, we began sampling 5 min
after PK stimulus offset, while Weber et al. (1998)
began sampling immediately. Despite these differences, we observed
similar effects. As such, we think that similar phenomena are being
measured in overground and in-place testing of PKAR.
Vestibular-podokinetic interactions
Angular velocities tended to increase in value across the
2-min period of each trial. We were able to fit these rises with exponential growth curves, supporting previous reports of an
exponential rise in PKAR response over the first 2 min. This rise is
thought to reflect vestibular-podokinetic interactions, with vestibular inputs suppressing PK responses in a decaying manner over the first 2 min of stepping before peak PKAR velocity is obtained (Weber et
al. 1998). Our values for rise time constants are quite similar
to those calculated previously for healthy subjects and subjects with
unilateral vestibular loss (Weber, Fletcher, Melvill Jones, and
Block, unpublished data). Additionally, elimination of the first
several data points in each trial resulted in very little change in the
mathematical results of analyses conducted. It is clear that
substantial interactions between vestibular and podokinetic systems
occur (Melvill Jones et al. 2000
), but the extent to
which vestibular influences suppress PKAR in the first minutes of the
response is unclear based on current data. This may be clarified by
studies of PKAR rise characteristics of subjects with bilateral
vestibular loss.
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ACKNOWLEDGMENTS |
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This work was supported by National Institute on Deafness and Other Communication Disorders Grant R01-DC-04082-01A1 and Medical Research Council Grant MA-15639.
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FOOTNOTES |
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Address for reprint requests: W. A. Fletcher, Dept. of Clinical Neurosciences and Neuroscience Research Group, The University of Calgary, Foothills Hospital, 1403-29th St. N.W., Calgary, Alberta T2N 2T9, Canada.
Received 18 January 2001; accepted in final form 4 June 2001.
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REFERENCES |
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