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Neuro-Otology Unit, Department of Clinical Neuroscience, Division of Neuroscience and Mental Health, Imperial College London, Charing Cross Hospital, London, United Kingdom
Submitted 31 October 2007; accepted in final form 7 January 2008
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ABSTRACT |
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INTRODUCTION |
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; Allum and Pfaltz 1985; Allum et al. 2001; Beule and Allum 2006; Buchanan and Horak 2001; Carpenter et al. 2001; Horak et al. 1990; Ito et al. 1995; Pozzo et al. 1989, 1995). However, in regular everyday life activities, bilaterally labyrinthine defective subjects (LDS) function with only a moderate degree of impairment (Grunfeld et al. 2000). This discrepancy may be explained by the use of anticipatory motor mechanisms in predictable conditions, whereby activation of postural muscles occurs in advance of a postural perturbation (Belenkiy et al. 1967).
Anticipatory postural adjustments have been mostly examined in simple experimental situations, such as rapidly raising the arms while observing electromyographic (EMG) activity in the lower limbs. These experiments show lower limb activation that is earlier than upper limb activation; i.e., the legs "anticipate" the instability that will be induced by moving the arms (Belenkiy et al. 1967; Bouisset and Zattara 1981; Brown and Frank 1987; Friedli et al. 1988; Horak et al. 1984). More recently, interest has shifted toward anticipatory mechanisms as they supposedly occur in everyday life (Cham and Redfern 2002; Marigold and Patla 2002; Pai et al. 2003; Pavol and Pai 2002; Pijnappels et al. 2001). We have recently studied a case in point, the "broken escalator" phenomenon, characterized by an odd sensation of imbalance and stumbling when walking onto an escalator that is stationary, despite full knowledge that the escalator will not move (Reynolds and Bronstein 2003). Experimentally, we reproduced a similar scenario by asking subjects to walk onto a moving motorized sled and concluded that the "broken escalator" phenomenon is an aftereffect of locomotor adaptation. Following locomotor adaptation on the moving sled (MOVING condition) subjects approach the stationary sled (AFTER condition) inappropriately fast and they experience a large forward overshoot of the trunk (see "Linear Fastrak"; Fig. 1, right).
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; Haffenden et al. 2001; Reynolds and Bronstein 2003, 2004). The motor behavior expressed in this locomotor aftereffect (LAE)—walking faster and leaning forward—is exactly what would be needed if the sled were to move, a "just in case" strategy (Bunday et al. 2006). However, because the sled does not move, the LAE represents an inappropriate release of anticipatory motor behavior (Reynolds and Bronstein 2004) that, in turn, induces postural instability.
Herewith, we report experiments with the LAE paradigm in LDS. On the basis that these patients have intact proprioceptive and CNS function we expected that locomotor adaptation would occur (Keshner et al. 1987) and therefore LDS would display an aftereffect. However, a question addressed here is concerned with the "braking" of the trunk overshoot, that is, what mechanisms ("brakes") stop subjects falling forward once they have been self-destabilized by the aftereffect? In this study we test bilaterally labyrinthine defective subjects (LDS) to see how, in the absence of vestibular function, they "brake" this component of the aftereffect. More generally, the question investigated is how complex anticipatory postural behavior is modified by the absence of sensory (vestibular) feedback. A prediction was that LDS would have a larger than normal trunk movement aftereffect, that is, a greater forward overshoot of the trunk in the AFTER trials due to the absence of vestibular function. However, if the braking during the aftereffect was also the result of anticipatory motor mechanisms, no difference between normal and LDS should be found.
In addition, since visual input is critical for balance in the absence of vestibular function, we carried out additional experiments, in normal and LD subjects, to investigate the effects of vision on this LAE. In contrast to vestibular function, which may play only a part in "braking" the aftereffect, vision could play a part both in the release of the aftereffect (e.g., visual confirmation that one is indeed on the sled) and, particularly in LDS, in "braking" the aftereffect.
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METHODS |
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The sled was powered by two linear induction motors, at a maximum velocity of 1.3 m/s, and enveloped by a fixed platform under which it could freely pass (Fig. 1, top left). Movement of the sled was triggered by gait initiation via an infrared light switch (Reynolds and Bronstein 2003). On walking through the sensor, after a 600-ms delay, the sled would travel about 3.7 m in 4.2 s (maximum velocity reached by 896 ms). A tachometer provided velocity output.
Subject sagittal trunk position was measured using an electromagnetic tracking device (Fastrak; Polhemus, Colchester, VT), accurate within 0.08 cm RMS for the receiver position. The sensor was placed over the C7 vertebrae and the transmitter was attached to the sled. A second sensor was earth-fixed so that movement of the sled could be accounted for when calculating approach (trunk) velocity. Step-timing information was given by pressure sensors (FlexiForce; Teckscan, South Boston, MA) placed under the first metatarsal phalangeal joint and heel. A linear sled-mounted accelerometer (Entran, Watford, UK) provided independent accurate foot–sled contact timing. Superficial bipolar EMG (band-pass filtered at 10–500 Hz) from the medial gastrocnemius (MG) and tibialis anterior (TA) muscles of each leg was also recorded in the LDS–NC experiments. All data were recorded at 500 Hz.
Procedure
EXPERIMENT 1. This experiment was conducted to see the effect of vestibular loss on the LAE. Nine LDS, ranging from 42 to 69 yr [mean = 57.7 ± 3.0 yr (SE)], were tested. All patients were in chronic compensated phase and able to walk unassisted with eyes open. Rotational and caloric nystagmic responses in the dark were reduced to <10% of normal (Rinne et al. 1999); etiology was idiopathic (six), gentamicin toxicity (one), postmeningitic (one), and posttraumatic/idiopathic (one). Time since vestibular failure was 2–15 yr. An age-matched normal control (NC) group of 13 subjects, ranging from 43 to 66 yr (mean = 57.5 ± 1.7 yr), was tested. All normal controls were healthy and reported no history of neurological illness.
The experimental sequence consisted of conditions BEFORE, MOVING, and AFTER, with eyes open throughout (Fig. 1, bottom left). Subjects completed baseline trials walking five times onto the stationary sled (BEFORE condition). Gait was initiated after an auditory cue (three "beeps"); they stepped with the right leg first onto the fixed platform, then with the left on the sled. Here they stopped and adopted a quiet stance with both feet on the sled, until recording was completed. Each trial lasted 16 s. Before continuing onto the MOVING trials each participant was shown how the platform would move. All subjects performed 15 MOVING trials; they were asked to use the available handrails only if absolutely necessary. When the MOVING trials were complete, a clear and unequivocal verbal warning was given that the sled would no longer move for the AFTER trials. A visual affirmation was given by wedging the sled in place with wheel stops; the motor was ostensibly turned off to reassure subjects that the sled would no longer move. All subjects then completed another five stationary AFTER trials.
EXPERIMENT 2. This experiment was conducted to assess the effect of vision on the LAE in young normals; 16 healthy subjects, ranging from 19 to 30 yr (mean = 22.6 ± 0.4 yr), were tested. Eight subjects were allocated to each group, eyes open (EO) and eyes closed (EC), according to whether the AFTER trials were initially conducted with EO or EC, respectively (Fig. 1, bottom left).
The experiment followed the same general sequence: BEFORE, MOVING, and AFTER. The EO group followed the same protocol as that of experiment 1. The EC group completed a slightly different protocol, where they completed five stationary BEFORE trials with eyes open and then five BEFORE trials with eyes closed. Subjects closed their eyes and were blindfolded at the beginning of each trial, but used vision to navigate back to the start position. Thus subjects did have the opportunity to view the sled prior to closing their eyes. MOVING trials were always conducted with eyes open for safety reasons. The EC group then completed two sets of five AFTER trials, first with eyes closed and then with eyes open (Fig. 1, bottom left).
EXPERIMENT 3.
Here we studied the aftereffect in LDS in the absence of visual input. Both patients and age-matched controls followed the same sequence as that of the EC group (see experiment 2 and Fig. 1, bottom left). Due to the difficulty of walking without vision the LDS were selected on the basis of a higher approach gait velocity in experiment 1. The fastest 7 LDS and all 13 NCs were asked to return, although only 5 LDS, age range 42–69 yr (mean = 58.6 ± 5.1), and 5 NC, age range 43–65 yr (mean = 56.6 ± 3.7) agreed to be retested. All subjects were tested 
12 mo after experiment 1. Local ethical approval and informed consent were obtained in all cases.
Data analysis
Pre and post foot–sled contact epochs were derived from the sled-mounted accelerometer and corroborated with foot pressure data. Trunk position was provided by the Fastrak (Fig. 1, right). For stationary trials (BEFORE and AFTER), forward trunk sway was measured as the maximum forward deviation ("overshoot") of the trunk, relative to the mean final resting stance position in the last 3 s of the trial [Fig. 1, right (a)]. Due to the nature of the MOVING data, trunk sway was measured as the maximum forward displacement of the trunk (peak backward to peak forward) [Fig. 1, right (b)]. The velocity at which subjects approached the platform (approach gait velocity) was calculated using the position sensor on the trunk, defined as the mean velocity in a 0.5-s time window prior to foot–sled contact [Fig. 1, right (c)].
EMG signals of the left leg (sled-contact leg) were rectified and integrated over a 500-ms time window after foot–sled contact [Fig. 1, right (d)]; MOVING and AFTER trial values were normalized with respect to a mean baseline integrated EMG measured in the BEFORE trials 3–5.
EMG latencies during the first after trial (AFTER 1 trial) were measured from nonfiltered grand averages and from AFTER to BEFORE subtracted grand averages. Latencies of left TA (LTA) and right MG (RMG) were measured from the second peak of forward trunk velocity, obtained from the differentiated trunk displacement signal (see Fig. 3). Left MG (LMG) was measured from left heel contact (Figs. 3 and 4). Latencies were calculated automatically taking a mean baseline ± 3SD over a 100-ms baseline period at the beginning of each trial, and visually corroborated in all cases. For graphical display purposes, EMG was low-pass filtered at 35 Hz. Latencies during the MOVING trials (due to linear motor and movement artifact) could not be measured reliably.
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For all experiments a two-way repeated-measures ANOVA (mixed design) analyzed each variable (Bunday et al. 2006). Factors group (two levels: LDS vs. NC and EO vs. EC) and trial (two levels: mean BEFORE vs. AFTER 1; an aftereffect is defined as a significant trial effect) were investigated. Bonferroni multiple comparisons were performed for post hoc trial effects. Any specific comparisons between groups were made through independent t-test.
A criterion was devised to assess how many LDS and NC subjects had an aftereffect. The mean + 2SD for BEFORE trials 1–5 was calculated for each subject for variables forward trunk sway (trunk overshoot), approach velocity, and EMG of the LMG (the leg leading onto the sled). If AFTER trial 1 was above the mean + 2SD this was considered to be an aftereffect. If at least two of the three variables yielded an aftereffect then this constituted an overall aftereffect. A 
2 test was used to determine differences in the frequency of occurrence of the aftereffect between the groups.
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RESULTS |
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Qualitative observations: All subjects performed the BEFORE trials without difficulty. During MOVING trials NC subjects were unsteady, using the handrails for one to two trials. The LDS were visibly more unsteady than the controls during MOVING trials and required handrail use and occasional manual support by two assistants, for the first four trials, on average. Gradually all subjects improved their stability. During the AFTER trials, most subjects subjectively reported an unusual or unexpected sensation of unsteadiness and could be seen to be unsteady on mounting the stationary sled for the first AFTER trial. Quantitative results now follow.
BEFORE and MOVING trials
APPROACH GAIT VELOCITY. Figure 2 shows approach walking velocity data for both NC and LDS. All subjects increase their approach gait velocity during the MOVING trials. Note that patients and controls reach 85 and 89%, respectively, of the final approach velocity on the first adaptation trial (MOVING trial 1). This increase must be an estimate based on seeing the platform move once (see METHODS), similar for both groups (t = –0.955, P = 0.351). Both controls and patients achieved steady-state velocity by the third trial (i.e., values plateau after MOVING trial 3; Fig. 2, "Approach Velocity"). LDS approached the MOVING sled slightly slower than NC, although this difference did not quite reach statistical significance [F(1,20) = 3.501, P = 0.076].
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AFTER trials
Figure 3 shows grand-averaged trunk motion signals and leg EMG recordings for the age-matched controls (dotted trace) and LDS (solid trace) during AFTER trial 1 (i.e., the aftereffect). Note the trunk overshoot in AFTER trial 1 (i.e., an aftereffect). EMG bursts are also larger in AFTER trial 1 (see below under Integrated EMG: LTA and LMG). Some EMG amplitude/latency differences can be seen between the groups but this will be subsequently discussed under Grand-averaged EMG. Figure 2 summarizes group data for normal controls and LDS. As in previous work (Reynolds and Bronstein 2003) an aftereffect was expressed as an increase in approach velocity, forward trunk sway, and leg EMG when AFTER trial 1 values were compared with BEFORE values. Statistics are subsequently given.
Trunk sway.
Figure 2 (top; AFTER) shows the mean forward trunk sway (or overshoot) for the LDS and the NC during the AFTER trials. A significant aftereffect can be seen in both groups [F(1,20) = 35.851, P = 0.000]. Although the LDS appear to have increased forward trunk sway compared with the NC, this was not significant [F(1,20) = 1.363, P = 0.257].
Approach gait velocity.
Figure 2 (second diagram from top; AFTER) shows that approach velocity in both subject groups was faster during the AFTER trials than BEFORE, in particular AFTER trial 1. This confirms the presence of significant aftereffects [F(1,20) = 109.787, P = 0.000]. LDS have slightly slower approach velocity compared with that of NC; thus a group effect was found [F(1,20) = 5.894, P = 0.025]. However, the lack of a significant interaction between trial and group [F(1,20) = 1.117, P = 0.303] indicates that the significant group effect depends on 1) LDS approaching the sled slightly slower than NC throughout, as expected, and 2) both groups showing a similar approach velocity aftereffect.
Integrated EMG: LTA and LMG.
Figure 2 (bottom two diagrams; AFTER) shows the mean normalized EMG activity of LTA and LMG during the AFTER trials, in the regions of interest (see METHODS). The increased levels of EMG activity in both muscles during the AFTER trials, with respect to the BEFORE levels, indicate the presence of an aftereffect [F(1,20) = 9.065, P = 0.007; F(1,20) = 44.787, P = 0.000, respectively]. Note 1) no obvious differences between the subject groups [LTA: F(1,20) = 1.895, P = 0.184; LMG: F(1,20) = 1.410, P = 0.249] and 2) that high EMG values in AFTER trials 1 and 2 rapidly attenuate on successive AFTER trials.
A similar proportion of subjects in both groups showed an aftereffect. Based on the criteria described in METHODS, 88.9% of the LDS and 84.6% of the NC displayed an aftereffect [2 (1, n = 22) = 0.082, P = 0.774].
GRAND-AVERAGED EMG. The experiments required subjects to take a first step with the right foot onto the fixed platform, then a second step taking the left foot onto the sled, followed by the right foot onto the sled for gait termination. Figure 3 shows the EMG events during such gait initiation; LTA activation precedes TA activity lifting the foot in the swing leg (RTA) (approximate time –2 s, –1.5 s in Fig. 3). This is followed shortly by LMG activation (starting at approximately –1 s), aiding forward motion of the center of mass. Later activity in RTA (approximate time –0.8 s) mediates right ankle dorsiflexion during single-limb stance for heel strike and controlled loading of the foot onto the fixed platform. The RMG activity and LTA dorsiflexion activity at about –0.5 s is another single-limb stance phase when subjects are preparing for left foot landing onto the platform. Within this general pattern of locomotor events we subsequently highlight three points of relevance.
LDS are known to display reduced EMG amplitudes, related to reductions in gait velocity (Sasaki et al. 2001; Tucker et al. 1998). In line with this, prior to foot contact, the patients exhibit decreased activity in both right and left MG and TA; this is particularly noticeable at gait initiation in LTA, RTA, and LMG, and later during single-limb stance activity in RTA (–1.75 to –0.5 s). This reduced muscle activity can be associated with the slower approach gait velocity seen in the patients. By subtracting the mean BEFORE from the AFTER 1 data, the EMG activity specifically due to the aftereffect can be displayed for each group (Fig. 4). Prefoot contact differences between the groups seen in Fig. 3 now disappear due to the normalization process.
After postfoot contact, however, some EMG latency differences become apparent (Figs. 3 and 4). Latencies were measured from peak trunk velocity (second hump in the differentiated trunk position signal) to the onset of EMG [NB: time to peak trunk velocity from left heel strike did not differ between the groups by >20 ms (LDS: 104 ± 14 ms; NC: 88 ± 14 ms)]. Due to the similarity of the grand-averaged latencies (Fig. 3) and the grand-averaged subtracted latencies (Fig. 4), only the subtracted latencies are reported. The left TA burst seen after left foot contact (
0.5 s) occurs later in the LDS (396 ms) compared with the controls (242 ms) (Fig. 4). Right MG is also delayed in the LDS (292 ms) with respect to the NC (186 ms) (Fig. 4; n.b.: visual inspection of individual subjects' recordings showed essentially similar latencies in all muscles). Because LDS walked on average 15% slower than NC, we corrected latencies of LDS by 15% but, despite this, they are still prolonged (TA: 337 ms; MG: 248 ms).
Despite these group differences, Figs. 3 and 4 bear out one critical similarity—that at foot–sled contact (time 0 s) LMG becomes suddenly active. This MG burst is an important active component of gait termination (Sparrow and Tirosh 2005); however, note that this activity, which was present in BEFORE trials, becomes significantly increased during the first AFTER trial (Reynolds and Bronstein 2003). This burst is similar in timing and amplitude in the LDS and NC and is, in fact, anticipatory (i.e., it occurs before foot–sled contact) at –20 and –13 ms, respectively. Visual inspection of all individual subjects' recordings showed this anticipatory burst (e.g., latencies 
0 ms). This burst is completely absent in MOVING – BEFORE subtracted data (Fig. 5), thus indicating that this LMG activity is not related to the adaptation induced by the MOVING trials but to the "braking" of the aftereffect (i.e., stopping the body from falling forward). We ascertained that grand averages were representative because individual EMG amplitudes did not differ by >14%.
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BEFORE TRIALS. This experiment was conducted in young normal subjects to see whether visual input played a part in aftereffect onset (triggering) or termination (braking). The EC group completed two sets of AFTER trials first with eyes closed then with eyes open and, accordingly, performed two sets of related baseline BEFORE trials. The EO group constituted the control group so all data were obtained with eyes open. The groups in Fig. 6 are labeled according to what subjects undertook first in the AFTER trials, eyes open or eyes closed. Data were similar to those of the normal controls in experiment 1 but, naturally, in eyes closed BEFORE trials, subjects walked slightly slower [drop in approach velocity between trials 5 and 1' (n.b.: the change from trial 5 to trial 1', indicated by the vertical black dotted line, represents the transition from eyes open to closed and vice versa; Fig. 6, bottom left)].
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FIRST SET OF AFTER TRIALS. Trunk sway and approach gait velocity. Figure 6 shows the mean forward trunk sway and approach velocity for groups EC and EO during the AFTER trials. Both groups show an aftereffect for trunk sway [F(1,14) = 6.999, P = 0.019]) but no significant group difference [F(1,14) = 0.000, P = 0.990]. Approach velocity also shows the presence of an aftereffect [F(1,14) = 47.051, P = 0.000], although again without a group difference [F(1,14) = 0.272, P = 0.610]. The findings indicate that vision does not influence release of the aftereffect.
SECOND SET OF AFTER TRIALS (EC GROUP). Interestingly, when the EC group reopened their eyes (AFTER trial 1'; Fig. 6), a small aftereffect reappears both in approach velocity (t = –3.565, P = 0.008) and trunk sway (t = –2.550, P = 0.038). This indicates that both components of the aftereffect reemerge on eye reopening.
Experiment 3: NC versus LDS (eyes closed)
BEFORE AND MOVING TRIALS. NC and LDS data during BEFORE and MOVING trials were very similar to those of experiments 1 and 2, and so they are not shown. However, this time during the MOVING trials (always with eyes open) there was little group difference in approach velocity [F(1,7) = 0.572, P = 0.474] (recall that LDS were selected by superior approach gait velocity). As in experiment 1, LDS swayed more than NC during the MOVING trials [F(1,7) = 7.288, P = 0.031].
FIRST SET OF AFTER TRIALS. Trunk sway. Figure 7 (left) shows the mean forward trunk sway for the LDS and NC retested with eyes closed. As in experiment 1 a significant aftereffect was found [F(1,8) = 9.692, P = 0.014]. The aftereffect was similar in magnitude to the previous eyes open aftereffect (LDS experiment 1 = 11.99 ± 1.94 cm, experiment 3 = 11.13 ± 4.80 cm; NC experiment 1 = 8.63 ± 2.00 cm, experiment 3 = 10.82 ± 1.68 cm). There were no differences between LDS and NC [F(1,8) = 0.357, P = 0.567], although the LDS, unlike the controls, remain somewhat unstable in the subsequent AFTER trials (recall they are walking with eyes closed).
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SECOND SET OF AFTER TRIALS. Trunk sway. In agreement with what was observed during experiment 2 the aftereffect reemerged on eyes reopening for both subject groups [F(1,8) = 10.425, P = 0.012]. The main finding is that the reemergence of the aftereffect on eye reopening is significantly larger in LDS than that in NC [F(1,8) = 11.982, P = 0.009] as shown in Fig. 7, right, top.
Approach velocity. A reemergence of the aftereffect on reopening the eyes was also noticed for approach velocity (Fig. 7, eyes reopen) [F(1,8) = 10.498, P = 0.012]. There was no significant difference between subject groups [F(1,8) = 0.832, P = 0.388].
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DISCUSSION |
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, 2004). In these experiments we investigated normal and LD subjects (eyes open and closed) to gain insight into the processes terminating ("braking") this aftereffect.
All subjects faced a postural challenge during the MOVING and the AFTER trials and the latter condition was used to study the role of the vestibular system in a self-generated postural perturbation. The challenge presented by the MOVING trials is an externally imposed postural perturbation. In contrast, the challenge posed during the AFTER trials is internally generated and, so, the stumble and trunk overshoot observed in the aftereffect are the result of the inappropriate release of learned motor activity. Examples of "self-inflicted" postural stimuli are scarce in the literature and, in the few available, they are the result of unexpected "catch" trials (e.g., Mille et al. 2003, 2005; Traub et al. 1980), unlike the paradigm used in the current experiments where subjects had full warning.
Impact of vestibular loss during MOVING (adaptation) trials
During the MOVING trials, forward trunk sway was almost twice as large in the patients as that in controls. This result is fully expected in that many studies have shown increased unsteadiness during support surface motion in LDS (Allum and Honegger 1998; Allum and Pfaltz 1985; Bacsi and Colebatch 2005; Beule and Allum 2006; Buchanan and Horak 2001; Creath et al. 2002; Dichgans and Diener 1989; Horak et al. 1994; Martin 1965). In addition, our results show that normal subjects plateau (i.e., learn the task as best as they can) by MOVING trial 3, whereas patients plateau by trial 6. In fact, LDS appear to continue to adapt throughout the MOVING trials, as shown by the progressive decline in the difference between trunk sway values in patients and normal controls (see gray area, Fig. 2, top). This finding suggests that vestibular loss also interferes with postural adaptation to repetitive stimuli (i.e., the moving sled). However, vestibular loss slows down this adaptation process but does not prevent it altogether since, by the end of the MOVING trials, LDS sway was approaching normal values. This is in agreement with some previous research (Keshner et al. 1987) and in contrast with other studies (Black et al. 1983; Buchanan and Horak 2001; Nashner et al. 1982). However, stimuli used and measurements of adaptation from such research are not always comparable to those of the current study (e.g., Buchanan and Horak 2001).
In contrast to forward trunk sway, approach gait velocity during the MOVING trials was only slightly and nonsignificantly decreased in LDS. Further, both groups' approach gait velocity plateau similarly on MOVING trial 3. What is the reason for this apparent discrepancy, whereby LDS show normal approach velocity but abnormally increased trunk sway? The crucial difference is that approach velocity is measured for the 500 ms prior to foot–sled contact, whereas trunk sway is measured after subjects are on the sled; i.e., approach velocity as measured in this experiment is an anticipatory parameter. In this regard, note that the increase in approach velocity deployed by the subjects to facilitate landing onto the moving sled consists of two components: 1) an increase in approach velocity already present in MOVING trial 1 (see Fig. 2), which is entirely anticipatory and based solely on a visual estimate, that is, watching the sled move once (cf. METHODS); 2) from then on, the velocity with which subjects approach the sled is based on preceding visual estimates plus the multisensory feedback experience of having stepped onto the moving sled. Perhaps not surprisingly, then, this dual predictive behavior is intact in LDS. Preservation of such anticipatory processes in LDS must be a crucial mechanism explaining their relatively well adapted performance in regular everyday life activities.
Impact of vestibular loss during the AFTER trials: "braking" the aftereffect
The aftereffect is an expression of the adaptive behavior seen during the MOVING trials. Since during the AFTER trials the sled is stationary, the increased approach velocity and forward trunk overshoot are inappropriate and the aftereffect itself is a threat to postural balance. Therefore we hypothesized that, in the absence of vestibular function, the forward trunk sway overshoot would be larger than normal. However, this was not the case and forward trunk sway data did not even approach significance, either in experiment 1 (eyes open) or in experiment 3 (eyes closed). On the basis of this, the conclusion is that the vestibular system does not participate in the braking of the forward overshoot produced by our aftereffect. In contrast, however, the early phase of the podokinetic aftereffect (elicited after prolonged walking on a rotating platform) is significantly increased in LDS (Earhart et al. 2004). Because their task involves fairly constant velocity rotation, the difference between normal and LDS is fully expected because the patients will not receive opposing inputs from the semicircular canals during the early portion of the self-generated rotation (Earhart et al. 2004). Our LAE, in contrast, does not expose subjects to prolonged rotations and, if phasic vestibular responses participated in the braking process, the trunk overshoot should have been larger than normal. The lack of difference between LDS and NC could be explained if the head velocity induced by the LAE was outside the operational range of the semicircular canals. However, angular motion at C7 was within the optimal velocity/frequency/acceleration range of the vestibular system (see APPENDIX). It is therefore likely that the braking of the forward trunk overshoot observed in this aftereffect is not vestibular based. In agreement, the only delayed EMG latencies found in our LDS occurred about 200 ms after peak trunk velocity, which would be too late for "braking" the forward sway in our experiments.
The current experiments provide insight into the mechanisms responsible for "braking" the trunk overshoot aftereffect. The subtracted data identifying the specific EMG patterns associated with the first AFTER trial (Fig. 4) show that during the first AFTER trial the left MG becomes highly active just before foot–sled contact (Figs. 3 and 4). Such left MG burst is a strong candidate for stopping the body lurching forward during the first AFTER trial. Two features are important in this left MG burst in AFTER trial 1: 1) that it just precedes foot–sled contact, indicating that it is an anticipatory (internally generated) process, and 2) that it is of a similar magnitude, shape, and latency in NC and LDS. These findings—that the "braking" process is essentially anticipatory and that it remains unchanged in LDS—explain why there are no significant differences in the forward sway aftereffect between the normal and LD subjects.
Such "braking" MG bursts occur when subjects voluntarily stop locomotion, as in this study (Sparrow and Tirosh 2005). The finding that this MG burst was larger in AFTER trial 1 than in BEFORE trials indicates that additional anticipatory EMG activity (for braking the faster approach gait velocity and the forward trunk sway aftereffect) was also incorporated. The origin of the anticipatory braking, as represented by enhanced left MG burst before foot–sled contact, cannot be ascertained from the current experiments but anticipatory mechanisms, generating EMG activity in advance of sensory triggers, are known to play an important part in postural and motor control (Belenkiy et al. 1967; Bouisset and Zattara 1981; Brown and Frank 1987; Friedli et al. 1988; Horak et al. 1984). In any case, the presence of this enhanced burst indicates, first, that the CNS is anticipating that a stumble (i.e., the aftereffect) is likely to occur on gait termination and, second, that relying on slow sensory feedback for avoiding a fall is likely to fail. Although proprioceptive mechanisms, which are intact or even enhanced in LDS (Day et al. 1997; Fitzpatrick et al. 1994; Inglis et al. 1995; Lund and Broberg 1983; Nashner and Wolfson 1974), could also be good candidates for braking the trunk overshoot, data in patients with peripheral neuropathy show that the early left MG braking activity seen in the LDS is also evident in neuropathy patients; in fact it occurs even earlier in these patients, showing that this braking activity is even more anticipatory when proprioceptive inputs are defective (K. Bunday 2008; PhD thesis, University of London).
Role of visual input in the locomotor aftereffect
Previous experiments established that the aftereffect was observed only if subjects walked onto the same stationary sled but not if they walked onto a different surface (Reynolds and Bronstein 2004). Thus it could be that sighting of the sled is a necessary precondition for aftereffect expression. However, experiments 2 and 3 showed that the aftereffect did not change with eye closure.
Although it can be concluded that visual feedback during execution of the first AFTER trial is not necessary for LAE release, the reciprocal is not true. Visual input confirming that one will not walk onto the sled inhibits aftereffect emergence (e.g., walking on the fixed launch platform does not release an aftereffect; Reynolds and Bronstein 2004). These apparently conflicting findings can be resolved if we accept that subjects know whether they are walking onto the sled on the basis of cognitive and/or contextual cues. Thus an internal judgment that the learned motor behavior might be required (i.e., the sled may move) releases the aftereffect, rather than just viewing the sled. In summary, the data show that release of the aftereffect is not specifically dependent on visual feedback during the movement but on more general spatial or "place" contextual cues. Vision still plays a part in building up this general spatial context as discussed in the following text.
Visual context and the reemergence of the aftereffect
Vision is likely to be important in building up a spatial context for this learned behavior since the adaptation (MOVING) trials were always conducted with eyes open. Having completed one set of AFTER trials with eyes closed, subjects in experiments 2 and 3 completed a second set of AFTER trials reopening the eyes. Noteworthy, eye reopening rereleased an aftereffect, both for approach gait velocity and trunk forward sway in the three subject groups (Figs. 6 and 7). This aftereffect was smaller than the previous aftereffect, yet consistent enough among subjects to be significantly larger than baseline BEFORE values. Reinstating the visual context in which the adaptation took place caused the adapted behavior to reemerge. This is in agreement with increasing evidence showing the importance of context in sensorimotor learning (Krouchev and Kalaska 2003; Salinas 2004; Varriane et al. 2002).
Of note, the reemerged aftereffect was significantly larger in LDS than that in NC (Fig. 7). This difference can be taken as evidence that LDS placed increased weight to visual information during the adaptation phase. In other words, LDS relied on vision more than normal controls when learning to negotiate the moving sled, as expected and previously shown in other support surface motion experiments (Buchanan and Horak 1999; Hollands et al. 1996; Patla et al. 2002). Then, when the original visual context was revisited, LDS showed an enhanced aftereffect. LDS are known to have enhanced sensitivity to visual input in tasks where vision is used for feedback control (e.g., increased postural sway with eye closure or in response to visual motion; Guerraz et al. 2001; Peterka and Benolka 1995). The current experiments indicate that LDS also have increased up-regulation of visual mechanisms when vision is used for feedforward control and context buildup.
Several areas of the brain have been implicated in sensory context learning. These include the cerebellum (Lewis and Tamargo 2001), the basal ganglia (Turner and Anderson 2005), and the hippocampus (Blair and Sharp 1995; Etienne et al. 1988; McNaughton et al. 1991; Poucet and Save 2005), the latter being important for visuovestibular spatial navigation (Brandt et al. 2005; Markus et al. 1994; Ossenkopp and Hargreaves 1993; Semenov and Bures 1989). One could speculate that in our experiments a distinct sensory-context map of the environment in which subjects learned to walk onto the moving sled was made. On reopening the eyes this distinct sensory context reappears, activating circuits that normally would include visuovestibular input. In the patients, the lack of vestibular input could make context-driven circuits supersensitive to visual input, e.g., by denervation supersensitivity (Bannerman et al. 2001), and on eye reopening these up-regulated circuits would trigger a larger aftereffect in LDS.
In conclusion, we have shown that the LAE is not increased in the absence of vestibular function even though, as expected, LDS are abnormally unsteady during the MOVING (adaptation) trials. This result suggests that the vestibular system may be more involved in counteracting externally imposed, rather than internally generated, postural perturbations. In agreement, we observed that braking of the aftereffect is executed by anticipatory EMG activity. This indicates that the CNS has advanced information that the aftereffect will occur and sets off feedforward mechanisms to deal with this potential source of unsteadiness. We have also found that the LAE does not necessitate vision to be triggered. However, visual input participates in building up a spatial context during the adaptation trials. The strength of this visuocontextual mechanism appears to be increased in the absence of vestibular function.
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APPENDIX |
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In 12 normal subjects angular velocity at C7 (as the nearest segment to the head) was measured (gyroscope; Silicone Sensing Systems, Hyogo-ken, Japan) to ascertain that motion parameters during these experiments were within the optimal functional range of the vestibular system. Peak C7 angular velocity during MOVING trial 1 and AFTER trial 1 was 61 ± 15 and 43 ± 8°/s, respectively, with frequency components of 1–1.7 Hz. Therefore peak C7 angular accelerations at these frequencies during MOVING trial 1 were 381 ± 96 to 648 ± 164°/s2 and AFTER trial 1 were 274 ± 49 to 465 ± 83°/s2, respectively. Such angular accelerations are well above threshold values of the semicircular canals [0.25–1.75°/s2; adapted from Guedry Jr. (1974)].
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GRANTS |
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Address for reprint requests and other correspondence: A. M. Bronstein, Imperial College London, Neuro-Otology Unit, Department of Clinical Neurosciences, Division of Neuroscience and Mental Health, Charing Cross Hospital, London W6 8RF, UK (E-mail: a.bronstein{at}imperial.ac.uk)
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REFERENCES |
|---|
|
Allum JH, Honegger F. Interactions between vestibular and proprioceptive inputs triggering and modulating human balance-correcting responses differ across muscles. Exp Brain Res 121: 478–494, 1998.[CrossRef][Web of Science][Medline]
Allum JHJ, Honegger F, Schicks H. The influence of a bilateral peripheral vestibular deficit on postural synergies. J Vestib Res 4: 49–70, 1994.[Medline]
Allum JHJ, Pfaltz CR. Visual and vestibular contributions to pitch sway stabilisation in the ankle muscles of normals and patients with bilateral peripheral vestibular deficits. Exp Brain Res 58: 82–94, 1985.[Web of Science][Medline]
Bacsi AM, Colebatch JG. Evidence for reflex and perceptual vestibular contributions to postural control. Exp Brain Res 160: 22–28, 2005.[CrossRef][Web of Science][Medline]
Bannerman DM, Gilmour G, Norman G, Lemaire M, Iversen SD, Rawlins JN. The time course of the hyperactivity that follows lesions or temporary inactivation of the fimbria-fornix. Behav Brain Res 120: 1–11, 2001.[CrossRef][Web of Science][Medline]
Belenkiy VE, Gurfinkel VS, Paltsev EI. On elements of control of voluntary movements. Biofizica 12: 135–141, 1967.[Medline]
Beule AG, Allum JH. Otolith function assessed with the subjective postural horizontal and standardised stance and gait tasks. Audiol Neurootol 11: 172–182, 2006.[CrossRef][Medline]
Black FO, Wall C 3rd, Nashner LM. Effects of visual and support surface orientation references upon postural control in vestibular deficient subjects. Acta Otolaryngol 95: 199–201, 1983.[Medline]
Blair HT, Sharp PE. Anticipatory head direction signals in anterior thalamus: evidence for a thalamocortical circuit that integrates angular head motion to compute head direction. J Neurosci 15: 6260–6270, 1995.[Abstract]
Bostock E, Muller RU, Kubie JL. Experience-dependent modifications of hippocampal place cell firing. Hippocampus 1: 193–205, 1991.[CrossRef][Medline]
Bouisset S, Zattara M. A sequence of postural movements precedes voluntary movement. Neurosci Lett 22: 263–270, 1981.[CrossRef][Web of Science]
Brandt T, Schautzer F, Hamilton DA, Bruning R, Markowitsch HJ, Kalla R, Darlington C, Smith P, Strupp M. Vestibular loss causes hippocampal atrophy and impaired spatial memory in humans. Brain 128: 2732–2741, 2005.
Brown JE, Frank JS. Influence of event anticipation on postural actions accompanying voluntary movement. Exp Brain Res 67: 645–650, 1987.[Web of Science][Medline]
Buchanan JJ, Horak FB. Emergence of postural patterns as a function of vision and translation frequency. J Neurophysiol 81: 2325–2339, 1999.
Buchanan JJ, Horak FB. Vestibular loss disrupts control of head and trunk on a sinusoidally moving platform. J Vestib Res 11: 371–389, 2001.[Medline]
Bunday KL, Reynolds RF, Kaski D, Rao M, Salman S, Bronstein AM. The effect of trial number on the emergence of the "broken escalator" locomotor aftereffect. Exp Brain Res 174: 270–278, 2006.[CrossRef][Web of Science][Medline]
Carpenter MG, Allum JH, Honegger F. Vestibular influences on human postural control in combinations of pitch and roll planes reveal differences in spatiotemporal processing. Exp Brain Res 140: 95–111, 2001.[CrossRef][Web of Science][Medline]
Cham R, Redfern MS. Changes in gait when anticipating slippery floors. Gait Posture 15: 159–171, 2002.[CrossRef][Web of Science][Medline]
Colebatch JG, Halmagyi GM. Vestibular evoked potentials in human neck muscles before and after unilateral vestibular deafferentation. Neurology 42: 1635–1636, 1992.
Creath R, Kiemel T, Horak F, Jeka JJ. Limited control strategies with the loss of vestibular function. Exp Brain Res 145: 323–333, 2002.[CrossRef][Web of Science][Medline]
Day BL, Severac Cauquiel A, Bartolomei L, Pastor MA, Lyon IN. Human body-segment tilts induced by galvanic stimulation: a vestibularly-driven balance protection mechanism. J Physiol 500: 661–672, 1997.
Dichgans J, Diener HC. The contribution of vestibulo-spinal mechanisms to the maintenance of human upright posture. Acta Otolaryngol 107: 338–345, 1989.[Medline]
Earhart GM, Sibley KM, Horak FB. Effects of bilateral vestibular loss on podokinetic after-rotation. Exp Brain Res 155: 251–256, 2004.[CrossRef][Web of Science][Medline]
Etienne AS, Maurer R, Saucy F. Limitations in the assessment of path dependent information. Behaviour 106: 81–111, 1988.
Fitzpatrick R, McCloskey DI. Proprioceptive, visual and vestibular thresholds for the perception of sway during standing in humans. J Physiol 478: 173–186, 1994.
Flanagan JR, Beltzner MA. Independence of perceptual and sensorimotor predictions in the size-weight illusion. Nat Neurosci 3: 737–741, 2000.[CrossRef][Web of Science][Medline]
Friedli WG, Cohen L, Hallett M, Stanhope S, Simon SR. Postural adjustments associated with rapid voluntary arm movements. II. Biomechanical analysis. J Neurol Neurosurg Psychiatry 51: 232–243, 1988.
Goldberg J, Peterson BW. Reflex and mechanical contributions to head stabilisation in alert cats. J Neurophysiol 56: 857–875, 1986.
Grunfeld EA, Morland AB, Bronstein AM, Gresty MA. Adaptation to oscillopsia: a psychophysical and questionnaire investigation. Brain 123: 277–290, 2000.
Guedry FE Jr. Psychophysics of vestibular sensation. In: Handbook of Sensory Physiology. Vestibular System. Psychophysics, Applied Aspects, and General Interpretations, edited by Kornhuber HH. New York: Springer-Verlag, 1974, vol. VI, pt. 2, p. 3–154.
Guerraz M, Yardley L, Bertholon P, Pollak L, Rudge P, Gresty MA, Bronstein AM. Visual vertigo: symptom assessment, spatial orientation and postural control. Brain 124: 1646–1656, 2001.
Haffenden AM, Schiff KC, Goodale MA. The dissociation between perception and action in the Ebbinghaus illusion: nonillusory effects of pictorial cues on grasp. Curr Biol 11: 177–181, 2001.[CrossRef][Web of Science][Medline]
Hollands MA, Marple-Horvat DE. Visually guided stepping under conditions of step cycle-related denial of visual information. Exp Brain Res 109: 343–356, 1996.[Web of Science][Medline]
Horak FB, Esselman PE, Anderson ME, Lynch MK. The effects of movement velocity, mass displaced and task certainty on associated postural adjustments made by normal and hemiplegic individuals. J Neurol Neurosurg Psychiatry 47: 1020–1028, 1984.
Horak FB, Shupert CL, Dietz V, Horstmann G. Vestibular and somatosensory contributions to responses to head and body displacements in stance. Exp Brain Res 100: 93–106, 1994.[Web of Science][Medline]
Huterer M, Cullen KE. Vestibuloocular reflex dynamics during high-frequency and high-acceleration rotations of the head on body in rhesus monkey. J Neurophysiol 88: 13–28, 2002.
Inglis JT, Shupert CL, Hlavacka F, Horak FB. Effect of galvanic vestibular stimulation on human postural responses during support surface translations. J Neurophysiol 73: 896–901, 1995.
Ito Y, Corna S, von Brevern M, Bronstein A, Rothwell J, Gresty M. Neck muscle responses to abrupt free fall of the head: comparison of normal with labyrinthine-defective human subjects. J Physiol 489: 911–916, 1995.
Keshner EA, Allum JH, Pfaltz CR. Postural coactivation and adaptation in the sway stabilizing responses of normal and patients with bilateral vestibular deficit. Exp Brain Res 69: 77–92, 1987.[CrossRef][Web of Science][Medline]
Krouchev NI, Kalaska JF. Context-dependent anticipation of different task dynamics: rapid recall of appropriate motor skills using visual cues. J Neurophysiol 89: 1165–1175, 2003.
Lewis RF, Tamargo RJ. Cerebellar lesions impair context-dependent adaptation of reaching movements in primates. Exp Brain Res 138: 263–267, 2001.[CrossRef][Web of Science][Medline]
Lund S, Broberg C. Effects of different head positions on postural sway in man induced by a reproducible vestibular error signal. Acta Otolaryngol 117: 307–309, 1983.[CrossRef]
Marigold DS, Patla AE. Strategies for dynamic stability during locomotion on a slippery surface: effects of prior experience and knowledge. J Neurophysiol 88: 339–352, 2002.
Markus EJ, Barnes CA, McNaughton BL, Gladden VL, Skaggs WE. Spatial information content and reliability of hippocampal CA1 neurons: effects of visual input. Hippocampus 4: 410–421, 1994.[CrossRef][Web of Science][Medline]
Martin JP. Tilting reactions and disorders of the basal ganglia. Brain 88: 855–874, 1965.
McNaughton BL, Chen LL, Markus EJ. "Dead reckoning," landmark learning, and the sense of direction: a neurophysiological and computational hypothesis. J Cogn Neurosci 3: 190–202, 1991.[CrossRef]
Mille ML, Johnson ME, Martinez KM, Rogers MW. Age-dependent differences in lateral balance recovery through protective stepping. Clin Biomech 20: 607–616, 2005.[CrossRef][Medline]
Mille ML, Rogers MW, Martinez K, Hedman LD, Johnson ME, Lord SR, Fitzpatrick RC. Thresholds for inducing protective stepping responses to external perturbations of human standing. J Neurophysiol 16: 192–198, 2003.
Nashner LM, Black FO, Wall C 3rd. Adaptation to altered support and visual conditions during stance: patients with vestibular deficits. J Neurosci 2: 536–544, 1982.[Abstract]
Nashner LM, Wolfson P. Influence of head position and proprioceptive cues on short latency postural reflexes evoked by galvanic stimulation of the human labyrinth. Brain Res 67: 255–268, 1974.[CrossRef][Web of Science][Medline]
Ossenkopp KP, Hargreaves EL. Spatial learning in an enclosed eight-arm maze in rats with sodium arsinilate-induced labyrinthectomies. Behav Neural Biol 59: 253–257, 1993.[CrossRef][Web of Science][Medline]
Pai Y-C, Wening JD, Runtz EF, Iqbal K, Pavol M. Role of feedforward control of movement stability in reducing slip-related balance loss and fails among older adults. J Neurophysiol 90: 755–762, 2003.
Patla AE, Niechwiej E, Racco V, Goodale MA. Understanding the contribution of binocular vision to the control of adaptive locomotion. Exp Brain Res 142: 551–561, 2002.[CrossRef][Web of Science][Medline]
Pavol M, Pai Y-C. Feedforward adaptations are used to compensate for a potential loss of balance. Exp Brain Res 145: 528–538, 2002.[CrossRef][Web of Science][Medline]
Peterka RJ, Benolken MS. Role of somatosensory and vestibular cues in attenuating visually induced human postural sway. Exp Brain Res 105: 101–110, 1995.[Web of Science][Medline]
Pijnappels M, Bobbert MF, Van Dieen JH. Changes in walking pattern caused by the possibility of a tripping reaction. Gait Posture 14: 11–18, 2001.[CrossRef][Web of Science][Medline]
Poucet B, Save E. Neuroscience. Attractors in memory. Science 308: 799–800, 2005.
Pozzo T, Berthoz A, Lefort T. Head kinematics during various motor tasks in humans. Prog Brain Res 80: 337–383, 1989.
Pozzo T, Levik Y, Berthoz A. Head and trunk movements in the frontal plane during complex dynamics equilibrium tasks in humans. Exp Brain Res 106: 327–338, 1995.[Web of Science][Medline]
Reynolds RF, Bronstein AM. The broken escalator phenomenon: aftereffect of walking onto a moving platform. Exp Brain Res 151: 301–308, 2003.[CrossRef][Web of Science][Medline]
Reynolds RF, Bronstein AM. The moving platform aftereffect: limited generalization of a locomotor adaptation. J Neurophysiol 91: 91–100, 2004.
Rinne T, Bronstein AM, Rudge P, Gresty MA, Luxon LM. Bilateral loss of vestibular function: clinical findings in 53 patients. J Neurol 245: 314–121, 1998.[CrossRef][Web of Science][Medline]
Salinas E. Fast remapping of sensory stimuli onto motor actions on the basis of contextual modulation. J Neurosci 24: 1113–1118, 2004.
Sasaki O, Asawa S, Katsuno S, Usami S, Taguchi K. Gait initiation in bilateral vestibular loss. Auris Nasus Larynx 28: 295–299, 2001.[CrossRef][Web of Science][Medline]
Semenov LV, Bures J. Vestibular stimulation disrupts acquisition of place navigation in the Morris water tank task. Behav Neural Biol 51: 346–363, 1989.[CrossRef][Web of Science][Medline]
Sparrow WA, Tirosh O. Gait termination: a review of experimental methods and the effects of ageing and gait pathologies. Gait Posture 22: 362–371, 2005.[CrossRef][Web of Science][Medline]
Traub MM, Rothwell JC, Marsden CD. Anticipatory postural reflexes in Parkinson's disease and other akinetic-rigid syndromes and in cerebellar ataxia. Brain 103: 393–412, 1980.
Tucker CA, Ramirez J, Krebs DE, O'Riley P. Centre of gravity dynamic stability in normal and vestibulopathic gait. Gait Posture 8: 117–123, 1998.[CrossRef][Web of Science][Medline]
Turner RS, Anderson ME. Context-dependent modulation of movement-related discharge in the primate globus pallidus. J Neurosci 25: 2965–2976, 2005.
Varraine E, Bonnard M, Pailhous J. Interaction between different sensory cues in the control of human gait. Exp Brain Res 142: 374–384, 2002.[CrossRef][Web of Science][Medline]
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ABSTRACT
INTRODUCTION
