1Department of Medical Physics and Biophysics, University of Nijmegen, 6525 EZ Nijmegen; 2Sint Maartenskliniek Research, 6500 GM Nijmegen; and 3Institute of Neurology, University Hospital Nijmegen, 6500 HB Nijmegen, The Netherlands
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ABSTRACT |
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Schillings, A. M., B.M.H. van Wezel, Th. Mulder, and J. Duysens. Muscular Responses and Movement Strategies During Stumbling Over Obstacles. J. Neurophysiol. 83: 2093-2102, 2000. Although many studies have investigated reflexes after stimulation of either cutaneous or proprioceptive afferents, much less is known about responses after more natural perturbations, such as stumbling over an obstacle. In particular, the phase dependency of these responses and their relation to the stumbling behavior has received little attention. Hence response strategies during stumbling reactions after perturbations at different times in the swing phase of gait were studied. While subjects walked on a treadmill, a rigid obstacle unexpectedly obstructed the forward sway of the foot. All subjects showed an "elevating strategy" after early swing perturbations and a "lowering strategy" after late swing perturbations. During the elevating strategy, the foot was directly lifted over the obstacle through extra knee flexion assisted by ipsilateral biceps femoris (iBF) responses and ankle dorsiflexion assisted by tibialis anterior (iTA) responses. Later, large rectus femoris (iRF) activations induced knee extension to place the foot on the treadmill. During the lowering strategy, the foot was quickly placed on the treadmill and was lifted over the obstacle in the subsequent swing. Foot placement was actively controlled by iRF and iBF responses related to knee extension and deceleration of the forward sway. Activations of iTA mostly preceded the main ipsilateral soleus (iSO) responses. For both strategies, four response peaks could be distinguished with latencies of ~40 ms (RP1), ~75 ms (RP2), ~110 ms (RP3), and ~160 ms (RP4). The amplitudes of these response peaks depended on the phase in the step cycle. The phase-dependent modulation of the responses could not be accounted for by differences in stimulation or in background activity and therefore is assumed to be premotoneuronal in origin. In mid swing, both the elevating and lowering strategy could occur. For this phase, the responses of the two strategies could be compared in the absence of phase-dependent response modulation. Both strategies had the same initial electromyographic responses till ~100 ms (RP1-RP2) after perturbation. The earliest response (RP1) is assumed to be a short-latency stretch reflex evoked by the considerable impact of the collision, whereas the second (RP2) has features reminiscent of cutaneous and proprioceptive responses. Both these responses did not determine the behavioral response strategy. The functionally important response strategies depended on later responses (RP3-RP4). These data suggest that during stumbling reactions, as a first line of defense, the CNS releases a relatively aspecific response, which is followed by an appropriate behavioral response to avoid the obstacle.
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INTRODUCTION |
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The pattern and timing of motor output during
human locomotion are determined by a mixture of influences, some
arising from neural circuits entirely within the CNS and others arising
from a variety of sensory afferents. The electromyographic (EMG)
responses in leg muscles occurring after stimulation of cutaneous and
proprioceptive afferents during locomotion have been described in many
studies (see reviews Dietz 1992; Duysens et al.
2000
). The amplitudes of the responses to such stimuli were
dependent on the phase (or time) of stimulation in the step cycle. For
instance, electrical stimulation of the human sural nerve yields
facilitation of the ankle flexor muscle tibialis anterior during early
swing, but leads to suppression when delivered during late swing
(reflex reversal) (Duysens et al. 1990
,
1992
, 1996
; Tax et al.
1995
; Van Wezel et al. 1997
; Yang and
Stein 1990
).
It has been assumed that the phase-dependent response modulation adapts
the responses in a functional way to the circumstances at various times
in the step cycle. Previous studies have suggested that the
phase-dependent responses and the corresponding joint angle changes
following selective cutaneous stimulation might be functionally
relevant in stumbling reactions (Van Wezel et al. 1997;
Zehr et al. 1997
). However, the EMG and the accompanying kinesiologic responses occurring after more realistic perturbations (e.g., stumbling over an object, such as a doorstep or a paving stone)
have not been studied very extensively. Hence it is of importance to
describe the compensatory reactions during stumbling and to study the
functional significance of the observed responses.
To evoke natural stumbling reactions in an experimental setting,
mechanical perturbations were induced by an obstacle suddenly rising
above the ground and perturbing the forward swinging foot of subjects
walking on a walkway (Eng et al. 1994). When a
perturbation occurred in early swing, an "elevating strategy" was
performed, during which the flexion angles of the hip, knee, and ankle
of the swinging leg increased after the perturbation. In contrast, during late swing, mostly a "lowering strategy" was performed, in
which the foot of the swinging leg was rapidly lowered to the ground
causing a shortened step length. The reflex responses in the leg
muscles during these recovery strategies had latencies varying from 60 to 140 ms.
It cannot be determined whether the responses described above were
mainly related to the phase of perturbation in the step cycle or to the
strategy performed. Hence a method was developed in which the
perturbations can be induced in all parts of the swing phase, including
mid swing, in which both strategies could occur (Schillings et
al. 1999a), allowing for a comparison of the two strategies in
the same phase. Perturbations are caused by an obstacle put on a
treadmill, which unexpectedly obstructs the forward swinging foot
(Schillings et al. 1996
). Because of its weight (2.2 kg), the obstacle has a considerable impact on the ongoing movement of
the forward swinging leg. A previous study showed that after
perturbations with this obstacle, short-latency stretch reflexes form a
consistent part of the stumbling reactions (Schillings et al.
1999b
). The aim of the present study is to describe the
responses with longer latencies and the coordination of leg muscle
activity compensating for this natural unexpected perturbation. The
questions whether these responses are dependent on the phase of
perturbation in the step cycle and/or whether the responses are
functionally related to the stumble strategy performed (elevating or
lowering) will be discussed.
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METHODS |
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Eight healthy subjects (5 male, 3 female) between 20 and 47 yr of age (mean age 27) participated in the experiment. They had no known history of neurological or motor disorder. The experiments were carried out in conformity with the declaration of Helsinki for experiments on humans. All subjects gave informed consent, and the study was approved by the local ethical committee.
Experimental setup
A detailed account of the experimental setup can be found in
Schillings et al. (1996). While subjects walked on a
treadmill (speed, 4 km/h), an obstacle (length, width, and height,
40.0, 30.0, and 4.5 cm, respectively; weight, 2.2 kg) was held by an electromagnet above the treadmill in front of the subject (Fig. 1A). To induce perturbations,
the obstacle was dropped on the belt, thereby unexpectedly obstructing
the forward sway of the left (ipsilateral) leg. Release of the obstacle
occurred at a predetermined delay after ipsilateral or contralateral
heel strike. In the thin flexible shoes, the toes were covered with a
piece of cotton to protect them. A pressure-sensitive strip attached to
the front of the obstacle measured the time at which the foot hit the
obstacle. The subjects wore a pair of glasses, which blocked downward
sight (and thus blocked the view of the obstacle). Earplugs eliminated
most of the sound perception of the obstacle landing on the treadmill.
In addition, the sound was masked by music through headphones. Further,
to avoid that the subjects could feel the vibration of the obstacle
landing on the treadmill, a heavy metal object was put on the treadmill
at irregular intervals (imitating the landing of the obstacle). As a
result of these measures, subjects were not able to perceive the
obstacle before the collision with the foot. Subjects were instructed
to keep the same position on the treadmill before the perturbation, but
after the collision they were free to react without restrictions. The
subjects wore a safety harness, fixed to a safety brake on the ceiling
that would hold the subject and stop the treadmill in case a subject should start to fall. In practice, this never occurred because none of
the subjects really started to fall. The harness was loosely suspended
and did not provide extra stability during the experiment.
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Data sampling
Bipolar surface electromyogram (EMG) activity of the biceps femoris (BF), rectus femoris (RF), tibialis anterior (TA), and soleus (SO) of both legs was measured. Laterally placed goniometers were used to measure the joint angles of the knee and ankle of the ipsilateral leg. Thin insole foot switches measured foot contact with the treadmill. Data were sampled in a time interval starting 100 ms before triggering the electromagnet and lasting for 2,100 ms. For the control trials the same intervals were sampled, but no obstacle was dropped after the trigger. The EMG was (pre-)amplified, high-pass filtered (>3 Hz), full-wave rectified, low-pass filtered (<300 Hz), AD-converted (500 Hz), and stored on hard disk along with the signals of the goniometers, foot switches, and pressure-sensitive strip. In practice, this sampling rate appeared to be sufficiently high. Increasing the sampling rate to 1,000 Hz did not lead to appreciable improvement of the signals for the purpose of this study. In addition, the subjects were recorded on video (25 Hz).
Experimental protocol
Each experiment consisted of three parts. Part one (5 min) consisted of the registration of unperturbed walking. This control condition enabled to check whether the presentation of the obstacles (in following parts) affected baseline-walking characteristics (because of possible effects due to anticipation or fear of stumbling).
In part two (20 min), the effect of the timing of the perturbation on
the behavioral response "strategies" (elevating or lowering) was
studied for a wide variety of delays after onset of swing. For this
purpose the computer triggered the electromagnet to drop the obstacle
on the treadmill after fixed delays (0, 40, 80, ... , 600 ms)
after heel strike. Each delay condition was randomly applied only once.
A perturbation-free period of at least 10 s was taken between two
succeeding trials to be sure that the subject was walking normally
again at the time of the next perturbation. The normal walking pattern
was usually regained within approximately two step cycles. The
behavioral responses were classified in two categories (Fig.
2) on the basis of video analysis. A
response was labeled as "elevating strategy" (Eng et al.
1994) when the ipsilateral foot was lifted over the obstacle
during the perturbed swing. The stumble response was classified as
"lowering strategy" when the foot was first placed on the treadmill
and then lifted over the obstacle.
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In part three (30 min) stumbling reactions were repeatedly and randomly introduced during early swing (5-25%, time of obstacle contact with respect to control swing duration), mid swing (30-50%), and late swing (55-75%) to construct averages. On average eight trials (minimal 5 trials) were obtained for each phase of perturbation. The responses during these perturbed cycles were compared with unperturbed control trials obtained in between the perturbation trials (perturbation-free period between trials >10 s).
Data analysis
The stumble responses of each subject occurring in the same
phase of the step cycle were averaged. In addition, the corresponding control trials were averaged. Then the averaged control activity was
subtracted from the averaged stumbling trials. To quantify the
amplitudes of the responses, the mean EMG activity was calculated in
the period between the beginning and end of the response. For this
purpose, windows were set around the individual response peaks
occurring within the first 200 ms (see Fig. 1B). To enable a
proper intersubject comparison of the response amplitudes, the resulting data of each muscle were normalized with respect to the
maximal EMG activity during the control step cycles. The normalized responses of all subjects were averaged. This type of analysis was
performed on four response peaks, namely RP1 (latency ~40 ms), RP2
(latency ~75 ms), RP3 (latency ~110 ms), and RP4 (latency ~160
ms, see Fig. 1B). The RP1 responses have already been
described in a previous publication (Schillings et al.
1999b) and are only included in the present paper as a basis
for comparison with the later responses. The Wilcoxon matched-pairs
signed-rank test was used to test whether the response amplitudes
during stumbling were significantly different from the control EMG
activity. The Friedman two-way ANOVA was used to test whether the
subtracted response amplitudes were different for the three phases of
perturbation (8 triples of comparison: 8 subjects, 3 phases;
P < 0.05). The Wilcoxon rank sum test was used to
compare the response amplitudes of the two strategies in mid swing
(P < 0.05). The choice for nonparametric tests was
based on the low number of averages that were compared (8 subjects).
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RESULTS |
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Normal walking
To check whether the normal walking pattern was affected by the knowledge that a stumble over an obstacle could occur, the normal walking pattern measured in between the stumble trials (control trials of part 3) was compared with the normal walking pattern measured during unperturbed walking (part 1, see METHODS). None of the subjects clearly changed his/her normal walking pattern during the stumble experiment.
Strategies in general
The choice for the behavioral strategy depended on the timing of the perturbation in the step cycle. This is shown for all subjects in Fig. 2C (data of 2nd part of the experiment). When perturbations were caused in early swing (5-25%, time of obstacle contact with respect to control swing duration), all subjects showed the elevating strategy (see Fig. 2A). After perturbations in late swing (55-75%), all subjects showed the lowering strategy (see Fig. 2B). In mid swing (30-50%) both strategies could occur. It can be seen that some subjects showed a distinct transition in choice from elevating to lowering strategy (subjects 3-5, 7, and 8, Fig. 2C), whereas others showed a zone of overlap of the two strategies (for example, 49-54% in subject 2; Fig. 2C). For each subject the transition point from the elevating to the lowering strategy was defined as the time for one-half the interval between the last elevating and the first lowering strategy occurrences. This transition point varied for all subjects from 35% into the swing phase (subject 7, Fig. 2C) to 52% (subject 2, Fig. 2C) and was on average 44 ± 5% (mean ± SD, n = 8 subjects).
Passive joint movements during both the elevating and the lowering strategy
During both the elevating and the lowering strategy, the collision of the foot with the obstacle induced small passive movements in the ipsilateral knee and ankle joint. These movements are considered to be passive because they start before the occurrence of the first EMG responses in the muscles that could influence these joints. As seen in both the elevating strategy of Fig. 3 and the lowering strategy of Fig. 4 the ankle is first plantar flexed due to the collision (amplitude for all subjects between 1 and 10°) with a latency of ~15 ms, whereas the first responses in ipsilateral soleus and tibialis anterior (iSO and iTA) occurred with a latency of ~40 ms. Second, the knee was flexed due to the collision with a latency of 46 ms and an amplitude of 13° during the elevating strategy (see Fig. 3) and 34 ms and 9° during the lowering strategy (see Fig. 4). In the muscles ipsilateral biceps femoris and rectus femoris (iBF and iRF), which could influence the knee joint angle, no responses were observed before this early flexion.
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Responses during the early swing elevating strategy
After the collision with the obstacle, active ipsilateral knee and ankle flexion assisted the elevation of the swing foot to step over the obstacle. The active knee flexion started ~160 ms after perturbation onset (see sudden increase of the knee flexion in Fig. 3; mean latency of active knee flexion for all subjects was 169 ± 47 ms). The maximum knee flexion reached during the elevating swing was considerably larger than during normal swing (96 vs. 58° for the subject of Fig. 3). The upper leg muscles typically showed first a large iBF burst (latency, 64 ms; Fig. 3) assisting knee flexion, followed by a large iRF burst (latency, 154 ms; Fig. 3) extending the knee before touch down.
The ankle dorsiflexion started 90 ms after perturbation, and the maximum dorsiflexion reached during the movement over the obstacle was ~17° larger than the maximum dorsiflexion during the unperturbed swing (Fig. 3). Facilitatory iTA responses (latency, ~75 ms) assisted this dorsiflexion. In two of eight subjects, suppressive iTA responses (latency, ~80 ms; suppressive response: the response EMG activity is lower than the control EMG activity) preceded the main facilitatory responses in iTA (latency, 112 and 214 ms). This suppression possibly had the function to allow for ankle plantar flexion to avoid that the foot got hooked behind the obstacle. The change in foot trajectory caused a lengthening of the ipsilateral swing and concomitant of the contralateral stance with on average 128 ± 30 ms and 81 ± 41 ms, respectively (see Table 1).
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Contralaterally, a large burst of activity in the cBF appeared with a
latency of 66 ms (subject of Fig. 3) after the perturbation. Because,
during stance the biarticular BF serves as a hip extensor (Winter 1987), the cBF response could contribute to
stabilizing the upper body by the standing leg after perturbations of
the swinging leg, as was also suggested by other authors (Dietz
et al. 1986b
; Eng et al. 1994
). In the other
contralateral muscles (cRF, cTA, and cSO), the responses were too
variable or small to give a detailed description.
Responses during the late swing lowering strategy
During the lowering strategy, the foot was quickly placed on the treadmill by shortening the forward sway and slightly extending the knee. The knee extension needed to place the foot was small in comparison with the knee extension before touch down during normal walking (see Fig. 4). This was first, because the foot was already close to the treadmill at the time of the perturbation (~2-4 cm above the treadmill) and second because the position of the foot during the landing (forefoot or flat foot landing) was different from normal (heel landing). The knee extension started 94 ms after perturbation and was presumably related to the large iRF burst (latency, 62 ms; see Fig. 4). For all subjects, the iRF burst occurred on average 53 ± 36 ms before the average foot placing in late swing. In three of eight subjects, responses in iBF occurred approximately simultaneously with the responses in iRF (see Fig. 4). In the other five subjects the onset of the main responses in the iBF occurred ~25 ms later than the onset of the main iRF burst. The iBF activity could slow down the forward swing in preparation of the early foot placement (hip joint angles were not measured).
In the lower leg muscles, first short-latency responses occurred with a
latency of 40 ms in both iTA and iSO, possibly transiently enhancing
ankle-joint stiffness (see Schillings et al. 1999b). Subsequently, a large activity burst was observed in iTA (latency, 66 ms after perturbation; Fig. 4), which could participate in the ankle
dorsiflexion (latency, ~90 ms; Fig. 4). A large iSO burst appeared
with a latency of 111 ms and was well timed to take up body support
during the preliminary stance phase. This sequence of iTA and iSO
responses was observed in seven of eight subjects and could support an
initial movement away from the obstacle (iTA activity and ankle
dorsiflexion) followed by foot placement (iSO activity). The mean
latency of the premature placing off all subjects was 125 ± 35 ms
after the collision. The ipsilateral swing phase and the contralateral
stance phase were shortened with, on average, 35 ± 25 ms and
62 ± 29 ms (Table 1), respectively. Contralaterally, the main
consistent responses occurred in the cBF, which showed a large response
with a latency of 62 ms (subject of Fig. 4).
Responses during mid swing
After mid swing perturbations (30-50% of swing), both strategies could occur. For the mid swing elevating strategy, the major characteristics were the same as for the early swing elevating strategy (lengthening of swing phase duration, increased knee flexion and ankle dorsiflexion, first iBF activation then iRF activation, large iTA activity). However, some small differences could be observed. For example, the duration of the perturbed swing was lengthened in both phases, but the swing phase duration increased on average 55 ± 42 ms more in mid swing than in early swing (average of subjects 1-5, see Table 1). Comparing the mid swing lowering with the late swing lowering strategy, it was found that the foot was placed later after mid swing (mean latency, 246 ms; subjects 5-7) than after late swing perturbations (mean latency, 125 ms; subjects 1-7).
The differences between responses in early and late swing could be related to the strategy performed. However, some of these differences may be related more to variations in the timing of the perturbation within the step cycle ("phase dependency"; see INTRODUCTION) than to changes in strategy. This complication does not occur for some of the data related to mid swing perturbations. Three subjects performed an elevating strategy in one trial, whereas a lowering strategy was used in another trial, despite the same timing of the perturbation. Hence in these cases it was possible to study which parts of the responses were strictly coupled to either lowering or elevating strategy. In Fig. 5 the signals of an elevating (thin lines) and a lowering strategy (heavy lines) occurring in the same phase are compared.
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The knee goniometer signals of both the elevating and the lowering strategy started deviating from the control (- - -) in the direction of knee flexion with a latency of 60 ms. This knee flexion increased during both strategies till ~150 ms. After this common movement, the knee flexed further to lift the foot over the obstacle during the elevating strategy, whereas the knee started to extend to place the foot on the ground during the lowering strategy.
It was observed that the responses in the first 100 ms after the perturbation were similar for both strategies (Fig. 5). In this interval, the most obvious responses were observed in iTA with a latency of ~70 ms in both the elevating and the lowering strategy. In the period after 100 ms, the first difference between the two strategies occurred in iBF, namely after 104 ms (subject of Fig. 5). In this subject, the iBF (knee flexor) showed a burst, which was followed by a burst in the iRF (latency, 148 ms; Fig. 5) during the elevating strategy. In contrast, during the lowering strategy the iRF was activated (latency, 136 ms; Fig. 5) before the iBF. Similar results were observed in two other subjects. In each case there was a common initial movement in the knee (mean onset of difference in knee trajectory was 136 and 186 ms, respectively). Correspondingly, these two subjects showed a common pattern of EMG responses during the first 100 ms for the two strategies.
Delayed lowering strategy
In the previous section it was shown that the EMG responses during the first 100 ms did not determine the ensuing behavioral response (strategy). Later EMG bursts (between 100 and 150 ms) were characteristic for the strategies, but the question remains how predetermined these later responses were. If these responses were completely defined from the moment of collision onward, a fixed response pattern could be expected and no changes should occur during the course of this reaction. The example shown in Fig. 6, however, illustrates that this is not the case. In this exceptional trial, the subject started with an elevating strategy after the early swing perturbation, but the obstacle stuck to the toes and the subject was unable to clear the obstacle. Instead, he extended the knee (latency, 236 ms) and placed the foot on the treadmill (latency, 416 ms) without clearing the obstacle ("delayed lowering"). In the succeeding swing phase the foot was lifted over the obstacle. In this situation, in which the reaction was in fact a mixture of the two strategies, the EMG responses of the two strategies (normal elevating and delayed lowering) showed similar responses till ~120 ms after perturbation. From then on the iRF showed a large response during the delayed lowering strategy that was absent during the elevating strategy. This iRF burst occurred 116 ms before the onset of the knee extension, which resulted in foot placement.
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Modulation of the response amplitudes
In the EMG traces the main responses of the stumbling reactions occurred with four peaks (RP1-RP4) within the first 200 ms. To study the amplitudes of the EMG peaks, time windows were set in these four periods, and the mean EMG activity was calculated within these time windows (see Table 2).
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In Fig. 7, the amplitudes of the mean
normalized control and response activity of all subjects are shown
during early swing elevating (n = 8 subjects), mid
swing elevating (n = 5), mid swing lowering
(n = 3), and late swing lowering reactions
(n = 8). Below the bars is indicated whether the pooled
average response amplitudes of all subjects were significantly
different from the average control activity (*) or not ().
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Representing the data of all subjects together (Fig. 7) enabled us to study phase and strategy dependency for the data of all subjects. First, to study whether different response peaks are phase dependent, the responses occurring in the three phases [early swing (ES) vs. mid swing (MS) vs. late swing (LS), Fig. 7] were compared, irrespective of the strategy performed. Almost all responses were phase-dependent as determined with the Friedman two-way ANOVA (P < 0.05). The only responses that did not show a significant phase effect were the RP2 of iSO, RP3 and RP4 of iBF, and RP1 and RP2 of iRF.
In general for all muscles, the response amplitudes were not strictly related to the background EMG activity (see Fig. 7). For a clear example, compare the response amplitudes of the iTA RP3 that showed largest responses in mid swing, when the background activity was lowest, and the smallest responses in late swing, when the background activity was largest.
Second, to study whether the responses are strategy dependent, the responses occurring during the two strategies [elevating (el) vs. lowering (lo), Fig. 7] in mid swing were compared. As expected on the basis of the observation of Fig. 5, no significant differences in the RP1 and RP2 amplitudes between the elevating and the lowering strategy in mid swing were observed (Wilcoxon rank sum test). The amplitudes of the late responses (RP4) in iSO were significantly related to the strategy. A general characteristic of the late iSO responses in mid swing was that they were small during the elevating strategy and large during the lowering strategy.
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DISCUSSION |
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The present study demonstrates that stumbling over a rigid object
on a treadmill induces a sequence of EMG and behavioral responses. The
elevating and lowering stumbling strategies presently described show
basic similarities with previously described stumbling reactions, which
were induced by more flexible obstacles (Eng et al.
1994). However, some differences were observed. First, the
short-latency stretch reflexes in the ipsilateral leg muscles were not
present after perturbations with the flexible metal strip (Eng
et al. 1994
; Rietdyk and Patla 1998
). The larger
impact of the collision, influenced by the weight and flexibility of
the obstacle, in the present study might be the cause of this
difference. The occurrence of short-latency stretch reflexes in both
flexors and extensors can be understood because these responses are
caused by a sudden jar through the ipsilateral leg due to the collision of the foot with the obstacle (see Schillings et al.
1999b
).
Second, in the late swing lowering strategy, the quick foot placement
after the perturbation was accompanied by iTA and iRF facilitations
(latency, ~75 ms). Eng et al. (1994) described
suppressive responses during the same period in these muscles, and they
speculated that this permitted gravity to assist the lowering of the
foot. Again, the observed difference might be related to the
characteristics of the perturbing obstacle. With the presently used
obstacle, subjects tried to avoid that they would step on the obstacle. So they tended to move away from the obstacle (iTA activity) before the
quick touchdown assisted by iRF. In the study of Eng et al. (1994)
, there was no chance to step on the obstacle, because
the flexible metal strip disappeared directly after the collision (the
strip turned to a flat position). Hence it was of less importance to
actively control the quick foot placement.
Third, Eng et al. (1994) described a "reaching
strategy" after late swing perturbations, whereas in the present
study this strategy was not observed. During this strategy, the foot is
directly lifted over the obstacle, primarily due to hip flexion rather than knee flexion. Apparently the reaching strategy was avoided in the
present study because it requires considerably more hip flexion to
cross a long obstacle than a short one.
Phase dependency of the EMG responses
Differences in response amplitudes in the three phases (early,
mid, and late swing) could either be due to changes in stimulation or
to modulation of reflexes by the nervous system. Changes in the
intensity of the collision of the foot with the obstacle could influence the amplitude of the EMG responses. The impact of the collision on the foot is mainly dependent on the horizontal toe velocity, which varies during the swing phase. The horizontal toe
velocity is ~1.5 times lower in early swing than in either mid or
late swing (Winter 1992). If the amplitudes of the
responses were completely determined by the impact of the collision,
one would always expect the smallest responses in early swing. This was
not the case. For example, the RP2 response of iBF was largest in early
swing and smallest in late swing (see Fig. 7). Furthermore, one would
expect about equal amplitudes in mid and late swing. However, different
response amplitudes were often observed in these two phases. Another
possible cause for the amplitude modulation observed could be that the
responses were related to the background activity (Matthews
1986
). However in general, there was no strict relation between
reflex amplitude and background activity. This leaves the possibility
that premotoneuronal mechanisms might contribute to the phase-dependent
modulation of the response amplitudes.
Initial common reaction of the two strategies in mid swing
The occurrence of the two strategies after perturbations in mid
swing offered the unique possibility to study which parts of the
responses were strictly coupled to either the lowering or the elevating
strategy. Both strategies in mid swing started with the same EMG
responses during the first 100 ms after the perturbation. Neither the
RP1 nor the RP2 responses predicted the choice for one of the two
strategies. Only the RP3 and RP4 responses (>100 ms) of some muscles
(iBF and iSO) correlated well with the behavioral strategy performed
(e.g., see the large iBF RP3 during the mid swing elevating strategy in
Fig. 5, and see the large iSO RP4 during the mid swing lowering
strategy in Fig. 7). The initial common reaction of the two strategies
in mid swing first consists of the short-latency stretch reflex (RP1),
which might contribute to a temporary stiffening of the joint
(Schillings et al. 1999b). Second, it involves the RP2
response in muscles such as iTA. The iTA RP2 activation could
contribute to the observed ankle dorsiflexion to move the foot away
from the obstacle. The same initial reaction of the two strategies
possibly provides the CNS sufficient time to integrate information
obtained by various sensory receptors (Brooke et al.
1997
; Dietz 1992
; Jankowska 1992
) and supraspinal sources (see review Dietz 1992
) to make
an appropriate decision about the final behavioral strategy.
Behavioral responses are not predetermined at the time of perturbation
The occurrence of both behavioral strategies in mid swing
indicates that the decision about the final behavioral strategy is not
tightly linked to the time of impact. Further support for this idea
comes from the example of a lowering strategy performed when a
subject's foot got hooked behind the obstacle during an early swing
perturbation. The foot was first lifted as in the elevating strategy
(initial reaction plus onset of the elevating strategy), but because
the obstacle stuck to the toes (continuing mechanoreceptor feedback
information), the subject decided to place the foot on the ground again
and finally completed a delayed lowering strategy. Apparently, on-line
afferent information during the stumble response is integrated in the
final reaction and can be used to adjust the strategy to the demands of
the moment. In the example of the delayed lowering strategy, the
earliest adaptive response to extend the leg for the foot placement on
the treadmill was observed after 120 ms in the iRF. This is too early
to be a voluntary reaction, because the earliest EMG changes during voluntary reactions occur after ~150 ms. For example, in a study of
Hase and Stein (1998), in which subjects were instructed
to stop walking as soon as they got a cue by electrical stimulation of
the superficial peroneal nerve, the earliest voluntary changes in EMG
activity of leg muscles occurred 150-200 ms after stimulation.
The idea that a corrective response can be adjusted en route has found
support in some earlier observations as well. While subjects were
walking on a treadmill, Dietz et al. (1986a) applied a
holding impulse by a cord attached to the swinging leg, which was
followed by a second perturbation, i.e., a treadmill deceleration. On
the basis of their results, they suggested that the first part of the
compensatory reaction is released as an immutable pattern within the
spinal cord. In contrast, the later part of the response (in the order
of 120 ms after the 1st perturbation, see their Fig. 2) can be modified
by external factors and adjusted to the actual nature of the task.
Furthermore, the present data are in line with the finding of bimodal
responses in subjects who were tripped while they were taking a single
step forward (Rietdyk and Patla 1998). In this situation, the perturbation always induced an initial change in ankle
trajectory (elevation of the ankle), which could or could not be
followed by a second elevation of the ankle. Thus the initial response
could be followed by a later correction, which resulted in an
enhancement of the initial movement. In the present study it was
demonstrated that the later correction is not always an enhancement of
the first movement as observed in the study of Rietdyk and Patla
(1998)
, but can also be a reversal of the first movement.
Origin of the responses
On the basis of several studies on cats, it has been assumed that
the responses observed during "stumbling corrective reactions" (Forssberg 1979) are mainly cutaneous in origin
(Forssberg 1979
; Forssberg et al. 1975
,
1977
; Prochazka et al. 1978
; Wand
et al. 1980
). In addition, for humans it has been suggested
that the medium-latency EMG responses and the accompanying joint angle changes after electrical cutaneous stimulation might be functionally relevant in the context of stumbling reactions (Van Wezel et al. 1997
; Zehr et al. 1997
; see, however,
Duysens et al. 1992
). There are indeed some similarities
between the modulation of medium-latency cutaneous responses and the
RP2 responses observed during stumbling. For example, the iTA
facilitation (RP2) with ankle dorsiflexion observed during the early
swing elevating strategy was also observed after sural nerve
stimulation in early swing (Duysens et al. 1992
; Van Wezel et al. 1997
). However, cutaneous stimulation
evoked suppression of the iTA activity in late swing (Duysens et
al. 1990
; Yang and Stein 1990
; Zehr et
al. 1997
), whereas the present mechanical perturbation evoked
facilitatory iTA (RP2) responses. Hence these differences indicate that
the RP2 observed during stumbling in humans cannot be fully attributed
to cutaneous responses (although we cannot rule out the possibility
that cutaneous responses after mechanical perturbations are different
from cutaneous responses after electrical stimulation).
Alternatively, proprioceptive afferents might contribute to the RP2
responses observed. Medium-latency stretch responses (M2 or MLR) in leg
muscles with latencies similar to the RP2 responses (~75 ms) have
been described by many authors after joint rotations during various
conditions (Fellows et al. 1993; Nielsen et al. 1998
; Schieppati and Nardone 1997
;
Schieppati et al. 1995
; Sinkjaer et al.
1988
; Toft et al. 1989
). Although some authors
suggested that Ia afferents could mediate medium-latency stretch
reflexes in leg muscles (Berardelli et al. 1982
;
Fellows et al. 1993
), most evidence points in the
direction of a contribution of muscle proprioceptive group II afferents
in these responses (see Corna et al. 1995
; Dietz
1992
; Nardone et al. 1996
; Nielsen et al.
1998
; Schieppati and Nardone 1997
;
Schieppati et al. 1995
). Even activations of Ib
afferents cannot be excluded because of the strong impact of the
obstacle (for review see Duysens et al. 2000
). The
contribution of vestibular afferents in the RP2 responses during
stumbling is probably small because vestibular responses have much
smaller amplitudes than somatosensory responses (Horstmann and
Dietz 1988
).
For the short-latency responses, there is little doubt that these are
spinal stretch reflexes mediated by Ia afferents (see Schillings
et al. 1999b). The responses with longer latencies (RP2-RP3)
during stumbling could follow both spinal or supraspinal neural
pathways. In principle, these responses might be polysynaptic EMG
responses of spinal origin and could be related to activation of slower
conducting afferents (see review Dietz 1992
). However, the latency of these responses is also long enough to be compatible with long-loop reflexes through the cortex (Christensen et al. 1999
; Nielsen et al. 1997
; Petersen et
al. 1998
; Pijnappels et al. 1998
). Although the
same neural pathways could contribute to the RP4 responses, these
responses are likely to be at least partly under voluntary control
because they have latencies above the voluntary reaction time of ~150
ms in leg muscles.
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ACKNOWLEDGMENTS |
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We thank P.H.J.A. Nieuwenhuijzen and H.W.A.A. Van de Crommert for help with the experiments and the analysis software. We also acknowledge G. Windau for developing the software and A. M. Van Dreumel and J.W.C. Kleijnen for technical assistance.
This study was supported by the Dutch Science Foundation (NWO).
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FOOTNOTES |
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Address for reprint requests: A. M. Schillings, Dept. of Medical Physics and Biophysics, University of Nijmegen, P.O. Box 9101, NL-6500 HB Nijmegen, The Netherlands.
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 9 August 1999; accepted in final form 13 December 1999.
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REFERENCES |
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