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1Department of Rehabilitation Medicine, Radboud University of Nijmegen Medical Center; and 2Sint Maartenskliniek, SMK-Research, Nijmegen, The Netherlands
Submitted 22 November 2006; accepted in final form 19 August 2007
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ABSTRACT |
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INTRODUCTION |
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; Patla 1993, 1996)? Most studies on sudden induced ankle inversions have investigated reactive control using responses after the perturbation in subjects who were standing (i.e., Konradsen and Ravn 1991a; Lynch et al. 1996). The peroneal muscles have been studied most extensively. Latencies for the early responses were around 50 ms (Konradsen et al. 1997), whereas later responses had a latency of 
100 ms (Lynch et al. 1996). However, inversion traumas do not occur during standing at rest (Lynch et al. 1996) but during more dynamic conditions like walking, running, or jumping. Both in vitro as in vivo studies have found evidence that the ankle stability increases with loading of the ankle (Scheuffelen et al. 1993; Stormont et al. 1985). According to Stormont et al. (1985) ankle instability occurs during the initial loading and terminal unloading (as occurs during walking at onset and termination of the support phase) and not once the ankle is fully loaded. Studying ankle instability during the loading acceptance of the stance phase of walking might give new insight in the control of ankle stability in situations where the foot is inverted. In a previous study we investigated ankle inversions during landing after a jump (Grüneberg et al. 2003). Main findings in this study were that both a short-latency response (SLR; latency of 
40 ms) and late-latency response (LLR; latency of 90 ms) were observed in a variety of leg muscles but that the LLR of the peroneal muscles was by far more prominent. The LLR response was observed after the inversion movement was completed. During jumping the inversion of the landing surface occurs very rapidly and it is possible that during walking the inversion is slower so that LLRs are timelier. Furthermore, the responses found during standing or jumping can differ from the responses found during gait because responses are known to be task dependent (Duysens et al. 1993; for review see Zehr and Stein 1999).
So far, however, little is known about ankle inversions during walking. Linford et al. (2006) used a runway consisting of trapdoors allowing an ankle inversion of 30°. They found peroneus longus reflex activations with a latency of 63 ms after onset of inversion but it is unclear whether this response occurred during or after the inversion, although the activity before touchdown was not studied. In contrast, the anticipatory activity was the focus of interest of Forestier and Toschi (2005). They used a mechanical device, mounted under the heel of the shoe, to introduce subtalar joint destabilization during gait (inversion and plantar flexion movement of the ankle). They found that the walking pattern was altered and that muscles counteracting the upcoming lengthening [e.g., the peroneal muscles and the tibialis anterior (TA)], were activated just before or at touchdown, whereas other muscles, such as the gastrocnemii, showed no significant change. In the latter experiments the shoe was unstable but the question remains whether similar anticipatory activity is seen when the surface is unstable.
To answer this type of remaining questions, in the present experiments ankle inversion was introduced by having subjects step on a box with a trap door, which could tilt (Nieuwenhuijzen et al. 2002). How do subjects adjust their step knowing that they must land on a surface that has the potential to invert the foot? To study this question one can compare such "potentially inverting" trials with those in which the subject knows that there will be no such inversion. Of special interest is the question whether subjects preactivate those muscles, in anticipation of the expected stretch during the forthcoming inversion movement (e.g., the peroneal muscles). Such preactivation would make sense because it overcomes the problem of electromechanical delay. Furthermore it is known that stretching preactivated muscles may result in larger spindle responses (Nichols and Cope 2004).
An equally important second question is whether the responses following the onset of the perturbation are affected by knowledge about the inverting surface. Because of ethical objections the use of completely unexpected induced ankle inversions were avoided. Still the first trial was always somewhat unexpected even when subjects were warned that an inversion could occur. Thus first-trial effects are to be expected, similar to those encountered after slips (Marigold and Patla 2002) or after steps on surfaces with unexpected stiffness (Marigold and Patla 2005; Nakazawa et al. 2004). Do such trials induce "startle-like" responses (large-amplitude LLR responses in antagonistic leg muscles)? If so, are these responses smoothly incorporated into the locomotor program as was seen with auditory startle (Nieuwenhuijzen et al. 2000, 2006)? It makes sense to induce a brief "freezing" when one encounters a novel type of perturbation. As one becomes more familiar with the stimulus, the responses usually decrease (habituation) with the exception of those that are of special significance for the perturbation. Is this habituation the same for SLR and LLR responses? Using repeated stretches of the wrist or thumb, Rothwell et al. (1986) found that LLR habituated strongly whereas SLR was unaffected. A similar discrepancy was previously noted for exteroceptive reflexes of short and long latencies (Desmedt and Godaux 1976).
Finally, most inversion studies have focused on the peroneal muscles and few data are available about the role of the other lower leg muscles in ankle inversions. However, previous work (Grüneberg et al. 2003) indicated that such other muscles could also contribute to the responses under particular circumstances. Therefore the present study concerns EMG responses in six lower leg muscles after ankle inversions during walking. In summary, the current study was undertaken to answer the question whether foot inversion during walking induces responses comparable to those seen in other tasks (standing, jumping) with respect to habituation characteristics, latency, amplitude, and type of muscles recruited. In addition the question is asked how mental set (anticipation of potential inversion) affects such responses.
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METHODS |
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The method used to elicit the inversion is extensively described in Nieuwenhuijzen et al. (2002). Only a summary of this method will be given in the present paper. At a preprogrammed delay after a left heel strike, an electromagnet released a custom-made box [35 x 20 x 10 cm (length x width x height)] on the treadmill in front of the left foot of the subject (Fig. 1). The delay ensured that the subjects could step on the box without changing their cadence of walking. To help subjects maintain the same anterior–posterior position, visual feedback about the position of the back of the body with respect to the back of the treadmill was given using a series of light-emitting diodes connected to a position-measuring device based on sonar. The top of the box contained a trap door that could tilt 25° with respect to the horizontal (during stimulus trials) or did not tilt (during control trials). Two types of experiments were performed. First, 10 control trials (no tilting of the trap door; stepping on 10 cm height) were measured. Before this experiment, the subjects were told that no tilting would occur during these trials. Subsequently, 20 stimulus trials and 20 control trials were presented randomly. Subjects were informed that tilting of the trap door could occur, but they were unaware during which trial this would occur. Thus in both conditions the subjects always had to step on the box and only in condition 2 sometimes it gave way to produce an inclined surface. Surface electromyography (EMG) was recorded of the tibialis anterior (TA), the peroneus brevis (PB), the peroneus longus (PL), the soleus (SO), the gastrocnemius lateralis (GL), and the gastrocnemius medialis (GM) of the left leg. Furthermore, the trap door was connected to a goniometer to record the tilting of the trap door. Thin insole foot switches detected contact with the treadmill and the left foot switch was used to trigger the electromagnet after a set delay. The subjects wore headphones through which loud music was played, to prevent the subjects from hearing the box fall on the treadmill and thereby getting possible cues about the type of trial condition.
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Zero time was defined as the onset of the rotation of the trap door. The onset was calculated as a difference of >1 SD of the average goniometer signal of the trap door before the inversion. To study the net effect of the perturbation in the randomized experiment the average control EMG data (0° tilt) was subtracted from the individual stimulus EMG (25° tilt). For each response peak and for each subject a time window was set manually on the average EMG data of all six muscles of each subject. Latency and duration of the peak was defined as the onset and duration of the time window. The response amplitude was calculated by averaging the rectified EMG within the time window. To enable a proper intersubject comparison of the response amplitudes, the resulting amplitude data of each muscle were normalized with respect to the maximum EMG activity during normal walking for each subject. To obtain the mean response of the whole population, the normalized response amplitudes of all subjects were averaged. Subtracted responses were obtained by subtracting the population control data from the averaged perturbation trials.
To study anticipation, the EMG signals from the first session in which 10 control trials were presented (no tilting occurred and no expectation of tilting) were subtracted from the signals obtained during the control trials of the randomized experiment, in which the subject could expect an inversion perturbation to occur in 50% of the trials (no tilting occurred but there was expectation of possible tilting, "anticipation").
To enable a proper comparison of the EMG amplitude between the different muscles and subjects, the subtracted EMG amplitudes were normalized with respect to the maximum EMG activity during normal walking (measured before each trial and averaged). To determine whether the responses observed were statistically significant and to compare mean response amplitude, incidence, and latency between the different muscles, the Wilcoxon signed-rank test was used because the data were not normally distributed and nonparametric testing was needed. Possible correlation between the weight of the subject and the velocity of the trap door was tested by the Spearman's rank correlation test. In all statistical tests a significance level of P > 0.05 was used.
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RESULTS |
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The 25° tilting of the trap door, causing the ankle inversion in the subjects, had an average duration of 62 ms with SE of 1.7 ms. This is equivalent to an angular velocity of 403°/s with SE of 18°/s (n = 12). No correlation was found between the velocity and the weight of the subjects (Spearman's rank correlation: r = 0.15, P = 0.64). The average of the individual SEs of the tilting duration of all subjects was 2.0 ms. For the intrasubject reproducibility of the EMG responses the latency and duration of the individual trials of the PL were analyzed. For the intersubject variation we refer to Table 1. The latency of SLR showed an average individual SE of 2.8 ms and LLR showed an SE of 1.7 ms. An average individual SE of 1.9 ms was observed for both SLR and LLR.
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In most muscles and all subjects two responses were detected (see Fig. 2). An early response called SLR was observed after about 40 ms and had a duration of about 25 ms. These responses were small but distinct. A larger response, called LLR, was observed after about 100 ms and had a duration of about 35 ms. Only TA showed hardly any LLR activity. The frequency of the response occurrence varied depending on the muscle and type of the response (SLR or LLR) (see Table 1).
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100 ms). The response amplitude depended on the type of the response (SLR or LLR). The LLR showed higher EMG activity than that of the SLR. In a comparison of the various muscles, the peroneal muscles showed the highest SLR response activity (Wilcoxon signed-rank test, P < 0.05), followed by the TA and then the GL (although the latter was not significantly different from the other triceps surae muscles). The GM showed small but significant SLR response activity. For the LLR, again the peroneal muscles (especially the PB) showed significantly larger response activity than that of the other muscles. Amplitudes of the peroneal muscles were more than threefold higher than the GL, which had the largest amplitude of the triceps surae muscles. The TA showed no significant LLR response activity.
Anticipation
During the randomized trials the subjects could anticipate the possibility of inversion (50% chance to have a trial with inversion). To study how this anticipation affected the activity around the moment of foot landing the trials in which subjects knew that no inversion would occur (the expected nontilting trials) were subtracted from the control trials in the randomized experiment (the nonexpected nontilting trials). In both cases no inversion occurred and any difference between the two sets of data had to be ascribed to the presence of anticipation of a potential inversion.
The most striking difference before touchdown was TA being less active than in control trials (see Fig. 3). This muscle is normally most active in the period before the touchdown on the box (from 106 ± 11.4 to 49 ± 12.7 ms) With a short delay after touchdown, both PL and PB showed an abrupt increase in activity (delay of 4 ± 6.6 and 3 ± 3.0 ms, respectively). These bursts of extra activity during the randomized trials were preceded and followed by a period of about 90 ms with lower activity, compared with the expected control trials.
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To study sequential effects of the inversion trials (in condition 2 with 50% chance of inversion), the mean response amplitudes of all first trials and thirteenth trial of each muscle were compared (13 was the minimum number of successful trials of a subject). The SLR did not show any significant decrease in response amplitude. In LLR, however, in all muscles except for the PB, a significant decrease in amplitude was observed (Wilcoxon signed-rank test, P < 0.05, n = 12) (see Fig. 4).
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DISCUSSION |
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). In the present study it is shown that the responses to unexpected inversions during walking do not differ fundamentally from those observed during landing from a jump, although the inverting surface rotated at a slower speed (403 vs. 595°/s). At present, in all subjects and most muscles two responses were detected (SLR with an average latency of about 90 ms and the LLR with a latency of 90 ms). One of the major aims of the present study was to compare these two types of responses with each other and with those found in other studies (using inversions during other tasks such as standing or jumping). The parameters of interest are habituation characteristics, latency, amplitude, and pattern of muscle activation. Habituation
First, there was a marked difference in habituation in the responses because LLR amplitudes decreased substantially with trial repetitions whereas SLR did not. The latter finding is in full agreement with observations made by others in different parts of the body. Rothwell et al. (1986) examined SLR and LLR amplitudes after repetitive stretches of finger and wrist muscles. They found that SLR was relatively unaffected by the repetitions but LLR responses showed marked habituation. A similar situation applies for exteroceptive reflexes. Stimulation of the upper lip induces both early and late exteroceptive reflex suppressions but only the later responses show some degree of habituation (Desmedt and Godaux 1976).
A related issue is the so-called first trial effect (first response is much larger than the ensuing ones). At present it was found that this effect was much larger for LLR than for SLR. The effect consisted primarily of a general cocontraction in most muscles investigated. This result is similar to what has been described for perturbed standing (Bloem et al. 1998; Hansen et al. 1988; Horak and Nashner 1986; Keshner et al. 1987; Timmann and Horak 1997) and other types of perturbed gait (Marigold and Patla 2002; Tang et al. 1998). Some of the authors mentioned (Hansen et al. 1988; Timmann and Horak 1997) explained the decrease of the amplitude as habituation of a "startle-like" response. This interpretation agrees well with our data. The LLR response in the first unexpected trial is present in both agonists and antagonists, indicating a high degree of cocontraction as is typically seen in startle-like responses (Delwaide and Schepens 1995; Nieuwenhuijzen et al. 2000). In contrast, LLR responses in later trials are much more selective. In this case (as in jumping) the LLR is mostly or exclusively seen in the peroneal muscles. It is suggested that this apparent selectivity is related to a difference in excitability and that all these LLR responses originate basically from a similar neural pathway.
Response latency, amplitude, and pattern
The presently described responses during walking show many similarities with those observed in studies using inversions during standing. The latency of the peroneal LLR response in the present study (80–90 ms) is comparable with these other studies (Konradsen et al. 1991a,b; Lynch et al. 1996). In contrast, the response latency of the SLR is slightly shorter than that observed by others. These differences might be caused by the difference in test conditions. Although in other studies the subjects were standing, at present the subjects were walking, thereby introducing an added impact to the inverting surface. In the standing situation the ankle is fully loaded at the onset of the inversion whereas during walking the collapse starts before full weight is transferred to the perturbed limb. Furthermore, there are not only biomechanical differences but also possible changes in the central modulation of the reflexes. Standing and walking are very different tasks and it is known that the amplitude of many reflex responses is task dependent (Duysens et al. 1993; for review see Zehr and Stein 1999). Furthermore, the onset of the rotation is often difficult to judge. In the present experiment the onset of the rotation was set at the point where the trajectories showed a difference of 1 SD of the mean signal before the rotation. Previous studies (during standing) do not mention how the onset of the rotation was determined. The short latency of the SLR suggests this response is a stretch response. Short-latency reflexes are known to be dependent on the velocity of stretch (Gottlieb and Agarwal 1979). The inversion velocity in the present study (403°/s) was higher compared with that of other studies [varying from 50°/s (Lynch et al. 1996) to 375°/s (Konradsen et al. 1997)]. Lynch et al. (1996), eliciting inversions 200°/s, did find a short-latency response, whereas Isakov et al. (1986) found responses of about 60 ms using inversions with a velocity of 250–333°/s. Konradsen et al. (1997), using a faster inversion of 375°/s, indeed found response latencies that were slightly shorter (50 ms). These findings are in conformity with the study of Lynch et al. (1996), who observed an effect of inversion speed on response latency. Gray et al. (2001) also found a modulation of the stretch reflex due to stretch velocity changes.
With respect to amplitude, the LLR was generally larger and more consistent than the SLR response. In the available literature on ankle inversions during standing the LLR is more often reported than the SLR (Lynch et al. 1996; Sheth et al. 1997). Furthermore, larger late than early responses have been reported for a variety of perturbations during walking (Schillings et al. 2000; Sinkjaer et al. 1988; Van Wezel et al. 1997; Zehr et al. 1997) or standing (Fellows et al. 1993; Schieppati et al. 1995). It follows that these LLR responses are likely to be functionally the more important parts of these reactions. In that respect it is also important to consider the muscles participating in these LLR.
With respect to the participation of various muscles in the responses it is clear that for both SLR and LLR, the peroneal muscles showed the largest and most consistent responses. This is not surprising because these muscles receive the largest stretch. In the average EMG data hardly any LLR response was detected in the TA, consistent with our previous findings after landing from a jump (Grüneberg et al. 2003). Few studies have investigated the TA during ankle inversion. Some found an SLR response (Löfvenberg et al. 1995), but in contrast to the present study, some authors did find LLR responses in the TA as well (Lynch et al. 1996; Sheth et al. 1997). Nevertheless, the latter study did mention a lower rate of occurrence in TA than that in other muscles (72% in TA compared with 97% in PB and 88% in PL). Again the difference could be caused by the difference in task (standing vs. walking). In triceps surae muscles the responses were much more consistent than those in TA, in agreement again with the jumping data (Grüneberg et al. 2003) and with those obtained in standing studies (Konradsen et al. 1997). The latter authors indicated that inversion during quiet standing induced a dorsal flexion of the ankle and leaning forward of the body, thereby inducing stretch to the triceps. Of the triceps surae the GL showed more consistent and larger response than the SO and GM, consistent with the jumping condition (Grüneberg et al. 2003). This suggests that the GL has a slightly different function in the inversion. This might be related to the lateral position of the muscle, thereby having some effect as an evertor, protecting the ankle against inversion. A selective recruitment of parts of the triceps surae has been noted in other types of perturbations as well [stepping on surfaces that collapse leads to larger responses in MG than in LG or SOL (Nakazawa et al. 2004)].
Anticipation and prior knowledge
A second major question to be answered relates to the role of anticipation in the generation of EMG activity related to ankle inversion. In a previous study it was shown that the preknowledge about a possible inversion appreciably affected the muscle activations around touchdown, even though no inversion occurred (Grüneberg et al. 2003). In the 50 ms preceding touchdown an increase in SOL activity was seen, consistent with a tendency toward increased plantar flexion or preparing the muscle to soften the impact (a general strategy of cautious landing). In the present study such a tendency toward plantar flexion may have been present as well but this time in relation to the decrease in TA activity before touchdown (as seen in trials where no inversion occurred but where subjects knew that an inversion could occur). This plantar flexion could be part of a more cautious gait, whereby the whole foot is put on the box instead of just the heel in an attempt to get more stability. Furthermore, the TA is also an invertor and thus decreasing its activity would help the evertors to resist the induced inversion. In addition, just after touchdown there was a clear increase in activity level of the PL and PB, which were about to be stretched by the inversion (see Fig. 3). Thus this constitutes another example of what McFadyen and Carnahan (1997) have labeled an ALA (anticipatory locomotor adjustment). It is clear that such muscle activations, occurring before or at the onset of the perturbations, can be more efficient than reactive responses, which may have a sizable delay. It is therefore not surprising to see anticipatory activations in various types of experiments that involve landing on a surface of unknown stiffness (Dyhre-Poulsen and Laursen 1984; Moritz and Farley 2004; Santello and McDonagh 1998).
Less clear so far is the meaning of the responses in the reactive control to unexpected perturbations. The responses in the evertors are too late to resist the induced stretch that is applied to the ankle joint during the inversion movement. The question arises what purpose this response serves in protecting the ankle, for example in a later phase (after completion of the inversion). Several studies have detected a disturbance in body posture after inversion elicited during quiet standing (Konradsen and Ravn 1990; Konradsen et al. 1997). Furthermore, damage can occur only when force is applied on top of the induced stretch, i.e., when weight is put on the leg after the inversion. Therefore the function of the LLR might lie in balance control and/or in reduction of the loading of the ankle in the period after the inversion movement stopped. The large amplitude of these responses is consistent with the idea that stretch reflexes are important for the stability of the supporting leg during walking, as was suggested by others as well (for stretch of the ankle dorsiflexors, see Christensen et al. 2001).
Origin of the LLR
Although the present experiments were not specifically aimed at the exploration of the origin of the various responses, it is worthwhile to summarize the possibilities. In a review and in a specific study (Christensen et al. 2000, Christensen et al. 2001, respectively) suggested that a TA response had a strong cortical component at the time of the LLR. Stretch of the ankle dorsiflexors was applied at different times of the walking cycle. The TA reflex response in the stance phase was abolished by ischemia of the lower leg, suggesting that large muscle afferents were involved in the generation of the response. They also suggested that a transcortical reflex may be partly involved in the generation of the TA LLR stretch responses during walking. Could a similar mechanism be in place for the muscles investigated in this study? Some authors have argued that the LLR responses in peroneal muscles are likely to have a supraspinal origin (Grüneberg et al. 2003; Lynch et al. 1996). More generally, it is currently thought that the likelihood of a transcortical component increases with the latency of the response (especially the LLR; see Jacobs and Horak 2007; Taube et al. 2006). However, it remains difficult to identify the different components (especially median-latency response and LLR) and one should not overlook the possibility of a contribution of brain stem reflexes to some of these components (Jacobs and Horak 2007). More definite proof should come from experiments combining transcranial magnetic stimulation and LLR reflexes to inversion perturbations, using a protocol similar to the one used by Taube et al. (2006).
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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: J. Duysens, Department of Rehabilitation Medicine, Radboud University Nijmegen Medical Center, P.O. Box 9101, 6500 HB Nijmegen, The Netherlands (E-mail: J.Duysens{at}reval.umcn.nl)
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