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MS 9770 Received 24 June 1999; accepted after revision 6 July 1999.
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ABSTRACT |
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INTRODUCTION |
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Cat experiments have demonstrated that the firing of Ia inhibitory interneurones, which convey reciprocal inhibition between antagonistic muscles, is rhythmically modulated during walking (Pratt & Jordan, 1987). Interneurones which are activated from quadriceps afferents are thus mainly active when the quadriceps muscle is active during fictive locomotion. This is in agreement with the idea that the interneurones help to switch off antagonistic muscle activity during walking.
Transmission in the disynaptic reciprocal Ia inhibitory pathway may also be investigated in human subjects using non-invasive techniques (for review see Crone & Nielsen, 1994). Stimulation of the common peroneal nerve (CPN) produces a short-latency depression of the soleus H-reflex (Tanaka, 1974). This depression is in all likelihood mediated by Ia inhibitory interneurones from ankle dorsiflexors onto ankle plantar flexors. Changes in the size of the depression during voluntary movement have been suggested to reflect changes in the transmission in the reciprocal Ia inhibitory pathway (Crone et al. 1987; Crone & Nielsen, 1989, 1994). At the onset of voluntary dorsiflexion the inhibition is strongly increased, whereas it is depressed at the onset of plantar flexion, which is in agreement with a parallel control of corresponding Ia inhibitory interneurones and motoneurones as suggested by Lundberg (1970).
It has not yet been investigated with this method whether transmission in the reciprocal inhibitory pathway is modulated during walking in human subjects in the same way as shown in the cat by Pratt & Jordan (1987). Capaday et al. (1990) investigated the modulation of the short-latency depression produced by stimulation of the CPN in the voluntary averaged and rectified soleus EMG in the stance phase of walking. This inhibition is likely - at least to a large extent - to be mediated by Ia inhibitory interneurones. Capaday et al. (1990) reported that the inhibition appeared to be of a similar size in the stance phase of walking to that observed during a tonic voluntary plantar flexion in a standing subject.
Capaday et al. (1990) were restricted to studying the stance phase of walking and they were therefore not able to answer whether the reciprocal inhibition was cyclically modulated during walking. Furthermore, rather strong stimulation of the CPN was used. As mentioned by Capaday et al. (1990) such strong stimuli may encroach on other nerve fibres than Ia afferents from the ankle dorsiflexors (see also Meunier et al. 1993; Petersen et al. 1998) and the transmission in the Ia inhibitory pathway may become saturated. Centrally induced changes in the transmission in the Ia inhibitory pathway may therefore not be demonstrated (Petersen et al. 1998).
The purpose of the present study was to evaluate the modulation of disynaptic reciprocal Ia inhibition between ankle dorsiflexors and ankle plantar flexors evoked by submaximal stimulation of antagonistic nerves using both the H-reflex technique and stimulus-triggered averaging of the voluntary EMG activity. We studied the inhibition of the soleus H-reflex by stimulation of the CPN in both the swing and stance phases of walking. The stimulus-triggered depression of the soleus EMG activity was studied in the stance phase of walking and during voluntary plantar flexion. In addition the stimulus-triggered depression of the tibialis anterior EMG activity following stimulation of the tibial nerve was studied in the swing phase of walking and during voluntary dorsiflexion. Taken together the findings from these experiments suggest that disynaptic reciprocal inhibition between ankle dorsi- and plantar flexors is modulated during human walking.
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METHODS |
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Seventeen healthy human subjects participated in the experiments. All gave informed consent to the experimental procedures, which were approved by the local ethics committee.
Experimental set-up
Reciprocal inhibition between antagonistic muscles of the ankle joint was investigated either when the subjects were sitting in a reclining armchair performing voluntary ankle plantar flexion or dorsiflexion, when walking on a treadmill or when performing voluntary ankle plantar flexion or dorsiflexion standing up.
In the sitting subjects the hip was semiflexed to 120 deg, the knee flexed to 160 deg and the ankle in 110 deg plantar flexion. The left foot of the subject was attached to a foot plate which was connected to a torque metre. The torque exerted on the foot plate and the voluntary rectified and integrated electromyographic activity (EMG) measured by surface electrodes placed on the tibialis anterior or soleus muscles were displayed on an oscilloscope placed in front of the subject.
Measurements were performed in various situations as follows:
At rest (for H-reflex experiments)
Tonic dorsi- or plantar flexion. The subject was requested to maintain a steady torque and EMG activity level in either the tibialis anterior or the soleus muscle at 6-8 prescribed levels of contraction ranging from 5 to 60 % (3-5 N m to 25-40 N m) of the maximal voluntary dorsi- or plantar flexion effort.
Dynamic plantar flexion. The rectified and integrated soleus EMG activity (average of 30 walking cycles) measured during the stance phase of walking was displayed on an oscilloscope in front of the subject. It was then the subject's task to match both the level and the rate of change of soleus EMG activity by performing an isometric dynamic plantar flexion. Most subjects had considerable difficulty achieving an acceptable match between the EMG activity in the two tasks and it was in general only achieved after several repetitions of the task. Measurements were made at different intervals in relation to the onset of the EMG activity.
Measurements at rest and during tonic contraction were performed at the beginning of the experiment and repeated after the walking session. The measurements during dynamic contraction were performed after the walking session. In most of the experiments measurements were in addition made while the subject performed different levels of tonic voluntary dorsi- or plantar flexion while standing on the treadmill.
Walking
The speed of the treadmill was set to 3·5-4·0 km h-1. Pressure sensitive triggers were placed under the heel and toe of the subject's left shoe. These were used to trigger the stimuli which could then be delivered at different intervals in relation to heel strike and toe off during walking.
In all situations the background EMG activity was amplified (× 2000 to × 20 000), band-pass filtered (25 Hz to 1 kHz), rectified and sampled (5 kHz sampling frequency) on a Concurrent computer workstation (Masscomp software, InfoWest Inc., Winnipeg, Canada). Care was taken that measurements were made at matched levels of background EMG activity in the different situations.
Reciprocal inhibition was measured either as the short-latency depression of the soleus H-reflex following stimulation of the common peroneal nerve (CPN) or as the depression of the soleus or tibialis anterior EMG activity following stimulation of the CPN or the posterior tibial nerve (PTN), respectively (Fig. 1).
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Reciprocal inhibition of soleus and tibialis anterior (TA) motoneurones was evoked by stimulating the common peroneal (CPN) and posterior tibial nerve (PTN), respectively (A). The amount of inhibition was evaluated either from the short-latency inhibition of the H-reflex (B) or from the depression of the voluntary averaged and rectified EMG activity (C). B, since it was not possible to evoke H-reflexes in the TA muscle during walking in any of the investigated subjects the H-reflex experiments were only performed for the soleus muscle. At the beginning of each experiment a time course of the effect of the CPN stimulation (1·0 × motor threshold; MT) on the soleus H-reflex was obtained. The conditioning-test interval within the initial 5 ms at which the reflex was maximally depressed in the resting subject was chosen for the recordings during walking (indicated by arrow in B). The ordinate is the size of the conditioned reflex as a percentage of the control reflex size (averaged traces of control and conditioned H-reflexes at a conditioning-test interval of 2 ms are shown to the left of the graph). C, the upper two traces to the left of the graph show the depression of the rectified TA EMG activity during tonic voluntary dorsiflexion and the M-response in the soleus EMG evoked by PTN stimulation. The two lower traces show the depression of the rectified soleus EMG activity during tonic voluntary plantar flexion and the M-response in the TA EMG evoked by CPN stimulation. The sweeps were triggered on the respective stimuli (usually 75-100 sweeps were averaged). The latency of the inhibition was around 35-45 ms in the different subjects. The graph demonstrates that the amount of inhibition (measured as the difference in microvolts between the amount of background EMG activity and the EMG activity during the inhibition) increases almost linearly with the amount of background EMG activity as also reported by Capaday et al. (1990). In all experiments regression lines were fitted to these data and used to calculate the amount of inhibition that should be expected during walking for a given level of background EMG activity. In this way it could be evaluated whether the inhibition during walking was larger or smaller than the inhibition observed during tonic contraction at any given level of background EMG activity. | ||
H-reflex
The soleus H-reflex was evoked by stimulation of the PTN through a monopolar electrode placed in the popliteal fossa. The indifferent electrode was placed below the patella. The position of the electrodes was secured by elastic straps. At the beginning of each experiment a maximal M-response (Mmax) was measured as the peak-to-peak value (in some experiments area measurements were also performed), and the H-reflexes were expressed in relation to Mmax (%Mmax). Throughout the experiments Mmax was checked several times. The control H-reflex was usually adjusted to the same size in all the investigated situations, since the sensitivity of the H-reflex to conditioning inputs depends crucially on its size (Crone et al. 1990). Since the H-reflex is strongly modulated with the different tasks investigated in the study (see Fig. 2 and Capaday & Stein, 1987), this could only be done by adjusting the intensity of the PTN stimulation. However, the major findings in the present study were qualitatively similar when no adjustment of the H-reflex was made. Because of the strong depression of the soleus H-reflex in the swing phase of walking we were forced to use rather small reflexes in all tasks. In only four subjects out of more than 30 tested were we able to obtain reflexes that were 5 % of Mmax in the swing phase of walking.
It was checked throughout the experiments that there were no systematic changes in the position of the stimulating electrode by monitoring the size of a small M-response in the soleus muscle. Since the intensity of the PTN stimulation, which evoked the H-reflex, was generally below the M-threshold, this could only be done by alternating the stimuli which evoked the H-reflex with stimuli at a slightly higher intensity to evoke an M-response. All trials in which the size of the average M-response deviated more than 10 % from a pre-set level were disregarded from further analysis. Although the M-response was not measured following the stimulation which evoked the H-reflex, it is unlikely that any change in the position of the electrode should occur only in those trials in which the H-reflex was evoked. If such changes did occur in some trials they would disappear from the averaged result because of the high number of measurements that was averaged (more than 100 reflexes for each alternative as compared to around 10-20 reflex responses in other studies using H-reflex testing in sitting subjects; cf. Iles, 1986; Day et al. 1987; Crone et al. 1987; Pierrot-Deseilligny, 1997).
Reciprocal inhibition of the soleus H-reflex was evoked by stimulating the CPN through a bipolar electrode placed at or distal to the neck of the fibula. Care was taken that the electrode was positioned so that an M-response in the tibialis anterior muscle had a lower threshold than an M-response in the peroneal muscle group (Petersen et al. 1998). A stimulation intensity of 1·1 × MT in the tibialis anterior muscle was used. Throughout the experiment the M-response evoked by the stimulation in the tibialis anterior EMG was monitored. Trials in which this M-response deviated by more than 10 % from a pre-set level were discarded from further analysis. At the beginning of each experiment a time course of the effect of the CPN stimulation on the H-reflex was obtained while the subject was sitting at rest (Fig. 1B). The interval at which a maximal amount of inhibition was observed was chosen for the rest of the experiment (arrow in Fig. 1B). The maximal amount of inhibition was usually found at conditioning-test intervals of 2-3 ms in the different subjects. In a few experiments tibialis anterior H-reflexes were seen to be evoked by the CPN stimulation in the swing phase of walking (cf. Fig. 1). These were, however, too small for an investigation of the effect of conditioning stimulation.
Control and conditioned reflexes were randomly alternated with each other and with a PTN stimulation at a higher intensity than that used to evoke the H-reflex (see above). The size of the reciprocal inhibition was expressed as the size of the conditioned reflex as a percentage of the control H-reflex size as in Fig. 1B. At least 100 control and conditioned reflexes were averaged for each point in each situation. The statistical significance of changes in the reciprocal inhibition was tested by Student's t test.
Stimulus-triggered averaging of rectified EMG
Stimulus-triggered averaging of rectified EMG was introduced by Capaday et al. (1990). As shown by them and illustrated in Fig. 1C (lower trace and filled circles) stimulation of the CPN produces a depression of the stimulus-triggered averaged and rectified soleus EMG. This depression is likely to be mediated at least partly by Ia inhibitory interneurones projecting from ankle dorsiflexors to ankle plantar flexors. In order to minimize the risk of activating afferents from the peroneal muscle group and to avoid saturation of the reciprocal inhibitory pathway we used significantly weaker stimuli to the CPN than Capaday et al. (1990). Whereas they used stimuli of more than 1·5 × MT, we used stimuli of less than 1·2 × MT. In some experiments stronger stimuli were used. We also studied the short-latency inhibition of the tibialis anterior EMG activity produced by stimulation of the PTN (1·1 × MT; Fig. 1C). This inhibition is likely to be mediated by Ia inhibitory interneurones projecting from ankle plantar flexors to ankle dorsiflexors. For both the CPN and PTN stimuli, the evoked M-responses in the respective muscles were monitored throughout the experiments and trials in which the size of the M-responses deviated by more than 10 % from a pre-set level were discarded from further analysis.
For both the inhibition in the soleus and tibialis anterior EMG activity 60-100 traces were averaged with a delay before the stimulus of 50 ms and a total duration of 200 ms. The EMG signals were amplified (× 2000 to × 20 000), filtered (25 Hz to 1 kHz) and averaged on a Concurrent computer workstation (Masscomp software).
The amount of inhibition was measured as the difference between the level of EMG activity within the first 10 ms from the onset of the inhibition and the level of background EMG activity. During tonic contraction the background EMG activity level was measured as the mean level of EMG activity 50 to 5 ms before the stimulus (see Fig. 1). Because of the ongoing changes in the EMG activity during dynamic plantar flexion and walking, this way of measuring the level of background EMG activity was clearly not always adequate in those tasks. In such cases the background EMG activity was measured from trials without any stimulation. Such trials were randomly intermingled with trials with stimulation and the level of background EMG activity was measured at the same time as the inhibition in the trials with stimulation.
During tonic plantar flexion there was a near linear relation between the amount of inhibition and the background EMG activity level (see also Capaday et al. 1990). This relationship was used to predict the amount of inhibition during dynamic contractions or during walking for a given level of background EMG activity. A first order regression line was fitted to the plot of the amount of inhibition vs. the level of background EMG activity (see Fig. 1C). The equation for this regression line was then used to calculate the expected amount of inhibition during walking and dynamic contraction for any level of background EMG activity in those situations.
Differences between the observed inhibition and the expected inhibition were tested for statistical significance with Wilcoxon's signed rank test and a two-way ANOVA. The level of significance was set to 0·05.
Experiments during ischaemia
In some experiments the modulation of the inhibition of the soleus EMG activity induced by CPN stimulation was investigated during ischaemia of the leg. The ischaemia was induced by inflating a tourniquet (to above 240 mmHg) placed below the knee joint distal to the stimulation of the CPN. Measurements were made during tonic plantar flexion in the standing subject and 300 ms after heel strike in the stance phase of walking at matched levels of background soleus EMG activity. A comparison was made between measurements without ischaemia and measurements when transmission in large diameter afferents was blocked by ischaemia. This was checked by monitoring a T-reflex in the soleus EMG evoked by a tendon tap applied to the Achilles tendon (4 ms duration; 4 mm amplitude; Brüel & Kjær vibration exciter model 1408). Transmission in motor axons was checked by monitoring Mmax in the soleus EMG evoked by a supramaximal stimulation to the PTN in the popliteal fossa. During these tests the subjects were sitting down. Measurements of the modulation of reciprocal inhibition were initiated when the T-reflex disappeared and the Mmax was unchanged. This usually occurred around 15 min after onset of ischaemia.
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RESULTS |
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Modulation of soleus and TA H-reflex during walking
Figure 2 demonstrates the modulation of the soleus (Fig. 2A) and TA H-reflexes (Fig. 2B) during walking. As demonstrated already by Capaday & Stein (1986) and Crenna & Frigo (1987) the soleus H-reflex was largest towards the end of the stance phase and completely abolished in the swing phase. The TA H-reflex was in contrast only present in the swing phase. In this subject a soleus H-reflex was never evoked in the swing phase and a TA H-reflex never in the stance phase regardless of the stimulation intensity. Both reflexes were easily evoked at rest. Similar findings were obtained in four other subjects. It seems likely that modulation of the activity of Ia inhibitory interneurones may at least contribute to the observed modulation of the H-reflexes (Lavoie et al. 1997). Increased Ia inhibition onto soleus motoneurones may thus contribute to the depression of the soleus H-reflex in the swing phase. Since Ia inhibitory interneurones projecting in opposite directions mutually inhibit each other (Hultborn, 1972), this increased inhibition would at the same time lead to decreased Ia inhibition of TA motoneurones and thereby contribute to the increase of the TA H-reflex in the swing phase. Similarly, a contributing factor to the depression of the TA H-reflex in the stance phase may be increased Ia inhibition onto TA motoneurones and - through mutual inhibition - this would also contribute to the increase of the soleus H-reflex. The experiments described below were performed to test these possibilities.
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The graphs show the size of H-reflexes ( | ||
Modulation of the inhibition of the soleus H-reflex evoked by CPN stimulation
Since the soleus H-reflex is generally as strongly depressed in the swing phase of walking as in the subject used for the illustration in Fig. 2, it was only possible in four out of more than 30 tested subjects to evoke a stable H-reflex in the swing phase. Data from these four subjects are illustrated in Fig. 3. In all four subjects a time course of the effect of the CPN stimulation on the soleus H-reflex was investigated at the beginning of the experiment and the interval at which the maximal amount of inhibition was observed was used for the rest of the experiment (cf. Fig. 1B). The graphs all show the size of the conditioned reflex as a percentage of the control H-reflex size at this conditioning-test interval. Except for the measurement at 100 ms after heel strike in the subject illustrated in Fig. 3C it was not possible in any of the four subjects to evoke an inhibition of the soleus H-reflex in the stance phase of walking, although a clear inhibition could be evoked in all subjects at rest either sitting down or standing with support (open circle in each of the graphs). However, around the onset of the swing phase a pronounced inhibition occurred. In two of the subjects this inhibition was clearly largest in the early and middle part of the swing phase and disappeared towards the end of the swing phase (Fig. 3A and B). In the other two subjects the inhibition had more or less the same size throughout the swing phase (Fig. 3C and D).
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The graphs show the effect of CPN stimulation on the soleus H-reflex during walking in 4 different subjects. In each subject a time course of the effect of the CPN stimulation on the soleus H-reflex was obtained at the beginning of the experiment and the conditioning-test interval at which the largest amount of inhibition was observed within the initial 5 ms was used for the experiment (cf. Fig. 1B). This interval varied between 2·0 and 3·0 ms in the different subjects. The ordinate is the size of the conditioned reflex as a percentage of the control reflex size. The control reflex was adjusted to the same size throughout walking by adjusting the intensity of the PTN test stimulation. Since only very small reflexes could be obtained in the swing phase, the reflexes were adjusted to around 5 % of Mmax. The intensity of the CPN stimulation was set just above 1·0 × MT in order to evoke a small M-response in TA, which was kept the same size throughout the entire experiments. Measurements were made at different intervals after heel strike. Each symbol represents the average of 50 conditioned and 50 control responses. The error bars indicate 1 standard error of the mean. The open circles to the left in each graph show the size of the conditioned reflex as a percentage of the control H-reflex size when the subjects were at rest. * P < 0·05 (Student's t test). | ||
The control H-reflex was maintained at around 5 % of Mmax in all four subjects throughout walking in order to take the different sensitivity of differently sized reflexes into account (Crone et al. 1990). In all four experiments measurements were, however, also made without compensation of the size of the control H-reflex. It was still not possible to evoke any inhibition of the (much larger) H-reflex in the stance phase of walking.
Measurements were also made in the stance phase of walking in five subjects in whom it was not possible to evoke an H-reflex in the swing phase. In none of these subjects was it possible to evoke an inhibition of the H-reflex in the stance phase, although a significant inhibition was evoked in all subjects at rest.
These findings suggest that Ia inhibitory interneurones projecting from ankle dorsiflexors onto ankle plantar flexors may be facilitated in the swing phase and inhibited in the stance phase of walking. To obtain further evidence of this we also measured the amount of inhibition in the background soleus EMG activity following CPN stimulation and in the background TA EMG activity following PTN stimulation.
Modulation of CPN-induced inhibition of the soleus background EMG activity
Figure 4A-C shows data from an experiment in which the inhibition in the soleus EMG activity evoked by CPN stimulation was investigated. The intensity of the CPN stimulation was adjusted to 1·1 × MT. The small M-response evoked by this stimulation in the TA EMG was maintained constant throughout the experiment by small adjustments in the intensity of the stimulation. As seen in the lower part of Fig. 4A the background soleus EMG activity increased steadily throughout the stance phase. At the beginning of the stance phase the CPN stimulation produced only a small inhibition of the EMG activity, although the same stimulation evoked a strong inhibition at a matched background EMG activity level during tonic plantar flexion (compare trace at 200 ms after heel trigger in Fig. 4A with second trace during tonic plantar flexion in Fig. 4B). At intervals longer than 200 ms after heel strike the inhibition was clear, but it remained smaller than the inhibition observed at matched background EMG activity levels during tonic plantar flexion (compare trace at 400 ms after heel strike in Fig. 4A with third in Fig. 4B). Only towards the very end of the stance phase a similar amount of inhibition was observed in the two situations (compare trace at 700 ms in Fig. 4A with fourth trace in Fig. 4B). In Fig. 4C these differences between the amount of inhibition in the stance phase of walking and during tonic plantar flexion are shown more clearly. The amount of inhibition that should be expected at any given level of background EMG activity during walking was calculated from the relation between the amount of inhibition and the background EMG activity level during tonic plantar flexion as explained in Methods (cf. Fig. 1). It is then clearly seen that in the early stance phase less inhibition was observed than would be expected from the amount of inhibition measured during tonic plantar flexion. In the end of the stance phase a difference can still be observed. When taking the level of background EMG activity into account it is clear that it is mainly in the early stance that the observed inhibition is much smaller than would be expected from a tonic plantar flexion.
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Inhibition of the soleus EMG activity induced by stimulation of the CPN (1·1 × MT) in the stance phase of walking (A) and at different levels of tonic isometric plantar flexion in a standing subject (B). The arrows in A and B indicate the approximate onset of the inhibition. A, the traces show the stimulus-triggered averaged (75 sweeps) and rectified soleus EMG activity at different times after heel strike; vertical calibration bars, 50 µV; horizontal bars, 20 ms; the latter indicate in addition the level of the baseline. The lower part of A shows the soleus EMG activity (average of 30 sweeps) during the stance phase; the abscissa shows the time interval after heel contact. B, similar measurements as in A, but at increasing levels of tonic isometric plantar flexion from top to bottom. The amount of inhibition measured from the traces in B were plotted as a function of the background EMG activity (cf. Fig. 1C) and regression lines were calculated for the data. These regression lines were used to calculate the amount of inhibition that should be expected for each of the levels of soleus background EMG activity in the stance phase of walking. C, the amount of inhibition ( | ||
Figure 4D shows pooled data from all 14 subjects in whom this experiment was performed. In order to compensate for differences in the background EMG activity between different subjects, the observed inhibition was expressed as a percentage of the expected inhibition (calculated as described in Methods). Applying a signed rank test on the group data revealed a clear difference between the observed and expected inhibition at the beginning of the stance (P < 0·01), whereas this difference was less clear towards the end of the stance and only just reached a statistically significant level (signed rank test, P < 0·05).
Influence of stimulation intensity
The observation that CPN stimulation produces a smaller inhibition in the soleus EMG activity in the stance phase of walking than during tonic plantar flexion is in contrast to the study by Capaday et al. (1990) who found an equal amount of inhibition in the two situations. A possible explanation of this discrepancy is provided in Fig. 5. In a recent study, Petersen et al. (1998) reported that the inhibition evoked by the CPN stimulation was not sensitive to modulatory influences when the stimulation intensity was high. At low intensities of stimulation (below 1·2 × MT) evidence of decreased transmission in the reciprocal inhibitory pathway with increasing plantar flexion was thus obtained, whereas no such evidence could be obtained when the stimulation intensity was increased to more than 1·5 × MT. In the experiment illustrated in Fig. 5 we therefore compared the modulation of the inhibition evoked by weak (1·1 × MT; Fig. 5A and C) and strong CPN stimulation (1·6 × MT; Fig. 5B and D) during walking and tonic plantar flexion at matched background EMG activity levels. With both stimulation intensities the amount of inhibition increased almost linearly with increasing background soleus EMG activity (regression coefficients of 0·98), but the slope of the regression line was steeper for the strong stimulation than for the weak stimulation (0·90 as compared to 0·73). The regression lines were used as in Fig. 4 to calculate the amount of inhibition that should be expected at each level of background soleus EMG activity during walking. In Fig. 5C and D the result of this calculation has been compared to the amount of inhibition that was actually observed (compare open circles, representing expected inhibition, with filled circles, representing observed inhibition). As can be seen the weak CPN stimulation failed to evoke any inhibition during walking at any time of the stance phase, although a significant amount of inhibition would have been expected based on the background EMG activity level (Fig. 5C). In contrast, when the CPN stimulation intensity was 1·6 × MT, the expected and observed inhibition were equally pronounced at most intervals (Fig. 5D). In the other three subjects tested this way the observed inhibition during walking was similarly smaller than the expected inhibition when the CPN stimulation was weak. With strong stimulation a difference between the expected and observed inhibition could still be seen, but this difference was less pronounced than when the stimulation intensity was weak.
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The data are from a single subject. The CPN was stimulated at an intensity of either 1·1 × MT (A and C) or 1·6 × MT (B and D). A and B show the amount of inhibition of the soleus EMG activity (µV) as a function of the level of the background EMG activity. The regression lines for these data were used to calculate the expected amount of inhibition for a given level of background EMG activity in the stance phase of walking (cf. Fig. 1C). The result of this calculation is shown as open circles in C and D, whereas the filled circles represent the amount of inhibition that was actually measured at each of the different intervals during the stance phase. Each symbol represents the mean of 75 measurements. | ||
Ramp contraction
During walking the background EMG activity is steadily changing, whereas it has an almost constant level during tonic contraction. To investigate whether this difference in the background EMG activity could explain the observed difference in the amount of inhibition during walking and tonic contraction, we also investigated the amount of inhibition during a dynamic plantar flexion in which both the level of EMG activity and the rate of change of EMG activity were matched to those observed in the stance phase of walking. When comparing the EMG traces in Fig. 6A and B it is seen that it was indeed possible for the subject to match the EMG activity measured during isometric dynamic plantar flexion sitting down with the EMG trajectory measured during walking. Despite this, the CPN stimulation evoked a much smaller inhibition of the soleus EMG activity during walking (Fig. 6C and D, open circles) than during the dynamic plantar flexion (filled circles). In Fig. 6C the data are shown as a function of the time after the onset of EMG activity in the two tasks and in Fig. 6D as a function of the background EMG activity. It is seen that irrespective of the time after the onset of movement or the EMG activity a smaller amount of inhibition was measured during walking.
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The data are from a single subject. In A and B the rectified (upper traces) and rectified and integrated (lower traces) soleus EMG activity is shown for the stance phase of walking and during dynamic isometric plantar flexion, respectively. In the latter task the subject was sitting down and used the rectified and integrated EMG signal to reproduce that recorded during walking. In C and D the amount of inhibition of the soleus EMG activity induced by CPN stimulation (1·1 × MT) in the stance phase of walking (open circles) and during the dynamic plantar flexion task (filled circles) is shown as a function of the time after EMG activity onset (C) and the background EMG activity (D). Each symbol is the mean of 75 measurements. | ||
This type of experiment was performed in five subjects. In all subjects the inhibition was smaller during walking than during dynamic plantar flexion at matched levels of background soleus EMG activity (Two-way ANOVA, P < 0·05).
Modulation of the inhibition in the soleus EMG activity during ischaemia
In order to investigate whether the decrease of inhibition in the soleus EMG activity during walking as compared to tonic contraction could be caused by peripheral feedback in large diameter afferents from the ankle dorsi- or plantar flexors, the modulation of the inhibition was also investigated during ischaemia induced by inflating (>240 mmHg) a blood pressure cuff placed just below the knee joint (distal to the stimulating electrode). Data from one of these experiments are shown in Fig. 7. It is seen from Fig. 7A that a pronounced inhibition was evoked by CPN stimulation during tonic plantar flexion in this subject, but the same stimulation had no effect on the soleus EMG activity 300 ms after heel strike in the stance phase of walking at a matched level of background EMG activity (Fig. 7C). Ischaemia was then induced and the transmission in soleus Ia afferents was evaluated by monitoring a T-reflex in the soleus EMG evoked by a tendon tap applied to the Achilles' tendon. Fifteen minutes after onset of ischaemia the T-reflex disappeared, signifying that Ia afferents were effectively blocked. At this time Mmax had the same size as before ischaemia, signifying intact transmission in motor axons. As seen from Fig. 7B the CPN stimulation still produced a significant inhibition of the soleus EMG activity during plantar flexion and this inhibition was still not present in the stance phase of walking (Fig. 7D). Similar findings were obtained in the other two tested subjects. This signifies that peripheral feedback in large diameter afferents cannot explain the decrease of reciprocal inhibition during walking as compared to tonic plantar flexion.
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The data are from a single subject. Stimulus-triggered averaged TA (upper traces) and soleus (lower traces) EMG activity following stimulation of the CPN (1·1 × MT) in the stance phase of walking 300 ms after heel trigger (C and D) and during tonic plantar flexion at a matched level of background soleus EMG activity (A and B). The arrows indicate the inhibition. Measurements were made in a control situation without ischaemia (A and C) and 19 min after ischaemia was induced in the leg by inflating (>240 mmHg) a cuff placed distal to the CPN stimulation (B and D). Transmission in large diameter muscle afferents was blocked 15 min after inflation of the cuff as evidenced from the disappearance of the Achilles T-reflex. Each trace is the average of 75 measurements. | ||
In two subjects the cuff was placed on the thigh above the patella and the stimulating electrode. In both subjects the CPN-induced inhibition of the soleus EMG activity during tonic dorsiflexion was abolished at the same time after the onset of ischaemia as the soleus H-reflex but prior to changes in Mmax in TA or soleus. This supports the idea that the inhibition is mediated by large diameter afferents.
Modulation of the inhibition in the TA EMG activity evoked by PTN stimulation
To investigate the inhibition from the ankle plantar flexors onto ankle dorsiflexors, the PTN was stimulated and the depression of the TA EMG activity was measured. This experiment was performed in eight subjects. In the subject used for the illustration in Fig. 8A-C, the PTN stimulation evoked a clear inhibition in the TA EMG during tonic dorsiflexion (Fig. 8B), but only a small inhibition during the swing phase of walking (Fig. 8A) - compare for instance trace at -300 ms in Fig. 8A with second trace in Fig. 8B during tonic dorsiflexion. As already explained for the inhibition in the soleus EMG activity (Fig. 4C), the amount of inhibition that should be expected at any given level of background TA EMG activity in the swing phase of walking was calculated from the relation between the amount of inhibition and the background TA EMG activity during tonic dorsiflexion (cf. Fig. 1). In Fig. 8C the expected amount of inhibition is compared to the amount of inhibition that is observed during walking. It is seen that throughout the swing phase less inhibition was measured than at a comparable level of TA EMG activity during tonic dorsiflexion, except at -400 ms after heel contact. This was also the case in the other seven subjects in whom this experiment was performed. The group data (n = 10) are shown in Fig. 8D. It is seen that the observed inhibition was smaller than the expected inhibition throughout the swing phase (P < 0·05; signed rank test).
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The figure is similar to Fig. 4. A, traces are the stimulus-triggered averaged (75 sweeps) and rectified TA EMG activity following PTN stimulation (1·1 × MT) applied at different times in relation to heel contact. The horizontal calibration bar (20 ms) indicates the level of the baseline; vertical bar, 50 µV. The rectified background TA EMG activity and soleus EMG activity (average of 30 cycles) in the swing phase is shown at the bottom. B, similar measurements as in A, but at increasing levels of tonic isometric dorsiflexion from top to bottom. As in Fig. 4, the arrows indicate the approximate time for the onset of the inhibition of the EMG activity. C, the amount of inhibition measured from the traces in A is plotted ( | ||
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DISCUSSION |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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We have demonstrated in this study that the short-latency inhibition of the soleus H-reflex evoked by CPN stimulation is modulated during walking, being pronounced in the swing phase and absent in the stance phase. The inhibition in the background soleus EMG activity evoked by CPN stimulation was similarly small in the stance phase and the inhibition in the background TA EMG activity evoked by PTN stimulation was small in the swing phase.
Origin of the inhibition
Previous studies have demonstrated that the short-latency depression of the soleus H-reflex is mediated by the disynaptic inhibitory pathway (reviewed by Crone & Nielsen, 1994). It is likely that the same pathway is of dominant importance for the depression of the soleus EMG activity. Stimulation of CPN at intensities above motor threshold in the TA muscle is likely to also activate group Ib, II and cutaneous afferents and - with certainty - also motor efferents. Short-latency pathways, excitatory or inhibitory, projecting to the soleus motoneurones or to the Ia inhibitory interneurones may therefore also influence the depression of the EMG activity. Several arguments, however, favour the short-latency depression of the soleus H-reflex and the background soleus EMG activity being mediated by the same mechanism. The two inhibitions have the same (low) threshold (Petersen et al. 1998) and the depression of the EMG activity disappears when transmission in large-diameter afferents is blocked by ischaemia (cf. Fig. 7). Recent experiments in patients with a mutation in the gene coding for the 
1 subunit of the glycine receptor have also failed to demonstrate the inhibition of both the H-reflex and the EMG suggesting that both are mediated by glycinergic interneurones (C. Crone, J. Nielsen, N. Petersen & G. Van Dijk, unpublished observations). Finally, since we also found that the modulation of the depression of the EMG activity was similar to the modulation of the inhibition of the soleus H-reflex, we do not find it likely that the depression of the EMG activity should be caused to any large extent by other pathways than the disynaptic Ia inhibitory pathway.
Methodological considerations
It is an important point that a difference in the amount of inhibition of the soleus EMG activity evoked by CPN stimulation during stance as compared to tonic plantar flexion could mostly only be demonstrated when the stimulation intensity was weak (i.e. below approximately 1·2 × MT). At higher intensities of stimulation we found an almost equal amount of inhibition in the two tasks as also reported by Capaday et al. (1990). Petersen et al. (1998) also found that it was only possible to obtain evidence of depression of transmission in the reciprocal inhibitory pathway during strong plantar flexion as compared to weak plantar flexion when the CPN stimulation was weak. They also found that the maximal amount of inhibition was evoked at stimulation intensities around 1·3 × MT. At stronger stimulation intensities transmission in the pathway is therefore saturated, which probably explains why it was not possible - with such strong stimuli - to demonstrate differences in the inhibition during walking and tonic contraction in the present study and during strong and weak plantar flexion in the study by Petersen et al. (1998). Recent cat experiments are well in line with this (H. Hultborn, R. Brownstone & J.-P. Gossard, personal communication). Large disynaptic Ia IPSPs in extensor motoneurones evoked by supramaximal stimulation of group I afferents thus increased with the amount of depolarization of the motoneurone during the extensor phase of fictive locomotion as should be expected from the increased driving force as the membrane potential depolarizes. In striking contrast, small IPSPs were, however, depressed in the extensor phase despite the depolarization of the motoneurones.
Mechanisms responsible for the modulation of the inhibition
Since the inhibition of the soleus EMG activity was more depressed in the stance phase of walking than during tonic or dynamic plantar flexion at matched levels of background EMG activity and (for the dynamic plantar flexion) at matched rates of change of EMG activity, it may be argued that the net excitability of the soleus motoneuronal pool was approximately similar in the three tasks and the difference in the amount of inhibition is therefore unlikely to be explained by differences in motoneuronal excitability. Motoneuronal mechanisms as an explanation of the differences in the inhibition should, however, not be ruled out. Although the orderly recruitment of motoneurones has been found to be conserved during most voluntary motor tasks, we have at present no way of knowing whether the same motoneurones are recruited in the stance phase of walking and during tonic and dynamic voluntary movement. The weaker inhibition during walking could thus be explained if motoneurones with a minor input from the Ia inhibitory interneurones contributed more to the EMG activity during walking than during the other two tasks. The soleus muscle is, however, rather homogeneous and consists mainly of type S motor units (Gollnick et al. 1974; Edgerton et al. 1975). We therefore find it unlikely that major changes in recruitment order during different motor tasks occur for this muscle. Furthermore, recent data suggest that the input from the Ia inhibitory interneurones to soleus motor units recruited over a wide range of voluntary force is more or less equal (H. Morita, N. Petersen & J. Nielsen, unpublished observations).
Presynaptic inhibition of Ia afferents on soleus motoneurones has been suggested to be increased in the stance phase of walking as compared to tonic plantar flexion (Capaday & Stein, 1986; Capaday et al. 1995; Faist et al. 1996; Lavoie et al. 1997) and the interneurones mediating presynaptic inhibition are likely also to project onto the synapses of the Ia afferents on the Ia inhibitory interneurones (Eccles et al. 1963; Enriquez-Denton et al. 1996). Increased presynaptic inhibition in the stance phase as compared to tonic and dynamic plantar flexion is thus a possible explanation of the decreased transmission in the reciprocal inhibitory pathway.
In addition to this it may be assumed that differences in the synaptic input to the Ia interneurones also contribute. A major inhibitory input to the interneurones comes from Renshaw cells and other Ia inhibitory interneurones projecting in the opposite direction (Hultborn et al. 1971; Hultborn, 1972). Renshaw cells have been shown to be facilitated during weak and inhibited during strong tonic plantar flexion (Hultborn & Pierrot-Deseilligny, 1979). Towards the end of similar dynamic plantar flexions to those investigated in the present study, Renshaw cells appear to be inhibited (Hultborn & Pierrot-Deseilligny, 1979). Little is known from human studies about the modulation of Renshaw cell activity during walking, but recent experiments suggest that Renshaw cell activity - at least when activated from heteronymous femoral nerve stimulation - may be decreased at the beginning and end of the stance phase and possibly increased in mid-stance (M. Faist, personal communication). This modulation of Renshaw cell activity may also contribute to the modulation of reciprocal inhibition that we have observed in this study, but it seems unlikely that it explains the full pattern of modulation. We thus found that reciprocal inhibition was mainly depressed in early stance, at which time Renshaw cell activity would appear to be least pronounced.
Decreased excitability of the interneurones during walking could also be explained if the opposite Ia interneurones were more strongly activated than during tonic and dynamic voluntary plantar flexion. There is indeed evidence that at least the plantar flexors are much more inhibited in the swing phase than during voluntary movements (Lavoie et al. 1997). It is, however, unclear whether the very strong decrease of the soleus H-reflex in the swing phase documented by these authors is only explained by disynaptic reciprocal inhibition or whether, which seems most likely, other mechanisms also contribute. Nevertheless, mutual inhibition of opposite interneurones is well in line with the small inhibition from plantar flexors to dorsiflexors in the swing phase (Fig. 8) where inhibition from dorsiflexors to plantar flexors is large (Fig. 3). The small inhibition from dorsiflexors to plantar flexors in stance (Figs 3 and 4) could likewise be explained by large inhibition from plantar flexors to dorsiflexors, but we have at present no direct evidence of this.
We have no way of determining whether the observed modulation of disynaptic reciprocal inhibition during walking is caused mainly by central or peripheral mechanisms. However, we found that the inhibition of the soleus EMG activity induced by stimulation of the CPN was similarly modulated when transmission in large diameter afferents was blocked by ischaemia. This suggests that peripheral feedback at least in these afferents alone cannot explain the observed modulation.
Regardless of the exact mechanism the observed changes in reciprocal inhibition are in accordance with the parallel activation of corresponding motoneurones and Ia inhibitory interneurones which was suggested by Lundberg (1970) and later confirmed by experiments investigating the control of reciprocal inhibition during voluntary movements (reviewed in Crone & Nielsen, 1994). When ankle dorsiflexor motoneurones are activated, Ia interneurones projecting to plantar flexor motoneurones are thus activated in parallel, whereas the same interneurones are inhibited when the plantar flexor motoneurones are active (Iles, 1986; Crone et al. 1987). The present experiments have demonstrated that at least in the swing phase this principle also seems to be valid (i.e. small inhibition from plantar flexors to dorsiflexors, large inhibition from dorsiflexors to plantar flexors). In the stance phase we found a small inhibition from the dorsiflexors to the plantar flexors as should be expected, but since it was not possible in any subject to evoke a TA H-reflex in the stance phase the inhibition from ankle plantar flexors to ankle dorsiflexors could not be investigated in this phase.
Functional considerations
The pronounced differences in the descending control of the spinal cord in human subjects as compared to non-primate animals (corticomotoneuronal pathways only exist in primates) makes a direct comparison to the available data regarding the activity of Ia inhibitory interneurones during walking in the cat difficult (Pratt & Jordan, 1987; H. Hultborn, unpublished observations). It is, however, noteworthy that the regulation of the activity of the interneurones that we have provided evidence for in the present study closely resembles the observed modulation of the activity of the interneurones during locomotion in the cat. Interneurones projecting to flexor motoneurones were thus found to be active during extension and silent during flexion (Feldman & Orlovsky, 1975; Pratt & Jordan, 1987). As with these authors, we suggest that the modulation of the reciprocal inhibition may help to inactivate antagonistic motoneurones in the appropriate phases of the walking cycle. Depression of the inhibition in the opposite phases may help to ensure an unhindered activation of the motoneurones by descending and segmental excitatory inputs.
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We are indebted to Hans Hultborn for valuable discussions and suggestions throughout the study. We are grateful to Charles Capaday for comments on a preliminary version of the manuscript. This study was supported by grants from the Danish Health Research Council, The Danish Sports Research Council and the Danish Society of Multiple Sclerosis.
Corresponding author
N. Petersen: Division of Neurophysiology, Department of Medical Physiology, The Panum Institute, University of Copenhagen, Blegdamsvej 3, 2200 Copenhagen N, Denmark.
Email: nicolas{at}mfi.ku.dk
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) and M-waves (
) in the soleus muscle (upper graph) and TA (lower graph) during a step cycle. The ordinate of the graphs is the area of the responses. Each symbol represents the mean of 100 responses. Standard errors of the mean (not shown) were less than 0·03. The data are from a single subject.