Keywords:
8628
Journal of Physiology (1999), 515.3, pp. 929—939
929
Amplitude of the human soleus H reflex during walking and
running
E. B. Simonsen and P. Dyhre-Poulsen*
Institute of Medical Anatomy and *Institute of Medical Physiology, The Panum Institute,
University of Copenhagen, Blegdamsvej 3C, 2200 Copenhagen N, Denmark
(Received 12 August 1998; accepted after revision 8 December 1998)
1. The objective of the study was to investigate the amplitude and modulation of the human
soleus Hoffmann (H) reflex during walking and during running at different speeds.
2. EMGs were recorded with surface electrodes from the soleus, the medial and lateral head of
the gastrocnemius, the vastus lateralis and the anterior tibial muscles. The EMGs and the
soleus H reflex were recorded while walking on a treadmill at 4·5 km h¢ and during running
at 8, 12 and 15 km h¢.
3. The amplitudes of the M wave and the H reflex were normalized to the amplitude of a
maximal M wave elicited by a supramaximal stimulus just after the H reflex to compensate
for movements of the recording and stimulus electrodes relative to the nerve and muscle
fibres. The stimulus intensity was set to produce M waves that had an amplitude near to
25% of the maximal M wave measured during the movements. As an alternative, the
method of averaging of sweeps in sixteen intervals of the gait cycle was applied to the data.
In this case the amplitude of the H reflex was expressed relative to the maximal M wave
measured whilst in the standing position.
4. The amplitude of the H reflex was modulated during the gait cycle at all speeds. During the
stance phase the reflex was facilitated and during the swing and flight phases it was
suppressed. The size of the maximal M wave varied during the gait cycle and this variation
was consistent for each subject although different among subjects.
5. The peak amplitude of the H reflex increased significantly (P = 0·04) from walking at
4·5 km h¢ to running at 12 and 15 km h¢ when using the method of correcting for
variations of the maximal M wave during the gait cycle. The sweep averaging method
showed a small but non-significant decrease (P = 0·3) from walking to running at 8 km h¢
and a small decrease with running speed (P = 0·3). The amplitude of the EMG increased
from walking to running and with running speed.
6. The relatively large H reflex recorded during the stance phase in running indicates that the
stretch reflex may influence the muscle mechanics during the stance phase by contributing to
the motor output and enhancing muscle stiffness.
The modulation and amplitude of the human soleus H reflex
during walking and running have been investigated by
Capaday & Stein (1987). They reported that the transition
from walking at 4·5 km h¢ to running at 8 km h¢ caused a
statistically significant decrease in the peak amplitude of
the human soleus H reflex. In an ensuing study Edamura et
al. (1991) measured the soleus H reflex during walking at
speeds from 2·0 to 7·5 km h¢ and during running from 5·0
to 9·0 km h¢. They also reported that the peak amplitude
of the soleus H reflex was always lower during running than
during walking. In the latter study the subjects were tested
during both walking and running at identical speeds. The
H reflex measuring technique bypasses the muscle spindle
and measures the central component of the monosynaptic
part of the stretch reflex, i.e. the efficacy of the transmission
from Ia afferents to the á-motoneurones in the spinal cord.
We have previously reported that the amplitude of the
maximal M wave (Mmax) in soleus muscle varied considerably
but systematically during walking (Simonsen et al. 1995).
To expand on our findings we proceeded to measure the
maximal M wave amplitude and the H reflex amplitude
during various motor tasks, including running. These
experiments showed that the soleus H reflex was not lowered
during running and we therefore decided to investigate this
observation systematically. Since the highest running speed
previously investigated was 9·0 km h¢, we decided to
930
E. B. Simonsen and P. Dyhre-Poulsen
compare walking at 4·5 km h¢ with running at 8·0, 12·0
and 15·0 km h¢. Preliminary results of the present study
have been published earlier in abstract form (Simonsen &
Dyhre-Poulsen, 1995).
Subjects
METHODS
Seven male subjects gave voluntary written consent to participate
in the experiments after being informed about the experimental
conditions. The study was approved by the local ethics committee.
The subjects were well trained but not specialized in running events.
Their mean age was 28 years (range, 24—35 years), mean height
was 1·85 m (range, 1·72—1·95 m) and mean body weight was 76 kg
(range, 65—89 kg).
Experimental procedure
When the subjects arrived EMG electrodes were mounted and the
site of nerve stimulation located. The maximal M wave and the
H reflex amplitude were measured at rest in the standing position.
EMG activity was measured during walking at 4·5 km h¢ and
during running at 8·0, 12·0 and 15·0 km h¢ without nerve
stimulation. Finally, the soleus H reflex was measured during the
same walking and running conditions. The subjects were walking
and running on a motor-driven treadmill (HS_1200; Technogym)
and were allowed to rest freely during the recording sessions to
avoid fatigue. The sessions were in random order and a total
experimental session lasted about 4 h. All measurements were
performed on the same day on the right leg.
Electromyography
Surface electrodes (Medicotest Q_10-A prefilled ECG electrodes) were
mounted 2 cm apart (bipolar) over five muscles. The electrodes were
placed as follows: for the soleus, about 15 cm above the calcaneus
over the gastrocnemius aponeurosis but below the muscle fibres of
the gastrocnemius heads; for the anterior tibial muscle about 12 cm
below the caput fibulae; for the lateral and medial head of the
gastrocnemius muscle, about 5 cm below the caput fibulae; and for
the vastus lateralis muscle about 16 cm above the patella. The
electrodes were connected to small custom-built preamplifiers
(input impedance, 80 MÙ) taped to the skin. The EMG signals were
then led through long shielded wires to custom-built amplifiers
with a frequency response between 20 Hz and 10 kHz. The set-up
permitted the subjects to move freely on the treadmill and the
preamplifiers reduced movement artefacts effectively.
Goniometry and microswitches
The ankle joint position was measured with an electrogoniometer
(M-series twin axis; Penny & Giles) placed on the lateral side of the
ankle joint. Foot—ground contact was detected by microswitches
placed under the heel and forefoot.
The H reflex
The soleus H reflex was elicited by stimulation of the tibial nerve
using an AgCl cathode in the popliteal fossa (Medicotest Q_10-A)
and a 40 mm diameter anode placed over the patella. The optimum
site of nerve stimulation was first located by a hand-held electrode
and it was a criterion that the soleus Ia afferents could be stimulated
selectively at low stimulus intensities. The stimulus was a 1 ms
square pulse delivered by a custom-built constant current stimulator.
The maximal M wave amplitude (Mmax) and the maximal H reflex
amplitude were measured during rest with the subjects in a
standing position. The stimulus intensity necessary to elicit Mmax
J. Physiol. 515.3
was determined and then increased by a factor of 2 prior to
measurement of Mmax. This doubled stimulus intensity was also
used to elicit Mmax during locomotion. The stimuli were given every
2 s during locomotion, which was slightly out of phase with the gait
cycle. In this way the stimuli were dispersed randomly over the gait
cycle. An integrator was reset by the microswitch placed under the
subject’s heel and a ramp function was generated from 0 to 2 V over
a 2 s period. The amplitude of the ramp function at the time of
stimulation was used to compute the time interval that had elapsed
since the preceding heel strike. A second, but supramaximal,
stimulus elicited a maximal M wave 60 ms after the first stimulus.
The Mmax therefore appeared just after the H reflex elicited by the
first stimulus (Fig. 1). The experiments were controlled by a ‘selftaught’ computer program written in ASYST and running on a
personal computer (Dyhre-Poulsen et al. 1993; Voigt et al. 1998).
The gait cycle was divided into twenty time slices for which the
computer ‘taught’ itself the appropriate stimulus intensity, which
varied during the gait cycle. The peak-to-peak amplitude of the
M wave was assumed to reflect the effective stimulus strength and
the computer calculated the stimulus intensity necessary to evoke an
M wave that was 25% of the actual Mmax measured in the same
sweep. Thus the computer program would go through the following
procedure every 2 s: (1) determine the actual time slice (out of 20) in
the gait cycle by measuring the actual value of the ramp signal reset
by the preceding heel strike; (2) look up the last notified stimulus
strength for the actual time slice; (3) send the stimulus information
to the stimulator and trigger the stimulator; (4) sample the soleus
EMG signal at 20 kHz for 120 ms; (5) measure the peak-to-peak
amplitudes of the M wave, the H reflex and Mmax; (6) determine
whether to accept or reject the sweep (the target amplitude for the
M wave was 25 ± 10 % of Mmax measured in the same sweep);
(7) store the sweep and the measured results on disk; and (8) adjust
and update the stimulus strength for the actual time slice.
During the first 5—10 min of an experimental session the program
showed a low score of acceptable stimulations, but after having
‘learned’ how to stimulate a specific subject, almost every
stimulation resulted in acceptable M waves.
The ‘learning algorithm’ of the program was quite simple. Initially
the stimulus intensity in all twenty time slices was set to 25% of
Mmax measured at rest. At each stimulation the computer program
measured the amplitude of Mmax and calculated the target 25%
M wave. If the measured M wave differed from the target then the
program would calculate an estimated new stimulus intensity based
on the reference excitability curve of the actual subject and store
the new value to be used next time. In practice it was found
convenient to add or subtract only 50% of the estimated difference
in stimulus intensity. In this way the program would gradually
turn up or turn down the stimulus intensity in each time slice
during the experiment.
The purpose of using the ‘self-teaching’ program was (i) to adjust
the stimulus strength to fluctuations of the maximal M wave during
the gait cycle and (ii) to avoid subject fatigue by reducing the total
experimental time.
Signal treatment and calculations
During off-line analysis the gait cycle was divided into sixteen time
slices (to match previous studies) and the peak-to-peak amplitudes
of the H reflex, expressed as a percentage of the actual Mmax in
every sweep, were averaged for each time slice.
The H reflex amplitude was also calculated as the percentage of
Mmax during standing. During this procedure the selection process
J.
Physiol.
515.3
931
H ref
lex during walking and running
was repeated off-line to accept only M waves 25 ± 10 % of max
during standing. Then the accepted sweeps were averaged for each
of the sixteen time slices by the method described by Capaday &
Stein (1986) (Fig. 1). The background EMG was thereby removed
by the averaging procedure. Finally the peak-to-peak amplitude of
the H reflex was measured for each slice and expressed as a
percentage of max during standing at rest to compare the two
different methods.
The EMG signals recorded without stimulation were sampled at
1000 Hz, high-pass filtered at 20 Hz and low-pass filtered at 500 Hz
(fourth order Butterworth digital filters with no phase lag). After
full wave rectification linear envelopes were obtained with a 15 Hz
low-pass filter. Then twelve sweeps, corresponding to twelve step
cycles, were averaged. The goniometer signal was low-pass filtered
at 50 Hz and averaged over twelve step cycles. The onset and offset
of the EMG signals were determined visually on a computer monitor
with an accuracy of 1 ms. Peak amplitude, mean amplitude and
integrated EMG (IEMG) were calculated for the activity period of
each muscle. IEMG was defined as the area under the linear
envelope expressed in microvolt seconds.
RESULTS
M
M
Statistical analysis
Differences in the selected parameters were tested between walking
and the three running speeds by the Friedman test for several
related samples (two-tailed) (Conover, 1980). The level of significance
was set to 5% in all cases. Only one value for each parameter is
returned by this test; however, when < 0·05 was obtained,
differences between the four gait conditions were examined by
multiple comparisons (Conover, 1980).
P
P
The mean amplitude of the maximal M wave during standing
was 9·1 mV (range, 7·2—10·7 mV) for the seven subjects. The
maximal H reflex, also measured during standing, was on
average 5·2 mV (range, 3·1—8·2 mV) corresponding to 56%
of max. The target M wave amplitude was set to 25% of
max measured during locomotion. However, a range of
±10% was considered acceptable. Off-line analysis of the
data from one subject showed no change in the mean H reflex
amplitude when the acceptance criteria were narrowed to
25 ± 5 %. Table 1 displays the amplitudes of the average
M waves elicited for each subject and the standard deviations.
On average, the M wave amplitude seemed to decrease from
2·1 mV during walking to 1·91 mV during running at
15 km h¢. However, no statistically significant differences
regarding the M wave amplitudes were observed between the
four gait conditions.
The modulation of the soleus H reflex during walking was
similar to that in earlier reports (Capaday & Stein, 1986,
1987; Crenna & Frigo, 1987; Simonsen
1995). The
amplitude of the reflex increased during the stance phase and
the reflex was suppressed during the swing phase (Figs 2
and 3). The modulation of the reflex during running was
also in accordance with previous reports (Capaday & Stein,
1987; Edamura
1991) as the reflex was facilitated
M
M
Figure 1. H reflex modulation of one subject during walking at
4·5 km h¢
The gait cycle was divided into 16 time slices starting at the bottom of
the figure corresponding to heel strike. In each slice 5 events are
visible, from left to right: s1, the first stimulus artefact; M, the
M wave; H, the H reflex; s2, the second stimulus artefact; and Mmax,
the maximal M wave. The duration of each sweep was 120 ms. The
H reflex appeared after approximately 35 ms and the second stimulus
(s2) was elicited 60 ms after the first stimulus (s1). The signals in each
time slice represent an average of multiple sweeps obtained by the
method described earlier by Capaday & Stein (1987). It can be seen
that the H reflex was facilitated during the stance phase, but
suppressed during the swing phase.
et
et
al.
al.
932
J. Physiol. 515.3
E. B. Simonsen and P. Dyhre-Poulsen
––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––
Table 1. M wave and H reflex amplitudes
––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––
Peak
Peak
Subject
Mean Mmax
Mmax
Mean M
M
H reflex H reflex (C&S)
(mV)
(mV)
(mV)
(mV)
(% Mmax)
(% Mmax)
––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––
A. 4·5 km h¢
BL
9·07
0·46
2·14
0·53
28·6
33·2
LK
7·30
0·40
1·71
0·40
47·1
68·1
JM
5·75
1·80
1·42
0·55
42·6
38·2
NI
8·98
0·63
2·32
0·50
43·2
53·1
SO
11·45
0·75
2·68
0·57
47·7
52·3
MO
10·25
1·06
2·40
0·50
41·0
48·6
HE
8·21
0·77
2·00
0·52
38·0
42·7
Mean
8·72
0·84
2·10
0·51
41·2
48·0
––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––
B. 8·0 km h¢
BL
8·46
0·49
1·96
0·48
33·2
31·7
LK
6·90
0·67
1·61
0·41
50·5
68·3
JM
6·64
2·89
0·96
0·84
54·9
38·2
NI
8·41
0·97
2·11
0·53
52·5
50·8
SO
10·98
1·02
2·65
0·58
47·7
47·3
MO
11·02
1·62
2·67
0·65
50·0
53·2
HE
8·85
1·62
2·09
0·60
36·4
38·9
Mean
8·75
1·33
2·01
0·58
46·5
44·2
––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––
C. 12·0 km h¢
BL
7·99
0·52
2·00
0·49
37·8
31·9
LK
7·07
0·61
1·69
0·46
52·9
58·4
JM
6·62
3·10
1·46
0·71
44·4
20·7
NI
7·39
1·17
1·98
0·46
60·9
46·5
SO
9·05
0·94
2·22
0·54
41·2
36·0
MO
11·35
1·72
2·67
0·76
55·7
62·6
HE
8·28
1·96
2·00
0·63
43·7
41·8
Mean
8·25
1·43
2·00
0·58
48·1
43·7
––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––
D. 15·0 km h¢
BL
7·95
0·62
1·84
0·42
36·8
37·0
LK
6·73
0·64
1·51
0·64
52·8
57·9
JM
6·80
3·68
1·69
1·12
61·0
11·3
NI
7·39
1·20
1·89
0·48
54·1
46·5
SO
7·63
1·37
1·81
0·56
41·6
23·5
MO
11·04
1·69
2·79
0·79
47·9
44·7
HE
7·98
2·15
1·85
0·66
49·5
42·8
Mean
7·93
1·62
1·91
0·67
49·1
37·7
––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––
Columns are, from left to right: the mean maximal M wave amplitude (Mmax) with standard deviation (
measured during locomotion, the mean M wave amplitude (M) with used as the conditioning stimulus
during locomotion, the peak H reflex measured during locomotion expressed as the percentage of Mmax also
measured during locomotion, and the peak H reflex measured during locomotion but expressed as the
percentage of Mmax during standing (peak H reflex (C&S)). A, walking at 4·5 km h¢. B, running at
8·0 km h¢. C, running at 12·0 km h¢. D, running at 15·0 km h¢.
––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––
s. d.
s. d.
s. d.)
s. d.
during the stance phase and suppressed during the swing
and flight phases (Figs 2 and 3).
Using the sweep averaging method of Capaday & Stein
(1987) and relating the peak H reflex amplitude to Mmax
during standing showed that the reflex amplitude decreased
from 48·0% of Mmax during walking to 44·2% during
running at 8 km h¢. In contrast to the results of Capaday &
Stein (1987) this decrease was small and statistically
non_significant (Table 1 and Fig. 4). Using the method of
correcting for fluctuations in Mmax showed that the peak
H reflex amplitude increased from 41·2% of Mmax during
walking to 46·5% during running at 8 km h¢ (Table 1 and
Fig. 4). However, this difference was also not statistically
J. Physiol. 515.3
H reflex during walking and running
significant. According to the statistical evaluation, the peak
H reflex amplitude was therefore unchanged between
walking at 4·5 km h¢ and running at 8 km h¢. The results
from the faster running speeds followed the same pattern.
Using the method of the present study showed a further
increase in reflex amplitude and the statistical analysis
showed significantly higher amplitudes during running at
12 and 15 km h¢ compared with walking (Table 1 and
Fig. 4). The H reflex amplitude was 6·9% higher during
933
running at 12 km h¢ than during walking (P = 0·04), and
at 15 km h¢ it was 7·9% higher than during walking
(P = 0·04) (the percentages refer to % Mmax and not
percentage increase). No significant differences were observed
between running conditions. When the method of Capaday
& Stein (1987) was used, it showed that the reflex amplitude
decreased with running speed, but no statistically significant
differences were observed between the four conditions
(P = 0·3) (Table 1 and Fig. 4).
Figure 2. Recordings from the same subject illustrated for 4 gait situations
The gait situations were: walking at 4·5 km h¢ (A); running at 8 km h¢ (B); running at 12 km h¢ (C);
and running at 15 km h¢ (D). For each of the 4 figures the following recordings are shown from bottom to
top: the soleus EMG (SOL) and the tibialis anterior EMG (TA) (linear envelopes averaged from 12 sweeps);
the ankle angle; the amplitude of the maximal M wave (Mmax) of the soleus muscle; and finally the amplitude
of the soleus H reflex expressed as percentage Mmax and corrected for variations of Mmax during the gait
cycle. For the H reflex and Mmax, each cross represents one stimulation given every 2 s. The stance phase
starts on the left at 0 ms and ends at the vertical dashed line. Note that the scales for the soleus and
anterior tibial EMG differ from A to D.
934
E. B. Simonsen and P. Dyhre-Poulsen
In general, the mean and peak amplitudes of the EMG
activity and the integrated EMG increased two- to threefold from walking at 4·5 km h¢ to running at 8 km h¢ and
further to running at 12 and 15 km h¢. Only eleven out of
seventy-five comparisons resulted in non-significant
differences (Table 2).
In the present study a supramaximal stimulus was applied
in every sweep to measure variations in Mmax. To test any
Figure 3. H reflex modulations
J. Physiol. 515.3
possible influence of the supramaximal stimuli on the size of
the H reflex, reference excitability curves with and without
the supramaximal stimuli were recorded in two subjects
during resting conditions (Fig. 5). It was clear from these
measurements that the size of the H reflex was unaffected
by the supramaximal stimuli (double stimulus condition).
Theoretically, it is possible that the supramaximal stimulus
given in every sweep could depress the size of the H reflex.
In the top tracings, the modulation of the soleus H reflex is shown as the average from 7 subjects during
walking at 4·5 km h¢ (+), running at 8 km h¢ (Ê), running at 12 km h¢ (1) and running at 15 km h¢ (²).
In the left column the results were obtained by the method of the present study, in which the maximal
M wave (Mmax) was measured in every sweep (Method 1). In the right column the same data were obtained
by the method described by Capaday & Stein (1987) (Method 2 (C & S)). For each of the two methods the 4
lower tracings show individual data for each subject and for each velocity investigated. Each of the 7 subjects
is represented by a specific symbol. All data are expressed as a percentage of Mmax. For Method 1, Mmax
was measured in every sweep while for Method 2, the Mmax measured in the standing position was used for
normalization. For both methods, only M waves between 15 and 35% of Mmax were accepted. The gait cycle
was divided into 16 time slices and normalized with heel strike at 0 and 100%.
J. Physiol.
515.3
H reflex during walking and running
935
––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––
Table 2. The mean, peak and IEMG for the soleus, medial gastrocnemius, vastus lateralis and
anterior tibial muscles at 4·5 km h¢ (walking) and for 3 running speeds
––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––
4·5 km h¢
8·0 km h¢
12·0 km h¢
15·0 km h¢
––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––
SOL mean
72 (10)
134 (21) n.s.12
151 (21)
165 (20)
SOL peak
160 (16)
346 (54)
385 (67)
401 (50)
SOL IEMG
107 (18)
383 (85)
487 (93)
556 (93)
n.s.15
GM mean
73 (7)
183 (22) n.s.12
224 (25)
233 (20)
GM peak
192 (13)
452 (65)
516 (56) n.s.15
588 (48)
GM IEMG
124 (17)
518 (89)
745 (89)
767 (72)
GL mean
38 (7)
131 (16)
164 (19)
203 (25)
GL peak
130 (24)
353 (52)
447 (55)
498 (52)
GL IEMG
62 (15)
364 (66)
514 (76)
719 (100)
VL mean
25 (6)
101 (12)
128 (15) n.s.15
149 (18)
VL peak
64 (17)
301 (44)
382 (57)
423 (42)
VL IEMG
55 (13)
279 (41)
394 (52)
510 (79)
n.s.12
TA mean
50 (6)
81 (7) n.s.12
100 (10)
127 (14)
TA peak
164 (18) n.s.8,12
237 (21) n.s.12
332 (39) n.s.15
424 (53)
TA IEMG
105 (44)
126 (19)
163 (21)
217 (32)
––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––
SOL, soleus muscle; GM, medial gastrocnemius muscle; GL, lateral gastrocnemius muscle; VL, vastus
lateralis muscle; TA, anterior tibial muscle; IEMG, integrated EMG. All values are the means of 7 subjects
with the s.e.m. in parentheses. All comparisons across speeds are significant unless indicated by n.s. The
number after n.s. denotes the velocities that are insignificant (P > 0·05).
––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––
However, we measured an increased H reflex during running,
and the peak H reflex during walking was seemingly not
lower than reported in previous studies. A direct comparison
of amplitudes would require identical electrodes and interelectrode distance. In the present study the inter-electrode
distance was 2 cm, but this information is lacking in the
previous reports (Capaday & Stein, 1987; Edamura et al.
1991).
The stimulus intensity necessary to elicit Mmax in the
standing subjects was 19 mA on average (range, 12—21 mA).
During locomotion these values were doubled to elicit Mmax.
However, as the maximal output of the stimulator was
90 mA, the intensities used were far from the maximum
capacity (Fig. 5).
Figure 4. Peak amplitude of the soleus H reflex during walking (4·5 km h¢) and during 3
running speeds
Hatched columns represent values obtained by the method of the present study where the maximal M wave
(Mmax) was measured in every sweep. Open columns represent values obtained by the method of Capaday
& Stein (1987) where variations of Mmax during the gait cycle are not accounted for. The bars are mean
values of 7 subjects and the error bars are + s.e.m. *Statistically significantly different from walking at
4·5 km h¢ (P < 0·05).
936
E. B. Simonsen and P. Dyhre-Poulsen
DISCUSSION
Surprisingly, the results of the present study showed that
the peak amplitude of the soleus H reflex was statistically
similar during walking at 4·5 km h¢ and during running at
8 km h¢. Group mean values showed an increasing trend
from walking to running using the method of the present
study and a decreasing trend using the method introduced
by Capaday & Stein (1987). However, both differences were
statistically non-significant. For the two faster running
speeds (12 and 15 km h¢) almost the same pattern was
observed. The reflex amplitude decreased a little further but
insignificantly using the method of Capaday & Stein (1987)
while a relatively small but statistically significant increase
was observed using the method of the present study. Despite
the statistical probabilities it should be emphasized that
Figure 5. Recordings of the maximal M wave
J. Physiol. 515.3
large inter-individual differences were observed (Table 1). It
was, however, clear that these differences were much smaller
when using the method of the present study (Table 1 and
Fig. 4). Unfortunately, group means and individual values
are missing in the two previous studies. It therefore remains
an open question if the observed variance is due to
methodological problems or inter-individual differences.
Methodological considerations
It is possible that the supramaximal stimuli may disturb the
movement pattern of the subjects. However, the stimuli given
every 2 s were out of phase with the gait cycle, so that the
subjects were unable to predict the stimulus in the step cycle.
Furthermore, in several cases supramaximal stimuli were
applied randomly rather than in every sweep, and this was
never observed to influence the modulation or the amplitude
The upper panels show the relation between stimulus intensity and the recorded M wave for two subjects. It
can be seen that the maximal M wave was achieved at a stimulation intensity of about 20 mA and stayed
relatively constant up to the maximum capacity of the stimulator. ², sweeps with a single stimulation;
1, sweeps with a double stimulation. In the latter condition the intensity of the second stimulus was set to
42 mA for both subjects. The lower panels show reference excitability curves of the same two subjects with
(1) and without (²) the second but supramaximal stimulus applied to every sweep. It can be seen that the
‘double stimulus’ condition did not affect the amplitude of the H reflex.
J.
Physiol.
515.3
937
H ref
lex during walking and running
of the H reflex. The duration of each step cycle was recorded
and the use of supramaximal stimuli never appeared to
influence this duration. The subjects verbally reported that
the steps after the stimulus were perceived as normal steps.
In the present study M waves with an amplitude of
25 ± 10 % of max were accepted as stimuli for the H reflex.
Due to variations in max during walking and running the
size of these M waves was expressed relative to the actual
max measured in the same sweep. In the two previous
studies the stimulus intensity was instead regulated to
obtain a preset absolute M wave (in mV) during all phases of
the movement (Capaday & Stein, 1987; Edamura
1991). In these studies no values for max during resting
conditions were mentioned, which precludes comparison with
the stimulus intensities in the present study. Theoretically,
the use of exceedingly high stimulus intensities will decrease
the size of the H reflex and confine the effects measured to
the smaller motoneurones, i.e. those not involved in the
formation of the M wave. Selective stimulation of Ia
afferents in the tibial nerve will often produce the largest
H reflex in the soleus muscle, but the use of no M waves or
very small ones is not practical during movement because
the M wave is used as a measure and control of the effective
stimulus strength. Using M waves below 15% of max
presents a problem due to the underlying EMG during
voluntary muscle activity in the stance phase. Although
averaging removes the underlying EMG, this may still pose
a problem since the size of the M wave must be measured in
every sweep prior to averaging. Otherwise, wrong (too high
or too low) stimulus strengths could have been applied. In
the study of Capaday & Stein (1987), averaged M waves of
about 2 mV are depicted in their Fig. 1 and about 1·5 mV in
their Fig. 2. Moreover, they state that for some of their
subjects it was necessary to use rather high M waves
corresponding to the falling part of the M wave—H reflex
recruitment curve. A comparison between the present and
previous studies regarding the absolute size of the H reflex
in millivolts is difficult due to the lack of mean values and
inter-electrode distances in the previous reports. In the
M
M
M
et
al.
M
M
Figure 6. Two subjects with a large difference in
variation of Mmax shown during running at 8 km h¢
The subject on the left showed a rather small variation in max
during the gait cycle, while the subject on the right showed large
variations. The H reflex is expressed as the percentage of the
maximal M wave ( max) measured in every sweep (²) and
during standing (0) (Capaday & Stein, 1987). For the subject
shown on the right this variation resulted in a clearly lower
H reflex amplitude during the stance phase of running when
using the method of Capaday & Stein (1987). The discrepancy
could not be demonstrated for the subject shown on the left.
The reason for the disparity is likely to be the use of an
excessively high stimulus intensity during the stance phase for
the subject shown on the right (see text for further explanation).
M
M
present study the peak H reflex during walking averaged
3·3 mV (range, 2·7—4·6 mV) while the previous reports
graphically presented values of approximately 4·8, 2·9 and
2·7 mV (Edamura
1991) and 8·0 and 1·8 mV (Capaday
& Stein, 1987). Therefore, it seems unlikely that the
stimulus intensities used in the present study were notably
higher than those of the earlier studies.
It may be considered a problem that max was elicited
60 ms after the stimulus for the conditioning M wave.
However, the twenty time slices represented each 60 ms of
the total walking cycle and max never appeared to change
considerably within one time slice. Off-line analysis where
the max modulation was shifted one time slice (60 ms)
backwards did not show any visible differences in the
H reflex modulation.
et
al.
M
M
M
Variations in the maximal M wave
In the present study the variations of max during the step
cycle were systematic and consistent for each subject.
However, the variation in the size of max during the step
cycle differed among the subjects. Figure 6 depicts the
variation of max and the modulation of the H reflex during
running at 8 km h¢ for two subjects. The subject JM showed
a large variation in max with the lowest values during the
stance phase. Subject NI, on the other hand, showed less
variation in max and the lowest values during the flight
phase. Further, it is notable that using both the methodology
of the present study and the one used in the previous
studies would yield identical H reflex amplitude and
modulation values for a subject with rather small variations
in max, while large discrepancies would be seen in a subject
with a large variation in max. In subject JM, max was
10·6 mV during rest while it was only •5 mV during the
stance phase of running (Fig. 6). Using M waves of about
25% of resting max in this phase of the movement would
therefore result in lower H reflexes due to methodology (too
high stimulation) rather than presynaptic or postsynaptic
inhibition in the spinal cord. Post-experimentally we selected
M waves close to 5 mV in subject JM during the stance
M
M
M
M
M
M
M
M
M
938
E. B. Simonsen and P. Dyhre-Poulsen
phase of running and found H reflexes close to zero. This
indicates that the true Mmax was about 5 mV in this phase
of the movement for this subject. The stimulus intensity
necessary to elicit Mmax in this subject during standing was
21 mA. Accordingly, during locomotion the stimulus
intensity was set to 42 mA. However, as the measured
amplitudes of the potentials were displayed on-line during
the experiments the stimulus intensity was increased to
90 mA for this subject. This did not increase the rather low
Mmax measured during the stance phase of running.
The reason why Mmax varies in amplitude during the step
cycle is most likely to be that the muscle fibres move under
the skin with respect to the surface electrodes. This will
change the muscle geometry and the electrical potentials
will be conducted to the electrodes under circumstances
constantly changing during the movement. This phenomenon
has been shown to influence the recorded potentials
significantly (Gerilowsky et al. 1989). The fibre movement is
believed to be caused by shortening and lengthening of fibres
and changes in the angle of fibre pennation (Gerilowsky et
al. 1989). The results of the present study show that it is not
only necessary to control the stimulus intensity due to
movements of the tibial nerve relative to the stimulus
electrodes as suggested by Capaday (1997), but that it may be
even more important to compensate for variations in Mmax
due to changes in muscle geometry.
Expression of the H reflex
The absolute amplitude in millivolts of the H reflex depends
strongly on anatomical factors, i.e. differences in the
thickness of axons from Ia afferents and á_motoneurones.
Expressing the H reflex as a fraction of the maximal M wave
does not eliminate this problem on an individual basis.
However, when a whole group of subjects is analysed the
Hreflex amplitude: Mmax ratio may provide a means for
comparing the reflex excitability during different motor
tasks and between different experiments. The H reflex may
also be related to the level of voluntary EMG activity as used
by Capaday & Stein (1986, 1987) and Edamura et al. (1991).
In our opinion this is inappropriate in the case of walking
and running, where the H reflex (after our normalization
procedure) may increase by about 20% while the soleus
peak EMG increases by about 250%.
Functional implications
When Capaday & Stein reported a lower H reflex amplitude
during running than walking, it was suggested that a
reduction of the reflex gain during running could be
necessary because of the potential danger of instability of
the motoneurone pool (tremor) caused by saturation of the
pool (Capaday & Stein, 1987). However, assuming the
excitability of the H reflex in the present study was very
close to maximum during running, it can be concluded that
saturation of the motoneurone pool is not a potential danger
during running. Instead we suggest that the stretch reflex
(as measured by the H reflex) plays a significant role during
running. Facilitation of the central component of the stretch
J. Physiol. 515.3
reflex indicates strongly that part of the motor output
comes from the stretch reflex unless the spindle afferents are
deactivated by reduced ã_activation. The latter would seem
unlikely since the stretch reflex and the H reflex, though
not completely identical, never undergo changes in the
opposite direction (Akazawa et al. 1982; Aldridge & Stein,
1982). At all three running speeds the duration of the stance
phase was about 300 ms and the duration of the soleus
lengthening contraction about 150—200 ms, as recorded by
the goniometer (Fig. 2). Assuming an electrical latency for
the stretch reflex of about 40 ms and an electromechanical
delay of about 50 ms with respect to the muscle (BiglandRitchie et al. 1983) there is time for the stretch reflex to be
elicited during a lengthening contraction in the stance
phase which could then assist the subsequent shortening
contraction. This would also correspond with Dietz et al.
(1979), who found a significant contribution of the stretch
reflex during sprint running evaluated by EMG. Finally, if
the stretch reflex can enhance muscle stiffness, as reported
by Hoffer & Andreassen (1981) and by Sinkjòr et al. (1988),
a considerable amount of elastic energy could be stored in
the tendons and be re-used during push-off (Voigt et al.
1995b), possibly leading to increased mechanical efficiency
during running (Voigt et al. 1995a).
Akazawa, K., Aldridge, J. W., Steeves, J. D. & Stein, R. B.
(1982). Modulation of stretch reflexes during locomotion in the
mesencephalic cat. Journal of Physiology 329, 553—567.
Nonlinear properties of
stretch reflex studied in the decerebrate cat. Journal of
Neurophysiology 47, 179—192.
Aldridge, J. W. & Stein, R. B. (1982).
Bigland-Ritchie, B., Johansson, R., Lippold, O. C. & Woods, J. J.
(1983). Contractile speed and EMG changes during fatigue of
sustained maximal voluntary contractions. Journal of
Neurophysiology 50, 313—324.
Capaday, C. (1997). Neurophysiological methods for studies of the
motor system in freely moving human subjects. Journal of
Neuroscience Methods 74, 201—218.
Capaday, C. & Stein, R. B. (1986). Amplitude modulation of the
soleus H-reflex in the human during walking and standing. Journal
of Neuroscience 6, 1308—1313.
Capaday, C. & Stein, R. B. (1987). Difference in the amplitude of the
human soleus H reflex during walking and running. Journal of
Physiology 392, 513—522.
Conover, W. J. (1980). Practical Nonparametric Statistics, 2nd edn.
John Wiley & Sons Inc., New York.
Crenna, P. & Frigo, C. (1987). Excitability of the soleus H-reflex arc
during walking and stepping in man. Experimental Brain Research
66, 49—60.
Dietz, V., Schmidtbleicher, D. & Noth, J. (1979). Neuronal
mechanisms of human locomotion. Journal of Neurophysiology 42,
1212—1222.
Dyhre-Poulsen, P., Simonsen, E. B., Voigt, M. & Bojsen-Mœller,
F. (1993). How to record H-reflexes during natural movements.
Proceedings of the International Congress on Biomechanics XIV,
p. 374. Paris, France.
J. Physiol. 515.3
H reflex during walking and running
Edamura, M., Yang, J. F. & Stein, R. B. (1991).
Factors that
determine the magnitude and time course of human H-reflexes in
locomotion. Journal of Neuroscience 11, 420—427.
Gerilowsky, L., Tsvetinov, P. & Trenkova, G. (1989). Peripheral
effects on the amplitude of monopolar and bipolar H-reflex
potentials from the soleus muscle. Experimental Brain Research 76,
173—181.
Hoffer, J. A. & Andreassen, S. (1981). Regulation of soleus muscle
stiffness in premammillary cats; intrinsic and reflex components.
Journal of Neurophysiology 45, 267—285.
Simonsen, E. B. & Dyhre-Poulsen, P. (1995). Excitability of the
soleus H reflex during running. Medicine and Science in Sports and
Exercise, suppl. 27, 968.
Simonsen, E. B., Dyhre-Poulsen, P. & Voigt, M. (1995).
Excitability of the soleus H reflex during graded walking in
humans. Acta Physiologica Scandinavica 153, 21—32.
Sinkjòr, T., Toft, E., Andreassen, S. & Hornemann, B. C. (1988).
Muscle stiffness in human ankle dorsiflexors: intrinsic and reflex
components. Journal of Neurophysiology 60, 1110—1121.
Voigt, M., Bojsen-Mœller, F., Simonsen, E. B. & Dyhre-Poulsen,
P. (1995a). The influence of tendon Youngs modulus, dimensions
and instantaneous moment arms on the efficiency of human
movement. Journal of Biomechanics 28, 281—291.
Voigt, M., Dyhre-Poulsen, P. & Simonsen, E. B. (1998). Modulation
of short latency stretch reflexes during human hopping. Acta
Physiologica Scandinavica 163, 181—194.
Voigt, M., Simonsen, E. B., Dyhre-Poulsen, P. & Klausen, K.
(1995b). Mechanical and muscular factors influencing the
performance in maximal vertical jumping after different pre-stretch
loads. Journal of Biomechanics 28, 293—307.
Acknowledgements
This study was supported by The Danish Research Council for Sport
and The Danish Elite Sports Association.
Address for correspondence
E. B. Simonsen: Institute of Medical Anatomy, Section C, Panum
Institute, University of Copenhagen, Blegdamsvej 3C, DK 2200
Copenhagen N, Denmark.
Email: E.Simonsen@mai.ku.dk
939