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Soleus H-reflex dynamics during fast plantarflexion in humans
Journal of Electromyography and Kinesiology 12 (2002) 367–374 www.elsevier.com/locate/jelekin
Soleus H-reflex dynamics during fast plantarflexion in humans Masaki Fumoto a, Tomoyoshi Komiyama b,∗, Yoshiaki Nishihira c b
a Department of Physiology, Toho University School of Medicine, Tokyo, Japan Department of Health and Sport Sciences, Faculty of Education, Chiba University, 1-33 Yayoicho, Inage-ku, Chiba City 263-8522, Japan c Institute of Health and Sports Sciences, University of Tsukuba, Japan
Received 22 March 2001; received in revised form 30 January 2002; accepted 23 February 2002
Abstract The relationship between the size of the soleus (Sol) Hoffmann (H-) reflex and the level of background (BG) electromyographic (EMG) activity was examined during plantarflexing at different force levels. The experiments were carried out on seven healthy male subjects aged 20–37 years. The subjects were asked to perform fast plantarflexion under a reaction-time condition. The amounts of contraction force were 10, 20, 50 and 80% of maximum voluntary contraction (MVC). Since the maximum size of the M-wave (Mmax) changed systematically during the plantarflexion, we tried to maintain the size of the reference M-wave, an indicator of the efficiency of the electrical stimulation, at a constant value (20% of Mmax) throughout the experiment. The size of the H-reflex was rapidly increased at the very beginning of the movement, and then it tended to decrease in the later phase of the movement. Consequently, even with the same level of BG EMG, the size of the H-reflex was always larger in the early rising phase of the EMG activity than in the later falling phase. The maximum size of the H-reflex was poorly correlated with the force exerted. In contrast, the size of the F-response was proportional to the force exerted. The non-linear relationship between the size of the Hreflex and the BG EMG suggests that the level of the presynaptic inhibition onto Ia terminals was modified depending on the required force level and during the course of the movement. 2002 Elsevier Science Ltd. All rights reserved. Keywords: H-reflex; Background EMG; Plantarflexion; Force; F-wave
1. Introduction It is well known that the size of Hoffmann (H-) reflex increases before and during voluntary contraction of the homonymous muscle [9,12,17,23,30,33–35,40]. Kgamihara et al. [23] showed that the time difference between the onset of the H-reflex facilitation and that of electromyographic (EMG) activity is dependent on the speed of movement. They argued that differences in the amount of the descending input to the motoneuron (MN) pool would account for the different behaviour of the premovement H-reflex facilitation. On the other hand, it was reported that the time course of the premovement H-reflex facilitation was not affected by the preparatory muscle contraction, suggesting that the premovement Hreflex facilitation is caused by removal of the presynaptic inhibition on the Ia terminal [12,34]. It is thus likely that
∗
Corresponding author. Tel./fax: +81-43-290-2621. E-mail address: [email protected] (T. Komiyama).
premovement H-reflex facilitation is caused by both the excitatory descending input and the level of the presynaptic inhibition at the Ia terminal. In contrast, it is still controversial as to whether the degree of the H-reflex facilitation during movement is closely correlated to the level of the output force or EMG [5,17,34]. This discrepancy appears, in part, to result from the methodology for recording the H-reflex [7,8,37]. The consistency of the stimulus intensity may be one of the crucial factors that must be confirmed throughout the experiment. Usually, a small M-wave which was evoked by direct firing of the motor axon, and which was elicited concomitant with the H-reflex, has been used as an indicator confirming the efficiency of the electrical stimulation for eliciting the H-reflex (reference M-wave) [35]. However, the muscle architecture would be distorted by muscle contraction itself, which could also affect the size of the H-reflex and M-wave. Indeed, the sizes of both the reference and the maximum M-wave (Mmax) were shown to be largely affected by the preceding muscle contraction under both static and dynamic experimental conditions
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[31,37,38]. Also, the effectiveness of the electrical stimulation for eliciting the H-reflex may be altered during the movement due to unavoidable movement of the tested limb. Therefore, it is of importance that the size of the reference M-wave is adjusted with respect to Mmax even when voluntary movement is performed under static conditions. In practice, to eliminate these artificial factors, the degree of the fluctuation of Mmax should be determined throughout the movement. Then, on the basis of the Mmax obtained at various movement phases, the intensity of the H-reflex stimulation should be adjusted so as to obtain the same relative size of the reference M-wave with respect to the Mmax. If a constant level of electrical stimulation could be applied, the relationship between the size of the H-reflex and the background (BG) EMG or the output force could be convincingly determined. Also, it would be possible to determine how the H-reflex was modulated phase dependently during movement. Some reflexes evoked by stimulating sensory organs are known to be modulated phase dependently [6,7,13,15,18,26,38]. Therefore, in the present study, we re-examined in greater detail the relationship between the size of the H-reflex and the level of the BG EMG activity of the homonymous muscle at different levels of contraction force. The size of the H-reflex was recalculated with respect to the Mmax that was obtained with the same timing as the H-reflex during the movement. It was hypothesized that if the H-reflex facilitation is caused solely by the excitatory descending input to the MN pool, the magnitude of the H-reflex would strongly depend on the level of the BG EMG.
2. Methods 2.1. Subjects and experimental settings The experiments were carried out on seven healthy male subjects aged 20–37 years, all of whom gave informed consent to the purpose and the procedures. The subjects sat in a reclining armchair with the knee and ankle joints at 170 and 110°, respectively. The feet were fixed to a pair of immobile metal foot plates to make the movement as isometric as possible. Subjects were asked to perform fast plantarflexion under a reaction time condition. Warning and “Go” signals were provided by an acoustic signal (1 kHz, 200 ms in duration) and a step jump (2 cm) of the continuous bright light beam on an oscilloscope, respectively. The oscilloscope was placed on the table about 70 cm in front of the subject. The time interval between the warning signal and the “Go” signal was randomly altered within the range from 1.5 to 2.5 s to avoid premature movement due to anticipation. The inter-trial interval was at least 12 s to eliminate any possible effects of previous trials. One experi-
mental session was composed of 10 trials. The subjects underwent the experimental session repeatedly from six to 10 times with a brief rest for each force level. Fiveto-ten minutes of rest was imposed before starting a different force level to reduce fatigue. 2.2. EMG recordings EMG signals were recorded from the soleus, the gastrocnemius medialis (GM) and the gastrocnemius lateralis (GL) muscles. Surface Ag/Ag–Cl electrodes (Nihon Khoden, M-10) were used to record the EMG signals (electrode spacing 3 cm). The skin impedance was reduced (below 10 K⍀) by light abrasion and cleaning with alcohol. EMG signals were amplified through a bio-amp system (Nihondenki Sanei, 1253A) with a band pass filter (band pass 30 Hz to 1 KHz, a gain ×1000, CMMR⬎60 db). The processed output was sent to a 12 bit A/D converter and then into a microcomputer running AXOTAPE (AXON Instruments Co.) data acquisition software at a sampling rate of 5 kHz. The amount of the BG EMG was calculated from the fullwave rectified and averaged (10 traces) EMG signal. The mean value for 5 ms before the electrical stimulation was taken as the BG EMG.
3. Task and stimulus procedure The subjects performed fast plantarflexion at various contraction levels. The levels of contraction force were set at 10, 20, 50 and 80% of maximum voluntary contraction (MVC). In most subjects, the order of the contraction force to be performed was set in the sequence of 10, 20, 50 and finally 80% MVC. This procedure was expected to minimize muscular fatigue effects. Some subjects performed 20% MVC at first, and then performed 10, 50 and 80% MVC. However, we did not observe any effect from this change of the order. The posterior tibial nerve was stimulated transcutaneously to elicit the H-reflex from the Sol. A rectangular pulse (1 ms duration) was used for the electrical stimulation. A constant current stimulator was used for the stimulation (Nihon Khoden, SS103J). The intensity of the test stimulus was carefully adjusted to result in an M-wave that was 20% of the maximum size in all cases. The constancy of the test stimulus was confirmed by checking the shape and peak-to-peak amplitude of the M-wave. The time interval between the onset of the EMG and the H-reflex stimulation was varied from 0 to 120 ms. Mmax was elicited with the same timing as the H-reflex by supramaximal electrical stimulation of the tibial nerve (1.5 times Mmax threshold, 1.5×Mth), and the mean amplitude of three times Mmax was used for normalizing the M-wave and the H-reflex amplitude. Mmax was accompanied by a small response, the F-
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wave, during movement. The F-wave was thought to result from the antidromic activation of the motoneurons following the electrical stimulation [14,24,25,32]. The changes in the F-wave size were also analyzed in relation to the force levels. To estimate the mechanical properties of the plantar flexion force, we analyzed the time interval from the initial EMG burst of the Sol to the initial change of the plantar flexion force (electro-mechanical delay, EMD). In addition, the time interval from the initial change of the plantar flexion force to the time at which the force reached to the peak value (time to peak force) was analyzed. When exerting 10 and 20% MVC, the subjects felt that it was difficult to exactly match the target forces due to a sudden impeding force evoked by the H-reflex stimulation. Therefore, control contractions without electrical stimulation, which served to reconfirm the required target force, were interposed in this experiment. 3.1. Statistics One-way ANOVA and Fisher’s PLSD post hoc test were performed to evaluate differences in the sizes of the M-wave, H-reflexes and F-wave obtained at different force levels. The level of statistical significance was set at p⬍0.05. Data are shown as grand means and standard error of the mean (s.e.).
4. Results The mechanical properties of the plantarflexion performed in the present study were analysed. The EMD of each force level tended to be shorter when higher force levels were exerted (F=11.89, p⬍0.01), with values of 31.0±40 ms (10% MVC), 26.1±4.2 ms (20% MVC), 21.9±4.6 ms (50% MVC) and 20.3±4.5 ms (80% MVC), respectively. In contrast, the time to peak force tended to be longer when higher force levels were exerted (10% MVC; 135.3±10.2 ms, 20% MVC; 133.9±10.8 ms, 50% MVC; 140.2±12.2 ms, 80% MVC; 161.4±31.8 ms), although the result of an one-way ANOVA showed no significant difference (F=4.93, p=0.06). Fig. 1 shows the change in the size of the Mmax (obtained from five subjects) induced by the supramaximal electrical stimulation (1.5×Mth) of the posterior tibial nerve while exerting 20% MVC. The size of the Mmax was first decreased for 40 ms after the EMG onset, and then tended to increase towards the end of the movement. One-way ANOVA showed no significant different in the pooled data. However, when looking at the individual data, a significant change in the time course of Mmax amplitude was seen in four subjects (p⬍0.01). We tried to minimize the possible effects arising from the changes in Mmax by adjusting the intensity
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of the test electrical stimulation. If this procedure was not effective, the intensity of the test stimulation would be higher during the decreasing phase of Mmax than during other phases. Mmax was determined for all time delays at which the test H-reflex was evoked, and then the intensity of the test stimulus was carefully adjusted to elicit an M-wave that was 20% of Mmax in all cases. It was also noted that the small muscle response after the supramaximal electrical stimulation was evoked depending on the movement phase. This response results from the antidromic activation of the motoneurons following the electrical stimulation, i.e., it is the F-wave. Fig. 2a and b show the timing at which the H-reflex was elicited and EMG traces obtained at the corresponding timing while performing plantarflexion (20% MVC). The size of the H-reflex was rapidly increased at the very beginning of the movement, and then it tended to be decreased in the later phase of the movement (Fig. 2c). As shown in Fig.1b and c, it is worth noting that the shape and the size of the M-wave remained constant with respect to Mmax (20% of Mmax) throughout the movement. Pooled data for seven subjects are shown in Fig. 2d. Almost the same result was seen for the pooled data, showing that the intensity of the H-reflex stimulation was kept constant throughout the movement, and that the H-reflex was modulated phase-dependently. Fig. 3 shows the size of the H-reflex analyzed in relation to the BG EMG level. As shown in Fig. 3 (left), the reference M-wave and the H-reflex were detectable even when exerting in 80% MVC. Fig. 3 (right) shows the relationship between the size of the H-reflex and the BG EMG for all target force levels. The size of the Hreflex increased steeply at the beginning of the movement, and then it tended to reach a plateau despite the increase in the BG EMG except for in the case of 80% MVC (thick lines). During the latter phase of the movement, the H-reflex gradually decreased (thin lines). The size of the H-reflex was always larger in the early rising phase of the EMG activity than in the later falling phase. As a result, hysteresis was seen in the relationship between the size of the H-reflex and the BG EMG for all target forces tested. We repeated the same experiment on different dates for six of the seven subjects, and obtained almost the same results. Thus, the H-reflex appeared to be controlled independently of the BG EMG. Fig. 4 shows the grand means (n=7) of the maximum size of the H-reflex obtained when exerting different target forces. The H-reflex was strongly facilitated even when the exerted force was only 10% of MVC, and we therefore found no significant difference in the maximum size of the H-reflex obtained with the different levels of plantarflexion force (F=1.533, p⬎0.05). In addition, no significant difference was seen in the size of the M-wave. As shown in Fig. 1, a small response could be seen
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Fig. 1. The change in the size of the Mmax after the EMG onset. The left panels show the specimen records for the Mmax obtained at different times after the Sol EMG onset. The right panel shows the grand mean (±1 s.e.) of the change in Mmax as a percentage of the Mmax that was obtained at resting situation. The abscissa shows the time interval from EMG onset (ms). It was noted that a small response (F-wave) was seen following the M-wave only during the movement.
Fig. 2. (a) Typical recordings of the full-wave rectified and averaged EMG of the Sol (upper line) and force (lower line) for the target force level corresponding to 20% MVC. (b) Recording 1: Control Sol H-reflex elicited at rest. Recordings 2–6 show the Sol H-reflexes elicited with different timings after the EMG onset during the plantarflexion. Each Arabic numeral (from 2 to 6) in panel B corresponds to the arrow with the same number in panel A. Each was made from 10 traces. (c) The time course of the change in the amplitude of the Sol H-reflex from the Sol EMG onset obtained for a single subject. Each symbol shows the mean (±1 s.e.) amplitude of the H-reflex (䊊) and M-wave (쎲) calculated from 10 samples. The ordinate shows the size of the H-reflex and M-wave as a percentage of the Mmax. The abscissa shows the time interval from the EMG onset. Panel (d) shows the grand mean (±1 s.e.) for all subjects.
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Fig. 3. The left panels show the examples of the M-wave and the H-reflex recordings for each force level. The right panel shows the relationship between the size of the H-reflex and the BG EMG during the fast movement with different force levels (䊊 with continuous line,10% MVC; 왕 with dotted line, 20% MVC; 䊐 with dotted line, 50% MVC; 䉫 with dashed line, 80% MVC) obtained from all subjects. The thick and the thin lines indicate the data obtained during the EMG rising and falling phases, respectively. The ordinate shows the size of the H-reflex as a percentage of Mmax. The abscissa shows the level of the BG EMG as a percentage of the maximum EMG level obtained in each subject. Horizontal and vertical bars show ±1 s.e. of the mean.
after the supramaximal electrical stimulation for the Mmax stimulation. This response was thought to be an F-wave, because the electrical stimulation was so high (1.5 times maximum M-wave). We analyzed the maximum size of the F-wave at each target force level. As shown in Fig. 4B, the maximum size of the F-wave was found to be significantly increased in relation to the target force (F=3.74, p⬍0.05). It is worth noting that these results were clearly different from those obtained in the H-reflex experiments described above.
5. Discussion 5.1. Methodological implications It was shown previously that the H-reflex is a linearly increasing and/or decreasing function of the BG EMG for a fixed stimulus [6–8,17,36]. The term “automatic gain compensation” has been proposed to show that the gain of the reflex increases with the excitation level of the motoneuron pool [27]. However, we found in the present study that the size of the H-reflex was controlled independently of the level of BG EMG when subjects were performing fast voluntary movement. The reasons for this discrepancy may be, at least partly, due to methodological differences. First, we used a fast movement as the motor task, but locomotor activity and steady muscle contraction were used in previous studies [5,7,8,17,34,39]. Thus, it is likely that a different supras-
pinal control acts on the H-reflex arc according to the type of voluntary movement. Second, in the previous studies, the consistency of the M-wave size with respect to the Mmax seemed not to be strictly confirmed. The present study showed that the size of the Mmax was systematically altered during the course of the movement [38]. This result may have been caused by the distortion of the muscle and/or a change in the effectiveness of the electrical stimulation. To compensate for these artificial factors, we carefully adjusted the intensity of the electrical stimulation so as to obtain a constant size of the Mwave throughout the movement. The M-wave size used in the present study, i.e., 20% of Mmax, is thought to provide sufficient sensitivity to reflect the change in the effectiveness of the electrical stimulation, because this response size is generally located at a steep rising phase in the recruitment curve [35]. The consistency of the Mwave size allows us to suggest that the changes in the H-reflex depending on the phase of the movement or target force were caused by changes in the central nervous system. 5.2. Possible mechanism for the H-reflex facilitation when exerting different force levels In the present study, the H-reflex was found to be increased to about 60% of the Mmax even when exerting only 10% MVC. This result suggests that large motoneurons with high threshold that were not activated by the Ia EPSP for eliciting the H-reflex (test Ia EPSP) at rest
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Fig. 4. Grand mean and s.e. of the maximum size of the H-reflex (A) and the F-wave (b) obtained for different force levels from all subjects. (a) Black and white bars show M-wave and H-reflex amplitude, respectively. The ordinate shows the M-wave, the H-reflex and the Fwave amplitudes as a percentage of Mmax.
were recruited by descending input during the fast movement [11]. However, we have not ruled out the possibility that the high threshold motor units were activated by the combined effect of the test Ia EPSP and the removal of the presynaptic inhibition at the Ia terminal. Therefore, the effect observed here may have resulted from recruitment of the high threshold motor units due to the combined effect of (1) the test Ia and descending EPSPs, (2) the test Ia EPSP, descending EPSPs and the removal of the presynaptic inhibition, (3) the test Ia EPSP or (4) the descending EPSP and the removal of the presynaptic inhibition. The first possibility cannot be the only mechanism underlying the effect observed here, because we found that the F-wave was proportional to the exerted force level (Fig. 4). The F-wave is thought to be evoked by discharge of an antidromic motor volley, thus suggesting that it is not influenced by presynaptic
inhibition [3,14,24,25,32]. Therefore, the changes in the F-wave amplitude may reflect the excitability of the MN pool, although the sensitivities of the H-reflex and Fwave are thought not to be equal [14]. The remaining possible mechanisms strongly suggest the importance of the presynaptic inhibition in the control of fast movement. Our finding that the H-reflex amplitude was poorly correlated with the level of exerted force strongly suggests that presynaptic inhibition is differentially controlled according to force. It has been demonstrated that the interneurons conveying presynaptic inhibition are controlled during various types of voluntary movement [20,29]. A more recent animal study strongly suggested that the tonic presynaptic inhibition mediated by the GABAB receptors at the Ia terminal would explain such task-dependent monosnyaptic reflex modulation [16]. If the presynaptic inhibition was more markedly decreased when exerting a smaller force than when exerting a larger force, the difference of the H-reflex facilitation with different force levels would tend to be small, as was observed in the present study. These lines of reasoning seem to contradict the findings of Meunier and Pierrot-Deseilligny [29]. However, the type of muscle contraction differed in their study and ours (fast vs. ramp contraction); therefore, it would be difficult to simply compare the results. It is thus likely that the size of the H-reflex may vary independently of the output force during fast movement. Lastly, a change in recruitment gain would lead to recruitment of high-threshold motor units and the appearance of a large-amplitude H-reflex [22]. However, the change in the recruitment gain would occur when stimulating cutaneous nerves or stimulating the red nucleus. Hence, this mechanism seems unlikely to explain our results. 5.3. Non-linearity between the H-reflex and the BG EMG Presynaptic inhibition at the Ia terminal, descending inputs to the MN, and fusimotor feedback should be taken into consideration in order to explain the non-linear relationship between the H-reflex and the BG EMG. It was shown in the present study that the size of the Hreflex increased at the very beginning of the movement, suggesting that the Ia afferent feedback from the spindle discharges is not a major reason for the H-reflex facilitation at this phase, because it takes more than 10 ms for an excitatory input to reach the MN pool via the fusimotor system [41]. Thus, descending input to the MN pool and the removal of the presynaptic inhibition onto the Ia terminal would play important roles in the H-reflex facilitation at the beginning of the movement. We observed that the maximum H-reflex occurred from 30 to 60 ms after the EMG onset. At this stage, the fast descending excitatory input, Ia inputs via the fusimotor
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system and the removal of the presynaptic inhibition at the Ia terminal could be involved in the H-reflex facilitation. Phasic changes in these three factors may be the cause of the hysteresis. As for the latter phase of the movement, both a decrease in the excitatory input to the MN and an increase in the presynaptic inhibition may play major roles in the attenuation of the reflex gain. In humans it was shown that presynaptic inhibition was increased during voluntary relaxing of muscles [36] and during the stretching phase of the homonymous muscle [2,19,21]. Also, post-activation depression is likely to be more effective for the H-reflex depression, because repetitive firing of the Ia afferent due to fusimotor drive could result in desensitization of the Ia terminal to the test Ia volley [10]. These features of the phase-dependent changes of the presyaptic inhibition were also supported by recent animal studies suggesting a phasic change of the presynaptic inhibition at the Ia terminal , possibly mediated by the GABAA receptor [16,28]. In conclusion, we found that the H-reflex was not a linearly increasing function of the BG EMG during fast movement. In addition, the size of the H-reflex was poorly correlated with the exerted force level. These results further support the idea that is fundamentally important in the control of the H-reflex during fast movement, as was suggested in previous studies done under different modalities of voluntary movements [1,2,4,7,8,20,29].
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[36] Schieppati M, Nardone A, Musazzi M. Modulation of the Hoffmann reflex by rapid muscle contraction or release. Human Neurobiol 1986;5:59–66. [37] Simonsen EB, Dyhre-Poulsen P, Voigt M. Excitability of the soleus H reflex during graded walking in humans. Acta Physiol Scand 1995;153:21–32. [38] Simonsen EB, Dyhrepoulsen P. Amplitude of the human soleus H reflex during walking and running. J Physiol 1999;515:929–39. [39] Stein RB, Kearney RE. Nonlinear behavior of muscle reflexes at the human ankle joint. J Neurophysiol 1995;73:65–72. [40] Sulvian SJ. Conditioned H-reflex prior to movement. Brain Res 1980;192:564–9. ˚ B. Muscle spindle response at the onset of isometric [41] Vallbo A voluntary contractions in man: time difference between fusimotor and skeletomotor effects. J Physiol 1971;318:405–31. Masaki Fumoto received his M.S. in Physical Education from Chiba University in 1996 and his Ph.D. degree in Exercise and Sports Science from Tsukuba University in 2001. He is currently and instructor in the Department of Physiology, Toho University School of Medicine (from 2001).
Tomoyoshi Komiyama received his Ph.D. degree in Exercise and Sports Sciences with a Human Neurophysiology concentration in 1989 from the University of Tsukuba. He is currently Associate Professor of the Health and Sports Sciences, Chiba University. His current research focus is on the neural control of human voluntary movements.
Yoshiaki Nishihira received his M.S. in Health and Physical Education from Tokyo University of Education (1976) and his Ph.D. degree in Health and Sports Sciences from Tsukuba University (1980). He is currently Professor of Physiology in the Department of Health and Sports Sciences, Tsukuba University.
Soleus H-reflex dynamics during fast plantarflexion in humans Masaki Fumoto a, Tomoyoshi Komiyama b,∗, Yoshiaki Nishihira c b
a Department of Physiology, Toho University School of Medicine, Tokyo, Japan Department of Health and Sport Sciences, Faculty of Education, Chiba University, 1-33 Yayoicho, Inage-ku, Chiba City 263-8522, Japan c Institute of Health and Sports Sciences, University of Tsukuba, Japan
Received 22 March 2001; received in revised form 30 January 2002; accepted 23 February 2002
Abstract The relationship between the size of the soleus (Sol) Hoffmann (H-) reflex and the level of background (BG) electromyographic (EMG) activity was examined during plantarflexing at different force levels. The experiments were carried out on seven healthy male subjects aged 20–37 years. The subjects were asked to perform fast plantarflexion under a reaction-time condition. The amounts of contraction force were 10, 20, 50 and 80% of maximum voluntary contraction (MVC). Since the maximum size of the M-wave (Mmax) changed systematically during the plantarflexion, we tried to maintain the size of the reference M-wave, an indicator of the efficiency of the electrical stimulation, at a constant value (20% of Mmax) throughout the experiment. The size of the H-reflex was rapidly increased at the very beginning of the movement, and then it tended to decrease in the later phase of the movement. Consequently, even with the same level of BG EMG, the size of the H-reflex was always larger in the early rising phase of the EMG activity than in the later falling phase. The maximum size of the H-reflex was poorly correlated with the force exerted. In contrast, the size of the F-response was proportional to the force exerted. The non-linear relationship between the size of the Hreflex and the BG EMG suggests that the level of the presynaptic inhibition onto Ia terminals was modified depending on the required force level and during the course of the movement. 2002 Elsevier Science Ltd. All rights reserved. Keywords: H-reflex; Background EMG; Plantarflexion; Force; F-wave
1. Introduction It is well known that the size of Hoffmann (H-) reflex increases before and during voluntary contraction of the homonymous muscle [9,12,17,23,30,33–35,40]. Kgamihara et al. [23] showed that the time difference between the onset of the H-reflex facilitation and that of electromyographic (EMG) activity is dependent on the speed of movement. They argued that differences in the amount of the descending input to the motoneuron (MN) pool would account for the different behaviour of the premovement H-reflex facilitation. On the other hand, it was reported that the time course of the premovement H-reflex facilitation was not affected by the preparatory muscle contraction, suggesting that the premovement Hreflex facilitation is caused by removal of the presynaptic inhibition on the Ia terminal [12,34]. It is thus likely that
∗
Corresponding author. Tel./fax: +81-43-290-2621. E-mail address: [email protected] (T. Komiyama).
premovement H-reflex facilitation is caused by both the excitatory descending input and the level of the presynaptic inhibition at the Ia terminal. In contrast, it is still controversial as to whether the degree of the H-reflex facilitation during movement is closely correlated to the level of the output force or EMG [5,17,34]. This discrepancy appears, in part, to result from the methodology for recording the H-reflex [7,8,37]. The consistency of the stimulus intensity may be one of the crucial factors that must be confirmed throughout the experiment. Usually, a small M-wave which was evoked by direct firing of the motor axon, and which was elicited concomitant with the H-reflex, has been used as an indicator confirming the efficiency of the electrical stimulation for eliciting the H-reflex (reference M-wave) [35]. However, the muscle architecture would be distorted by muscle contraction itself, which could also affect the size of the H-reflex and M-wave. Indeed, the sizes of both the reference and the maximum M-wave (Mmax) were shown to be largely affected by the preceding muscle contraction under both static and dynamic experimental conditions
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[31,37,38]. Also, the effectiveness of the electrical stimulation for eliciting the H-reflex may be altered during the movement due to unavoidable movement of the tested limb. Therefore, it is of importance that the size of the reference M-wave is adjusted with respect to Mmax even when voluntary movement is performed under static conditions. In practice, to eliminate these artificial factors, the degree of the fluctuation of Mmax should be determined throughout the movement. Then, on the basis of the Mmax obtained at various movement phases, the intensity of the H-reflex stimulation should be adjusted so as to obtain the same relative size of the reference M-wave with respect to the Mmax. If a constant level of electrical stimulation could be applied, the relationship between the size of the H-reflex and the background (BG) EMG or the output force could be convincingly determined. Also, it would be possible to determine how the H-reflex was modulated phase dependently during movement. Some reflexes evoked by stimulating sensory organs are known to be modulated phase dependently [6,7,13,15,18,26,38]. Therefore, in the present study, we re-examined in greater detail the relationship between the size of the H-reflex and the level of the BG EMG activity of the homonymous muscle at different levels of contraction force. The size of the H-reflex was recalculated with respect to the Mmax that was obtained with the same timing as the H-reflex during the movement. It was hypothesized that if the H-reflex facilitation is caused solely by the excitatory descending input to the MN pool, the magnitude of the H-reflex would strongly depend on the level of the BG EMG.
2. Methods 2.1. Subjects and experimental settings The experiments were carried out on seven healthy male subjects aged 20–37 years, all of whom gave informed consent to the purpose and the procedures. The subjects sat in a reclining armchair with the knee and ankle joints at 170 and 110°, respectively. The feet were fixed to a pair of immobile metal foot plates to make the movement as isometric as possible. Subjects were asked to perform fast plantarflexion under a reaction time condition. Warning and “Go” signals were provided by an acoustic signal (1 kHz, 200 ms in duration) and a step jump (2 cm) of the continuous bright light beam on an oscilloscope, respectively. The oscilloscope was placed on the table about 70 cm in front of the subject. The time interval between the warning signal and the “Go” signal was randomly altered within the range from 1.5 to 2.5 s to avoid premature movement due to anticipation. The inter-trial interval was at least 12 s to eliminate any possible effects of previous trials. One experi-
mental session was composed of 10 trials. The subjects underwent the experimental session repeatedly from six to 10 times with a brief rest for each force level. Fiveto-ten minutes of rest was imposed before starting a different force level to reduce fatigue. 2.2. EMG recordings EMG signals were recorded from the soleus, the gastrocnemius medialis (GM) and the gastrocnemius lateralis (GL) muscles. Surface Ag/Ag–Cl electrodes (Nihon Khoden, M-10) were used to record the EMG signals (electrode spacing 3 cm). The skin impedance was reduced (below 10 K⍀) by light abrasion and cleaning with alcohol. EMG signals were amplified through a bio-amp system (Nihondenki Sanei, 1253A) with a band pass filter (band pass 30 Hz to 1 KHz, a gain ×1000, CMMR⬎60 db). The processed output was sent to a 12 bit A/D converter and then into a microcomputer running AXOTAPE (AXON Instruments Co.) data acquisition software at a sampling rate of 5 kHz. The amount of the BG EMG was calculated from the fullwave rectified and averaged (10 traces) EMG signal. The mean value for 5 ms before the electrical stimulation was taken as the BG EMG.
3. Task and stimulus procedure The subjects performed fast plantarflexion at various contraction levels. The levels of contraction force were set at 10, 20, 50 and 80% of maximum voluntary contraction (MVC). In most subjects, the order of the contraction force to be performed was set in the sequence of 10, 20, 50 and finally 80% MVC. This procedure was expected to minimize muscular fatigue effects. Some subjects performed 20% MVC at first, and then performed 10, 50 and 80% MVC. However, we did not observe any effect from this change of the order. The posterior tibial nerve was stimulated transcutaneously to elicit the H-reflex from the Sol. A rectangular pulse (1 ms duration) was used for the electrical stimulation. A constant current stimulator was used for the stimulation (Nihon Khoden, SS103J). The intensity of the test stimulus was carefully adjusted to result in an M-wave that was 20% of the maximum size in all cases. The constancy of the test stimulus was confirmed by checking the shape and peak-to-peak amplitude of the M-wave. The time interval between the onset of the EMG and the H-reflex stimulation was varied from 0 to 120 ms. Mmax was elicited with the same timing as the H-reflex by supramaximal electrical stimulation of the tibial nerve (1.5 times Mmax threshold, 1.5×Mth), and the mean amplitude of three times Mmax was used for normalizing the M-wave and the H-reflex amplitude. Mmax was accompanied by a small response, the F-
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wave, during movement. The F-wave was thought to result from the antidromic activation of the motoneurons following the electrical stimulation [14,24,25,32]. The changes in the F-wave size were also analyzed in relation to the force levels. To estimate the mechanical properties of the plantar flexion force, we analyzed the time interval from the initial EMG burst of the Sol to the initial change of the plantar flexion force (electro-mechanical delay, EMD). In addition, the time interval from the initial change of the plantar flexion force to the time at which the force reached to the peak value (time to peak force) was analyzed. When exerting 10 and 20% MVC, the subjects felt that it was difficult to exactly match the target forces due to a sudden impeding force evoked by the H-reflex stimulation. Therefore, control contractions without electrical stimulation, which served to reconfirm the required target force, were interposed in this experiment. 3.1. Statistics One-way ANOVA and Fisher’s PLSD post hoc test were performed to evaluate differences in the sizes of the M-wave, H-reflexes and F-wave obtained at different force levels. The level of statistical significance was set at p⬍0.05. Data are shown as grand means and standard error of the mean (s.e.).
4. Results The mechanical properties of the plantarflexion performed in the present study were analysed. The EMD of each force level tended to be shorter when higher force levels were exerted (F=11.89, p⬍0.01), with values of 31.0±40 ms (10% MVC), 26.1±4.2 ms (20% MVC), 21.9±4.6 ms (50% MVC) and 20.3±4.5 ms (80% MVC), respectively. In contrast, the time to peak force tended to be longer when higher force levels were exerted (10% MVC; 135.3±10.2 ms, 20% MVC; 133.9±10.8 ms, 50% MVC; 140.2±12.2 ms, 80% MVC; 161.4±31.8 ms), although the result of an one-way ANOVA showed no significant difference (F=4.93, p=0.06). Fig. 1 shows the change in the size of the Mmax (obtained from five subjects) induced by the supramaximal electrical stimulation (1.5×Mth) of the posterior tibial nerve while exerting 20% MVC. The size of the Mmax was first decreased for 40 ms after the EMG onset, and then tended to increase towards the end of the movement. One-way ANOVA showed no significant different in the pooled data. However, when looking at the individual data, a significant change in the time course of Mmax amplitude was seen in four subjects (p⬍0.01). We tried to minimize the possible effects arising from the changes in Mmax by adjusting the intensity
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of the test electrical stimulation. If this procedure was not effective, the intensity of the test stimulation would be higher during the decreasing phase of Mmax than during other phases. Mmax was determined for all time delays at which the test H-reflex was evoked, and then the intensity of the test stimulus was carefully adjusted to elicit an M-wave that was 20% of Mmax in all cases. It was also noted that the small muscle response after the supramaximal electrical stimulation was evoked depending on the movement phase. This response results from the antidromic activation of the motoneurons following the electrical stimulation, i.e., it is the F-wave. Fig. 2a and b show the timing at which the H-reflex was elicited and EMG traces obtained at the corresponding timing while performing plantarflexion (20% MVC). The size of the H-reflex was rapidly increased at the very beginning of the movement, and then it tended to be decreased in the later phase of the movement (Fig. 2c). As shown in Fig.1b and c, it is worth noting that the shape and the size of the M-wave remained constant with respect to Mmax (20% of Mmax) throughout the movement. Pooled data for seven subjects are shown in Fig. 2d. Almost the same result was seen for the pooled data, showing that the intensity of the H-reflex stimulation was kept constant throughout the movement, and that the H-reflex was modulated phase-dependently. Fig. 3 shows the size of the H-reflex analyzed in relation to the BG EMG level. As shown in Fig. 3 (left), the reference M-wave and the H-reflex were detectable even when exerting in 80% MVC. Fig. 3 (right) shows the relationship between the size of the H-reflex and the BG EMG for all target force levels. The size of the Hreflex increased steeply at the beginning of the movement, and then it tended to reach a plateau despite the increase in the BG EMG except for in the case of 80% MVC (thick lines). During the latter phase of the movement, the H-reflex gradually decreased (thin lines). The size of the H-reflex was always larger in the early rising phase of the EMG activity than in the later falling phase. As a result, hysteresis was seen in the relationship between the size of the H-reflex and the BG EMG for all target forces tested. We repeated the same experiment on different dates for six of the seven subjects, and obtained almost the same results. Thus, the H-reflex appeared to be controlled independently of the BG EMG. Fig. 4 shows the grand means (n=7) of the maximum size of the H-reflex obtained when exerting different target forces. The H-reflex was strongly facilitated even when the exerted force was only 10% of MVC, and we therefore found no significant difference in the maximum size of the H-reflex obtained with the different levels of plantarflexion force (F=1.533, p⬎0.05). In addition, no significant difference was seen in the size of the M-wave. As shown in Fig. 1, a small response could be seen
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Fig. 1. The change in the size of the Mmax after the EMG onset. The left panels show the specimen records for the Mmax obtained at different times after the Sol EMG onset. The right panel shows the grand mean (±1 s.e.) of the change in Mmax as a percentage of the Mmax that was obtained at resting situation. The abscissa shows the time interval from EMG onset (ms). It was noted that a small response (F-wave) was seen following the M-wave only during the movement.
Fig. 2. (a) Typical recordings of the full-wave rectified and averaged EMG of the Sol (upper line) and force (lower line) for the target force level corresponding to 20% MVC. (b) Recording 1: Control Sol H-reflex elicited at rest. Recordings 2–6 show the Sol H-reflexes elicited with different timings after the EMG onset during the plantarflexion. Each Arabic numeral (from 2 to 6) in panel B corresponds to the arrow with the same number in panel A. Each was made from 10 traces. (c) The time course of the change in the amplitude of the Sol H-reflex from the Sol EMG onset obtained for a single subject. Each symbol shows the mean (±1 s.e.) amplitude of the H-reflex (䊊) and M-wave (쎲) calculated from 10 samples. The ordinate shows the size of the H-reflex and M-wave as a percentage of the Mmax. The abscissa shows the time interval from the EMG onset. Panel (d) shows the grand mean (±1 s.e.) for all subjects.
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Fig. 3. The left panels show the examples of the M-wave and the H-reflex recordings for each force level. The right panel shows the relationship between the size of the H-reflex and the BG EMG during the fast movement with different force levels (䊊 with continuous line,10% MVC; 왕 with dotted line, 20% MVC; 䊐 with dotted line, 50% MVC; 䉫 with dashed line, 80% MVC) obtained from all subjects. The thick and the thin lines indicate the data obtained during the EMG rising and falling phases, respectively. The ordinate shows the size of the H-reflex as a percentage of Mmax. The abscissa shows the level of the BG EMG as a percentage of the maximum EMG level obtained in each subject. Horizontal and vertical bars show ±1 s.e. of the mean.
after the supramaximal electrical stimulation for the Mmax stimulation. This response was thought to be an F-wave, because the electrical stimulation was so high (1.5 times maximum M-wave). We analyzed the maximum size of the F-wave at each target force level. As shown in Fig. 4B, the maximum size of the F-wave was found to be significantly increased in relation to the target force (F=3.74, p⬍0.05). It is worth noting that these results were clearly different from those obtained in the H-reflex experiments described above.
5. Discussion 5.1. Methodological implications It was shown previously that the H-reflex is a linearly increasing and/or decreasing function of the BG EMG for a fixed stimulus [6–8,17,36]. The term “automatic gain compensation” has been proposed to show that the gain of the reflex increases with the excitation level of the motoneuron pool [27]. However, we found in the present study that the size of the H-reflex was controlled independently of the level of BG EMG when subjects were performing fast voluntary movement. The reasons for this discrepancy may be, at least partly, due to methodological differences. First, we used a fast movement as the motor task, but locomotor activity and steady muscle contraction were used in previous studies [5,7,8,17,34,39]. Thus, it is likely that a different supras-
pinal control acts on the H-reflex arc according to the type of voluntary movement. Second, in the previous studies, the consistency of the M-wave size with respect to the Mmax seemed not to be strictly confirmed. The present study showed that the size of the Mmax was systematically altered during the course of the movement [38]. This result may have been caused by the distortion of the muscle and/or a change in the effectiveness of the electrical stimulation. To compensate for these artificial factors, we carefully adjusted the intensity of the electrical stimulation so as to obtain a constant size of the Mwave throughout the movement. The M-wave size used in the present study, i.e., 20% of Mmax, is thought to provide sufficient sensitivity to reflect the change in the effectiveness of the electrical stimulation, because this response size is generally located at a steep rising phase in the recruitment curve [35]. The consistency of the Mwave size allows us to suggest that the changes in the H-reflex depending on the phase of the movement or target force were caused by changes in the central nervous system. 5.2. Possible mechanism for the H-reflex facilitation when exerting different force levels In the present study, the H-reflex was found to be increased to about 60% of the Mmax even when exerting only 10% MVC. This result suggests that large motoneurons with high threshold that were not activated by the Ia EPSP for eliciting the H-reflex (test Ia EPSP) at rest
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Fig. 4. Grand mean and s.e. of the maximum size of the H-reflex (A) and the F-wave (b) obtained for different force levels from all subjects. (a) Black and white bars show M-wave and H-reflex amplitude, respectively. The ordinate shows the M-wave, the H-reflex and the Fwave amplitudes as a percentage of Mmax.
were recruited by descending input during the fast movement [11]. However, we have not ruled out the possibility that the high threshold motor units were activated by the combined effect of the test Ia EPSP and the removal of the presynaptic inhibition at the Ia terminal. Therefore, the effect observed here may have resulted from recruitment of the high threshold motor units due to the combined effect of (1) the test Ia and descending EPSPs, (2) the test Ia EPSP, descending EPSPs and the removal of the presynaptic inhibition, (3) the test Ia EPSP or (4) the descending EPSP and the removal of the presynaptic inhibition. The first possibility cannot be the only mechanism underlying the effect observed here, because we found that the F-wave was proportional to the exerted force level (Fig. 4). The F-wave is thought to be evoked by discharge of an antidromic motor volley, thus suggesting that it is not influenced by presynaptic
inhibition [3,14,24,25,32]. Therefore, the changes in the F-wave amplitude may reflect the excitability of the MN pool, although the sensitivities of the H-reflex and Fwave are thought not to be equal [14]. The remaining possible mechanisms strongly suggest the importance of the presynaptic inhibition in the control of fast movement. Our finding that the H-reflex amplitude was poorly correlated with the level of exerted force strongly suggests that presynaptic inhibition is differentially controlled according to force. It has been demonstrated that the interneurons conveying presynaptic inhibition are controlled during various types of voluntary movement [20,29]. A more recent animal study strongly suggested that the tonic presynaptic inhibition mediated by the GABAB receptors at the Ia terminal would explain such task-dependent monosnyaptic reflex modulation [16]. If the presynaptic inhibition was more markedly decreased when exerting a smaller force than when exerting a larger force, the difference of the H-reflex facilitation with different force levels would tend to be small, as was observed in the present study. These lines of reasoning seem to contradict the findings of Meunier and Pierrot-Deseilligny [29]. However, the type of muscle contraction differed in their study and ours (fast vs. ramp contraction); therefore, it would be difficult to simply compare the results. It is thus likely that the size of the H-reflex may vary independently of the output force during fast movement. Lastly, a change in recruitment gain would lead to recruitment of high-threshold motor units and the appearance of a large-amplitude H-reflex [22]. However, the change in the recruitment gain would occur when stimulating cutaneous nerves or stimulating the red nucleus. Hence, this mechanism seems unlikely to explain our results. 5.3. Non-linearity between the H-reflex and the BG EMG Presynaptic inhibition at the Ia terminal, descending inputs to the MN, and fusimotor feedback should be taken into consideration in order to explain the non-linear relationship between the H-reflex and the BG EMG. It was shown in the present study that the size of the Hreflex increased at the very beginning of the movement, suggesting that the Ia afferent feedback from the spindle discharges is not a major reason for the H-reflex facilitation at this phase, because it takes more than 10 ms for an excitatory input to reach the MN pool via the fusimotor system [41]. Thus, descending input to the MN pool and the removal of the presynaptic inhibition onto the Ia terminal would play important roles in the H-reflex facilitation at the beginning of the movement. We observed that the maximum H-reflex occurred from 30 to 60 ms after the EMG onset. At this stage, the fast descending excitatory input, Ia inputs via the fusimotor
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system and the removal of the presynaptic inhibition at the Ia terminal could be involved in the H-reflex facilitation. Phasic changes in these three factors may be the cause of the hysteresis. As for the latter phase of the movement, both a decrease in the excitatory input to the MN and an increase in the presynaptic inhibition may play major roles in the attenuation of the reflex gain. In humans it was shown that presynaptic inhibition was increased during voluntary relaxing of muscles [36] and during the stretching phase of the homonymous muscle [2,19,21]. Also, post-activation depression is likely to be more effective for the H-reflex depression, because repetitive firing of the Ia afferent due to fusimotor drive could result in desensitization of the Ia terminal to the test Ia volley [10]. These features of the phase-dependent changes of the presyaptic inhibition were also supported by recent animal studies suggesting a phasic change of the presynaptic inhibition at the Ia terminal , possibly mediated by the GABAA receptor [16,28]. In conclusion, we found that the H-reflex was not a linearly increasing function of the BG EMG during fast movement. In addition, the size of the H-reflex was poorly correlated with the exerted force level. These results further support the idea that is fundamentally important in the control of the H-reflex during fast movement, as was suggested in previous studies done under different modalities of voluntary movements [1,2,4,7,8,20,29].
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[36] Schieppati M, Nardone A, Musazzi M. Modulation of the Hoffmann reflex by rapid muscle contraction or release. Human Neurobiol 1986;5:59–66. [37] Simonsen EB, Dyhre-Poulsen P, Voigt M. Excitability of the soleus H reflex during graded walking in humans. Acta Physiol Scand 1995;153:21–32. [38] Simonsen EB, Dyhrepoulsen P. Amplitude of the human soleus H reflex during walking and running. J Physiol 1999;515:929–39. [39] Stein RB, Kearney RE. Nonlinear behavior of muscle reflexes at the human ankle joint. J Neurophysiol 1995;73:65–72. [40] Sulvian SJ. Conditioned H-reflex prior to movement. Brain Res 1980;192:564–9. ˚ B. Muscle spindle response at the onset of isometric [41] Vallbo A voluntary contractions in man: time difference between fusimotor and skeletomotor effects. J Physiol 1971;318:405–31. Masaki Fumoto received his M.S. in Physical Education from Chiba University in 1996 and his Ph.D. degree in Exercise and Sports Science from Tsukuba University in 2001. He is currently and instructor in the Department of Physiology, Toho University School of Medicine (from 2001).
Tomoyoshi Komiyama received his Ph.D. degree in Exercise and Sports Sciences with a Human Neurophysiology concentration in 1989 from the University of Tsukuba. He is currently Associate Professor of the Health and Sports Sciences, Chiba University. His current research focus is on the neural control of human voluntary movements.
Yoshiaki Nishihira received his M.S. in Health and Physical Education from Tokyo University of Education (1976) and his Ph.D. degree in Health and Sports Sciences from Tsukuba University (1980). He is currently Professor of Physiology in the Department of Health and Sports Sciences, Tsukuba University.