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1 Departments of Motor Dysfunction, Research Institute of National Rehabilitation Center for the Disabled, 4–1 Namiki, Tokorozawa 359-8555, Japan; 2 Sensory and Communication Disorders, Research Institute of National Rehabilitation Center for the Disabled, 4–1 Namiki, Tokorozawa 359-8555, Japan
Submitted 3 March 2003; accepted in final form 27 May 2003
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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); namely, it cannot fire without neuronal inputs. However, recent studies using reduced animal preparations have challenged this notion (Bennett et al. 1998; Crone et al. 1988; Hounsgaard et al. 1984, 1988; Schwindt and Crill 1980a,b). Transient current injection or excitatory synaptic inputs can trigger sustained motoneuron activity that outlasts input cessation. Most importantly, it comes from intrinsic properties that generate sustained depolarization of the motoneuron (plateau potential) (Hultborn 1999).
However, the emergence of plateau potentials in awake animals or humans is difficult to demonstrate because the membrane voltage of the motoneuron cannot be recorded intracellularly. Nevertheless, indirect evidence that plateau potentials contribute to motoneuron firing has been provided by investigations of the motor-unit firing pattern in animals that were awake (Bennett et al. 2001; Eken 1998; Gorrassini et al. 1999) and in humans (Gorassini et al. 1998, 2002; Kiehn and Eken 1997). A paired motor-unit method adopted in these studies, where the firing frequency of the lower threshold motor unit is used as a measure of common synaptic inputs, has ingeniously shown that motoneuron firing could be partly maintained by intrinsically mediated depolarization.
If the plateau potential actually contributes to motoneuron firing, as implied in previous studies, self-sustained motoneuron activity can also be observed in humans. Preliminary evidence can be found in the work of Lang and Vallbo (1967). They described low intensity stimulation of the tibial nerve that occasionally induced sustained muscle activity, although they did not emphasize this point. Other evidence was obtained from patients who suffered from cramping (Baldissera et al. 1994). These authors revealed that electrical stimulation of Ia afferents could trigger sustained muscle contractions; furthermore, they ascribed this mechanism to the plateau potentials of human spinal motoneurons. More recently, it has been shown that direct electrical stimulation of the muscle belly in normal human subjects can induce sustained, involuntary muscle contractions that outlast the stimulus period (Collins et al. 2001). However, several counter arguments should be answered to reach the conclusion that these muscle contractions come from an intrinsic mechanism of the motoneurons or interneurons. For example, although Collins et al. (2001) described that the sustained muscle contractions could be induced even for sleeping subjects, it was not evaluated to what extent this muscle contraction was involuntary. Also, it remains unclear to what extent these contractions were maintained by reverberating activity within closed neuronal circuits.
The percutaneous application of an electrical pulse to the tibial nerve is well known to reflexively activate human triceps surae muscles (H-reflex) (Schieppati 1987). In the present study, first, we demonstrate that train stimulation, instead of single-pulse stimulation, induces sustained muscle contractions that outlast the stimulation period, as reported in previous human (Collins et al. 2001, 2002) and animal experiments (Crone et al. 1988). We then provide evidence that this muscle contraction comes from autonomous neuronal activity within the spinal cord (possibly plateau potentials in motoneurons and/or interneurons). Specifically, we have focused mainly on the degree of "autonomy" of muscle contractions with various types of electrical stimulation and transcranial magnetic stimulation of the primary motor cortex.
Parts of the present study have been presented in abstract form (Nozaki et al. 2002).
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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In total, 11 male subjects (22–39 yr old) participated in this study. The subjects provided informed consent. This study was performed according to the Declaration of Helsinki and was approved by the ethics committee of our research institute. Participants were placed on a bed on their left side with the inside of their right leg also placed on the bed. Their hip and knee joints were flexed approximately 60°. The right foot was not fixed because foot fixation with an ankle brace or footplate allowed subjects to be aware of muscle contractions through sensation of the reaction force from the sole of the foot. The surface electromyography (EMG) signal was recorded from the right soleus (Sol), the medial (MG) and lateral (LG) heads of the gastrocnemius; and the tibialis anterior (TA) with use of a bipolar electrode. The EMG signal was amplified (Amplifier; Nihon-Kohden, AB-651-J) with band-pass filtering between 15 Hz and 3 kHz and digitized at 5 kHz. The tibial nerve was percutaneously stimulated by applying rectangular electrical pulses of 1 ms duration to the popliteal fossa (Fig. 1) with a constant voltage stimulator (DPS-1300D, Dia Medical System). Typically, 50 Hz train stimulation for 2 s of 1.2 x H-reflex threshold (this was below the direct motor response threshold) was used to elicit sustained muscle contractions in the triceps surae muscles (Fig. 1). This stimulus intensity did not evoke any apparent ankle joint movement (i.e., the induced muscle contraction was isometric) because the friction between the inside of the foot and bed surface was sufficient to prevent movement. The subjects were instructed to ignore the electrical stimulation as far as possible and to remain relaxed. In addition, the same experiment was conducted for two subjects after placement of a topical anesthetic on the skin surrounding the stimulation electrode by subcutaneous injection of 3 ml lidocaine (10 mg/ml). We then determined whether cutaneous sensation was responsible for involuntary sustained muscle contractions. In the following parts of this paper, we tentatively refer to this muscle contraction as "the self-sustained muscle contraction," even though this has not been clarified at this stage. At the end of experiment, the subjects conducted isometric maximal voluntary plantarflexion and dorsiflexion in the same posture described above and the EMG signals were recorded.
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Conditioning electrical stimulation
Six subjects participated in experiments 1 and 2. In experiment 1, the common peroneal nerve (CPN) was stimulated during the self-sustained muscle contraction by using a bipolar surface electrode at the level of the caput fibulae (Fig. 1, arrow 1) (Tanaka 1983). The stimulus intensity was set to 1.05, 1.2, and 1.5 x motor threshold (MT) of TA. Similarly, in experiment 2, the tibial nerve was stimulated to elicit an H-reflex in the Sol by applying an electrical pulse via the same electrodes as those used to induce the self-sustained muscle contraction (Fig. 1, arrow 2). The stimulus intensity was set to 1.0 x motor threshold of the Sol. In both cases, the interstimulus interval was 6 s. Ten responses were elicited in one trial.
Transcranial magnetic stimulation
In experiment 3, the primary motor cortex (M1) for the ankle joint muscles of the right leg was stimulated using Magstim 200 (The Magstim Company, UK) for 10 subjects (Fig. 1, arrow 3). A double cone coil was placed over and around the vertex with its long axis parallel to the frontal plane. The coil was firmly fixed to the subject's head using a custom-built helmet. During the experiment, subjects were asked to close their eyes. The stimulus intensity was set to the threshold level of the Sol in the resting condition (from 55 to 90% of maximal stimulator output). The interstimulus interval was random (
7 s apart) and a total of five responses were evoked in one trial. First, the motor evoked potential (MEP) was evoked during the self-sustained muscle contraction while background muscle activity (BGA) of the Sol was continuously monitored on a realtime basis. The BGA was calculated from the root mean square value (RMS) of the EMG during the 100 ms just before the onset of stimulation. After that, the MEP was evoked during voluntary plantarflexion, where the subjects were requested to adjust the Sol BGA level to the last sustained muscle contraction. This cycle was repeated six times per subject. The magnitude of the MEP was evaluated by the area of the EMG response.
To investigate the excitability of the Sol motoneuron pool, the Sol H-reflex was evoked using the same method from experiment 2. The experimental procedure was the same as the TMS experiment described above. The stimulus intensity was adjusted to evoke a constant motor response (M-response) in the Sol (7 ± 2% of maximal M-response). The magnitude of the Sol H-reflex and M-response was evaluated by the peak-to-peak amplitude of the EMG response.
Additional experiments
Experiment 3 was designed to clarify the extent of motor cortex association with the sustained muscle contraction by comparing the MEP and the H-reflex between both muscle contraction modes. However, two problems remained with this strategy. First, since the H-reflex was much larger than the MEP (see Fig. 4A and C), it is possible that the large H-reflex does not have sufficient sensitivity to detect the difference in contraction modes (Crone et al. 1990). Second, since the MEP contains considerable polysynaptic components, it would reflect not only the motor cortex excitability but also the interneuron excitability (Nielsen et al. 1999). We conducted the following two additional experiments to overcome these problems.
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The first additional experiment consisted of matching the size of the H-reflex with the MEP by using a very weak stimulus intensity for six subjects. The experimental procedure was the same as the main H-reflex experiment; however, the H-reflex size was quantified by the area of EMG response, as done in the TMS experiment. In this case, we were unable to monitor the M-response to guarantee the constancy of the stimulus intensity, so we readjusted the stimulus intensity every cycle (unless the stimulus intensity was adjusted, the drift was sometimes observed in H-reflex magnitude because of the change of impedance between the skin and electrode). We compared the size of the H-reflex size between voluntary and self-sustained muscle contractions every cycle.
In the second additional experiment, we compared the amount of the earliest H-reflex facilitation conditioned by the TMS (Nielsen et al. 1993) between self-sustained and voluntary muscle contractions. This method is suitable for examining the excitability of the motor cortex because the earliest H-reflex facilitation is probably caused by activation of direct monosynaptic projections from the motor cortex to spinal motoneurons (Nielsen and Petersen 1995). Five subjects participated in this experiment. First, the test H-reflexes were conditioned by TMS applied at various conditioning-test intervals from –10 to 3 ms with 1 ms resolution (negative value indicates that the TMS was applied after tibial nerve stimulation) while the subjects conducted voluntary plantarflexion. The amplitude of unconditioned H-reflex was set to approximately 15% of maximal M-response throughout this experiment. The earliest conditioning-test time interval to facilitate the H-reflex was obtained for each subject. The H-reflex for each muscle contraction mode then was conditioned by the TMS applied at this interval or at 1 ms earlier than this interval (in the latter case, the size of the H-reflex was almost equivalent to that of the unconditioned H-reflex). These two intervals were alternated randomly and 20 H-reflexes were obtained for each muscle contraction mode and each time interval. The amount of H-reflex facilitation was calculated for each muscle contraction mode by taking the ratio of H-reflexes induced at these two interstimulus intervals. The same ratio was calculated for the Sol BGA to examine whether the H-reflex facilitation was due to the larger Sol BGA.
The repeated measures ANOVA with replication was used to compare the size of MEP, H-reflex, M-response, and BGA between the two muscle contraction modes. In the second additional experiment, a Student's t-test was used for each subject to test whether the H-reflex facilitation was significant. The probability P < 0.05 was accepted as a significant level.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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In previous studies using direct electrical stimulation to the muscle belly (Collins et al. 2001, 2002), large reflex-like force increments during the stimulation period have been reported. In contrast to studies with stimulus contaminations to EMG signals, our method allowed a full investigation of the EMG response during the stimulation period (Fig. 2B). After a large reflex response was induced by the first stimulus, several subsequent responses were considerably depressed. However, the response gradually recovered with repeated stimulations. Moreover, the size of response never reached that of the first H-reflex. The averaged size of the last two H-reflexes was 19.5 ± 2.3% of the first H-reflex (means ± SE across all subjects). This gradual reflex increment was always observed in all 11 subjects prior to subsequent sustained muscle contractions.
Figure 3A shows the effect of an electrical pulse stimulation of the CPN (Fig. 1, arrow 1) on the sustained muscle contractions. This conditioning electrical stimulation reduced the rectified Sol EMG with latency 30 to 40 ms (Fig. 3A, arrows), indicating this EMG reduction might be caused by disynaptic Ia reciprocal inhibition. The degree of reduction in Sol EMG was larger when larger stimulations were used (Fig. 3A). Furthermore, electrical train stimulation of the CPN larger than 1.2 x MT (50 Hz x 2 s) reduced (13 of 29 trials in 4 subjects) or often terminated (13 trials) the sustained muscle contractions (Fig. 3B), as previously reported in animal experiments (Crone et al. 1988). When the intensity of stimulation was 1.05 x MT, it had no effect. As shown in Fig. 3A, the possible disynaptic Ia reciprocal inhibition was followed by excitation and subsequent inhibition. These might partly come from the synchronized firing of motor units. In addition, when the stimulation intensity was strong, it is possible that the strong dorsiflexion evoked by the CPN stimulation induced the stretch reflex response in the soleus muscle and the subsequent silent period. However, it was unlikely that these factors contributed to the termination of the sustained muscle contractions by the train CPN stimulation. This is because the train tibial nerve stimulation failed to stop the sustained muscle contractions (data not shown), although it also induced the H-reflex and the subsequent silent period (see Fig. 3C) as the CPN stimulation did.
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The effect of an electrical pulse stimulation of the tibial nerve (Fig. 1, arrow 2) during sustained muscle contractions is shown in Fig. 3C. The stimulus intensity was set to 1.0 x MT, which can induce nearly a maximal H-reflex in the Sol. This reflexive muscle contraction was followed by the silent period of approximately 100 ms (Fig. 3C, gray bar). However, the Sol EMG level recovered to the level prior to the application of conditioning stimulation.
To quantify the influence of descending commands from the M1, the size of the MEP induced by TMS to M1 (Fig. 4A) was evaluated. Figure 4B indicates that the Sol MEP was significantly smaller (P < 0.005) for the sustained muscle contractions than for voluntary plantarflexion. The Sol BGA was not different between the two muscle contraction modes. Furthermore, the significant interactions (P < 0.005) between subjects and muscle contraction modes existed for the BGA of other muscles (i.e., some subjects had larger BGA for the voluntary plantarflexion). Hence, these subjects had to activate MG, LG, and even TA (i.e., cocontraction) to voluntarily adjust the Sol BGA level to that during sustained muscle contractions. The MEP of these muscles was also significantly larger (P < 0.01 for MG, P < 0.05 for LG and TA) for voluntary contractions (Fig. 4B). However, whether this result reflects some substantial difference between muscle contraction modes is unclear from our experiment, because BGA levels were not matched for both contraction modes.
It is possible that the Sol MEP size only reflects the excitability of the spinal motoneuron pool rather than the M1. Therefore we also examined the excitability of the spinal motoneuron pool using the H-reflex method (Fig. 4C). The result was different from the TMS experiment (Fig. 4D). Specifically, the Sol H-reflex amplitude was at the same level for both contraction modes (the BGA level and the size of the M-response were not different). Furthermore, the significant interaction between subjects and muscle contraction modes (P < 0.005) indicates that the Sol H-reflex of some subjects was smaller for the voluntary plantarflexion. Figure 5A indicates the result of additional H-reflex experiments for six subjects. Even when the magnitude of H-reflex was adjusted to that of TMS, the larger MEP for voluntary muscle contractions (Fig. 5B) cannot be explained by the difference in the excitability of the spinal motoneuron pool.
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In the second additional experiment, the earliest facilitation of the H-reflex was observed at the conditioning-test interval of –3 to –1 ms. The typical facilitation effect is shown in Fig. 6A. In this subject, the earliest facilitation was observed at the conditioning-test interval of –3 ms (TMS intensity was 35% of maximal stimulator output). The amount of the facilitation was statistically significant for the voluntary muscle contraction (P < 0.05), but it was not for the sustained muscle contraction. Figure 6B indicates that the amount of the earliest H-reflex facilitation for all five subjects. In four of five subjects, the amount of the facilitation was significant only for the voluntary muscle contraction (in 1 subject, P = 0.08). The difference in the BGA level could not explain such a facilitation effect in voluntary muscle contraction (Fig. 6C).
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Thus these results indicate that M1 activity itself is lower during the self-sustained muscle contraction than for the ordinary voluntary muscle contractions.
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DISCUSSION |
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, 2002). In those studies, large reflex-like force increments during the stimulation period were considered evidence of plateau potentials in human spinal motoneurons. This is because it closely resembled the firing frequency acceleration of the motoneuron during the neuronal input period at the initiation of plateau potentials (Hounsgaard et al. 1984, 1988; Hultborn 1999). Since stimulus contamination to EMG signals is much smaller in our method, the EMG activity during the stimulation period was fully investigated (Fig. 2B). When double stimulation procedure is used, it is well known that the second H-reflex is almost depressed if the interval is within several tens of milliseconds (Kagamihara et al. 1998; Magladery et al. 1952). In accordance with this well-known behavior, several subsequent responses were considerably depressed (Fig. 2B) after a large reflex response was induced by the first stimulus. However, the response gradually recovered with repeated stimulation (Fig. 2B), which is similar to the frequency acceleration phenomenon (Hounsgaard et al. 1984, 1988). Although gradual increases in muscular responses have been reported in a study on the tonic vibration reflex (De Gail et al. 1966; Matthews 1966; Stuart et al. 1986), this type of H-reflex behavior during repetitive electrical stimulations has not been reported yet. Hence, some novel factors have to counter the well-known depression effect during this recovery period. One of the explanations for this phenomenon is the depolarization of the membrane voltage of the motoneuron through plateau potential emergence.
The gradual reflex increment (Fig. 2B), as well as the force increment reported in previous studies (Collins et al. 2001, 2002), supports the hypothesis that induced muscle activity comes from plateau potentials in human spinal motoneurons. However, as Granit et al. (1957) originally considered, the posttetanic potentiation by repetitive stimulation (Hirst et al. 1981) can contribute to the maintained increase in motoneuronal excitability. Furthermore, it is possible that the temporal summation of excitatory postsynaptic potential evoked by repetitive stimulation could have affected our results. Therefore we have to turn our attention to the sustained muscle contraction rather than to the EMG behavior during the stimulation period.
We hypothesize that the sustained muscle contraction induced here is evidence for the emergence of plateau potentials in human spinal motoneurons or in interneurons at least. To reinforce this hypothesis, several possible counter arguments should be answered. 1) Is the sustained muscle contraction really associated with motoneuron activity? 2) Isn't the sustained muscle contraction generated by reverberating activity within the closed neuronal circuit? 3) Is it true that spinal motoneurons do not receive volitional descending commands from the motor cortex? We conducted three experiments to examine each possibility.
The first matter to be clarified is whether motoneurons are really firing during the sustained muscle contractions. For some pathological situations, like the syndrome of continuous muscle-fiber activity (Isaacs 1961), muscle fibers can be active without motoneuron firing. To investigate this, we provided conditioning electrical pulse stimulation to the common peroneal nerve, which is known to have an inhibitory connection to the Sol motoneuronal pool (Fig. 1, arrow 1) (Crone et al. 1988; Tanaka 1983). If the observed muscle contractions were not associated with motoneuronal activity, this stimulation would not affect the Sol EMG signal. However, the conditioning stimulation reduced the rectified Sol EMG via the reciprocal inhibitory pathway (Fig. 3A), indicating that the self-sustained muscle contractions are certainly supported by spinal motoneuronal activity.
The second possibility is that reverberations of neuronal signals within closed neuronal circuits maintained the self-sustained muscle activity. To investigate this, the silent period of 100 ms was induced by providing electrical pulse stimulation to the tibial nerve during self-sustained muscle contractions (Fig. 1, arrow 2). During the silent period, the firing of spinal motoneurons was actually stopped by several mechanisms, such as the pause of Ia afferent discharges during a twitch contraction (Merton 1951), the Renshaw inhibition (Anastasijevi
and Vu
o 1980), and so on. Hence, it may stop reverberations of neuronal signal(s) within the closed neuronal loop, if the motoneurons are involved in that loop. Therefore, if the sustained muscle contraction was due to its reverberation, it should have also terminated after the silent period. However, this single pulse stimulation was unable to terminate the sustained muscle contractions (Fig. 3C), indicating that at least they are not supported by reverberating activity within closed neuronal loops involving the motoneurons. In contrast, when the possible closed neuronal loops do not involve the motoneurons, the situation is more complicated and it is very difficult to draw a decisive conclusion (see following text).
Whether the volitional descending commands contribute to the motoneuron activity is the third and most critical matter. The following facts still cannot guarantee that descending commands were not associated with the self-sustained muscle contraction: 1) subjects maintained relaxation and 2) they did not recognize their muscle activity. Likewise, although Collins et al. (2001) have described that the self-sustained muscle contraction can be induced even for sleeping subjects, the involvement of M1 in the muscle contraction should be examined quantitatively. To quantify the influence of descending commands from M1, we evaluated the size of the MEP when TMS was applied to M1. If the observed self-sustained muscle contractions were supported by autonomous neuronal activity within the spinal cord, they should not have been accompanied with M1 activity. On the other hand, M1 activity should have always been involved during voluntary plantarflexion (Johannsen et al. 2001). Our hypothesis was that the MEP should be smaller during the self-sustained muscle contractions than during voluntary plantarflexion due to the lower excitability of M1 (Hallett 2000) (assuming equal muscle activity levels). The results shown in Figs. 4, B and D, 5, and 6 indicate that this hypothesis might be correct. Although the result that both the MEP and the H-reflex facilitation by the conditioning TMS was smaller for the self-sustained muscle contractions does not completely exclude the possibility that M1 is not involved in supporting them, the smaller activity of M1 should be compensated by other factors, such as autonomous activity of the spinal motoneuron. Furthermore, the result that some subjects could not voluntarily adjust all muscle activity levels simultaneously to those during the sustained muscle contractions (Fig. 4B) indicates that the self-sustained muscle contractions are apparently different from the voluntary muscle contractions.
Our results reinforce the view that self-sustained muscle contractions induced by our method are primarily maintained by autonomous neuronal activity within the human spinal cord. Considering the similarity of this study to the animal study by Crone et al. (1988), this autonomous neuronal activity is most likely to be explained by the plateau potentials in spinal motoneurons. However, alternative explanations are still possible for the experimental results. For example, our experimental method was unable to exclude the contribution of the closed neuronal circuits whose circuit times were longer than the silent period. However, considering that most of the EMG response to stretch in the Sol lies within approximately 100 ms from stretch onset (Schieppati and Nardone 1997), the contribution of such circuits is small. Another possibility is that neuronal systems, except M1, provide the sustained synaptic excitation to the spinal motoneurons. Their candidate is the plateau potentials in spinal interneurons (Morisset and Nagy 1999) or the reverberating activity within closed neuronal circuits that do not involve the spinal motoneurons as their constituents. These mechanisms can also account for our experimental results without any contradiction. It should be noted that, even in these cases, the present results demonstrate the novel phenomenon that the plateau potentials in interneurons or the sustained activity of neuronal network can be triggered in humans by applying electrical train stimulation to an Ia afferent nerve.
From the conventional viewpoint of motor control, the spinal motoneuron can fire only by receiving excitatory inputs from the supraspinal systems or the peripheral neuronal receptors. However, the present results suggest that the human spinal cord has the ability to generate autonomous neuronal activity maintaining muscle contraction. This finding forces reconsideration of this common belief. In the future, this autonomous activity of the spinal neuronal system should be taken into consideration when investigating the control of movements (Bennett et al. 1998; Collins et al. 2002; Gorassini et al. 2002; Hultborn 1999). For example, under the existence of the autonomous activity mode, the motor cortex does not have to continue to send commands for motoneurons to fire continuously. It only has to send a signal of "switch on" or "switch off" to control them. This may help reduce the burden on supraspinal systems for tasks such as locomotion or standing (Eken 1998). Furthermore, a recent study (Collins et al. 2002) has shown the possibility that the strength of plateaus can be controlled by volitional commands. From the viewpoint of clinical applications, as pointed out in a previous study (Collins et al. 2001), muscle contractions induced by electrical stimulation to the afferent nerve has several advantages over conventional functional electrical stimulation. It can recruit the nonfatigable motor unit at first and it also prevents synchronous muscle fiber contractions. Furthermore, this type of stimulation can be used as a useful and efficient method in preventing muscle atrophy during inactivity of elderly people or during the microgravity conditions of astronauts.
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DISCLOSURES |
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Address for reprint requests and other correspondence: Daichi Nozaki, Department of Motor Dysfunction, Research Institute NRCD, 4–1 Namiki Tokorozawa, Saitama 359-8555, Japan, (E-mail: dnozaki{at}rehab.go.jp).
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1 ms earlier of the effective interval. The H-reflex facilitation was significant (*P < 0.05) in 4 of 5 subjects only for voluntary muscle contraction. In 1 subject, the t value did not reach the significance level (P = 0.08). C: BGA level at the effective conditioning-test interval was expressed as the percentage of that at 1 ms earlier than this interval. Note that the BGA level did not explain the results in B.