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1School of Kinesiology, Simon Fraser University, Burnaby, British Columbia, Canada; and 2Department of Neurosurgery, Upstate Medical University, Syracuse, New York
Submitted 11 October 2005; accepted in final form 2 June 2006
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ABSTRACT |
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80% of the motor-unit pairs examined. There was no difference in rotation incidence by muscle type. For the unit pairs showing rotation, surface EMG values were significantly higher immediately prior to rotation than after rotation had occurred. Our findings show that rotation of motor units with similar recruitment thresholds during such contractions is common in distal muscles of the arm and leg and may help offset neuromuscular fatigue. |
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INTRODUCTION |
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). The potential benefit of motor-unit rotation during a sustained, sub-maximal contraction is obvious: alternating discharge periods of motoneurons with close recruitment thresholds would allow time for the contractile elements of the now-silent motor unit to recover their ability to generate force, while the overall force being produced within the muscle remains constant (or nearly so).
The findings by Forbes were disputed when numerous investigators reported an inability to demonstrate rotation during prolonged contractions in humans (Gilson and Mills 1941; Lindsley 1935; Smith 1934). This concept was revisited in the 1970s through multiple studies (Person 1974; Smith et al. 1974; Thomas et al. 1978). Once again, though, there was limited enthusiasm for this position, as it was frequently interpreted as an exception to the "size principle" of motoneuron recruitment (Henneman et al. 1965).
The continuing controversy on this subject is perhaps due to terminology and methodological differences (Stuart et al. 1983). As used by Forbes (1922), rotation describes an increase in threshold of a rhythmically discharging (i.e., tonic) motoneuron during prolonged usage. A motor unit of similar threshold is now recruited, while the "fatigued" unit cannot continue to discharge. After some minutes, this second motor unit falls silent, and the originally discharging unit resumes tonic discharge. Thus the two motor units have "rotated" in their discharge without causing an appreciable change in force output.
Most studies reporting motoneuron rotation did so using functional tasks that differed in subtle but nevertheless important ways (Fallentin et al. 1993; Person 1974; Smith et al. 1974; Thomas et al. 1978). Thus recruitment within a given task group (Loeb 1985) was orderly, but motoneurons contributing to different task groups showed short-term recruitment patterns that appeared to be disorderly (i.e., erroneously referred to as rotation) as these different contraction tasks were carried out (Riek and Bawa 1992).
The question remains: has rotation—as originally described by Forbes (1922)—been clearly described in human motoneurons during prolonged contractions? A study by Westgaard and De Luca shows the answer is "yes," at least for the trapezius muscle (Westgaard and De Luca 1999). These authors attributed this rotation to the fact that trapezius is a postural muscle, in which low-threshold units are expected to be active for prolonged periods of time, conditions that would presumably favor motoneuron rotation. In a follow-up study by Adam and De Luca (2003), rotation of vastus lateralis motoneurons during relatively brief contractions was not observed. Our goal through the present study was to expand on these findings of Westgaard and De Luca (1999), by showing that motor-unit rotation does indeed occur in distal muscles of the upper and lower limb in normal human subjects, provided that prolonged contractions are utilized.
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METHODS |
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Six subjects (3 female and 3 male, 21–60 yr) were studied; five subjects were tested multiple times. Four subjects were naive to the study's goals; the other two subjects (authors PB and BC) did not intend to examine rotation during the preliminary studies involving transcranial magnetic stimulation (TMS) and nerve stimulation (see following text). Therefore most of the data were collected without the possibility that subjects could bias the findings by modifying their contraction strategy. Studies were approved by the Ethics Review Boards of Simon Fraser University and Upstate Medical University. All subjects signed an Informed Consent form before participating.
Instrumentation
Data were collected from one of the following muscles: flexor carpi radialis (FCR), extensor carpi radialis (ECR), tibialis anterior (TA), or soleus. Surface electromyography (EMG) was recorded with a pair of pregelled or Ag/AgCl-paste electrodes applied to the skin overlying the muscle belly. Single motor-unit (SMU) activity was recorded with a concentric or a bipolar needle electrode (Nicolet Biomedical) inserted in one of the muscles under study; typically the needle tip was inserted between the two surface electrodes. Signals were amplified (typically x10,000) and filtered (30 Hz to 2 kHz for surface EMG; 100 Hz to 5 kHz for needle EMG) prior to storage on digital tape (Wintron Technologies VDAT8 or Microdata Instruments MD-1600) for later analysis. Audio and visible feedback [Spike2; Cambridge Electronic Design (CED)] of surface- and needle-recorded EMG was provided throughout all recording sessions. In some cases, isometric force (torque) at the wrist or ankle was measured with a strain gauge [EA-13-250MQ-350 (Measurements Group) or FT03 (Grass Instruments)]. Force signals were amplified (Vishay Instruments/Measurements Group) and also stored on tape.
In an earlier study, we examined the influence of brief ultra-high-frequency excitatory inputs on the recruitment properties of tonically active motoneurons, using both repetitive TMS (Bawa and Calancie 2004) and repetitive Ia afferent stimulation. In carrying out these studies, we frequently observed rotation between pairs of distinct motor-unit potentials being recorded for long periods at a time. Episodes of such rotation from these earlier studies were reanalyzed and included herein, and comprise 20% of the total sample. For both inputs, stimuli were delivered about every 7–9 s, using an intensity just adequate for causing recruitment (i.e., threshold-level). For TMS, a MagStim "Pyramid" unit (i.e., 4 MagStim 200 units linked via 3 BiStim units) was connected to a double-cone coil optimized for stimulation of either hand-area or leg-area of the motor cortex. For Ia afferents, stimuli to the median nerve (at the elbow, for activating FCR) or tibial nerve (at the knee, for activating soleus) were delivered by a Digitimer DS7A constant-current stimulator driven by a Master 8 pulse generator. Stimulus pulse-width was 0.5 and 1.0 ms for median and tibial nerves, respectively.
Protocol
The subject's task was to gently contract the test muscle until a motor unit with a clearly defined potential was recruited into rhythmic discharge. The subject was to then modulate the force of contraction as necessary to maintain continued tonic discharge of that motor unit at a constant discharge rate until either the motor-unit potential could no longer be discriminated from other potentials (suggesting a shift in position of the recording electrode tip) or the subject needed to rest. In the event that a second well-defined motor-unit potential now also began to discharge tonically, the subject was asked to relax the contraction just enough to cause one of the two motor-unit potentials to fall silent. The discharge rate of the motor unit being examined was typically 10 Hz for FCR, ECR, and TA motor units, and 6 Hz for motor units from soleus (i.e., these were weak contractions). For the majority of motor-unit pairs examined, there were no external perturbations of motoneuron excitability beyond those caused by the voluntary contraction efforts of the subjects. Alternatively, excitatory inputs (TMS or Ia stimulation, as described in the preceding text) were superimposed on this voluntary contraction and tonic SMU discharge. An experiment usually lasted from 2 to 4 h, often involving contractions and continuous motor-unit discharge for periods of 
30 min.
Analysis
All analysis was conducted from the taped records. Each motor-unit waveform was identified and discriminated by Bak window discriminators, producing a TTL pulse for each spike of the same motor unit. Sometimes the motor-unit waveform changed gradually during the course of the experiment; when this occurred, adjustments were made to the Bak controls to maintain accurate waveform discrimination. Surface EMG, needle-electrode EMG, force, and TTL pulses were digitized (CED) and stored on a hard-drive. Acquisition rates were 4 and 15 kHz for surface- and needle-EMG, respectively. All spike trains and corresponding TTL pulse records were manually compared, and errors in discrimination were corrected. As a further safeguard against possible errors in motor-unit waveform discrimination, the surface-EMG potential associated with a given TTL pulse was averaged at different times throughout the period of tonic activity; this potential serves as a "fingerprint" of the muscle unit, remaining constant despite changes in shape of the needle-recorded motor-unit potential.
The instantaneous discharge rate of motor units was calculated from their TTL pulse train and expressed as a histogram. Surface EMG was offset to 0 V and rectified. The mean rectified EMG amplitude over a 5-s period was calculated at four different times relative to an episode of rotation between two motor units: 1) T1—beginning 20 s before unit 2 was first recruited (i.e., while unit 1 was still discharging tonically); 2) T2—beginning 5 s before unit 2 was first recruited; 3) T3—beginning immediately after unit 1 fell silent [i.e., when unit 2 (only) was now discharging tonically]; and 4) T4—beginning 20 s after unit 1 fell silent. In trials including TMS or Ia stimulation, stimulus artifacts were excluded from the sampled periods, to avoid introducing errors in EMG values. For each motor-unit pair, EMG values at T2–T4 were expressed relative to the value at T1 (i.e., values were normalized). These normalized EMG values were examined through repeated-measures ANOVA followed by Tukey pair-wise testing. Comparison of the incidence of motor-unit rotation across different muscles was made with the 
2 test. Statistical testing was carried out with SigmaStat. Results were considered significant for P < 0.05.
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RESULTS |
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Figure 1A illustrates a 36-min period during which unit 1 (from ECR) was discharging at a rate of 10 Hz after being recruited at an earlier time (not shown). During the first phase of unit 1 discharge, both force (Fig. 1C) and surface EMG (Fig. 1D) were increasing (that is, the subject needed to gradually increase the contraction strength to maintain unit 1's discharge rate). This gradual increase in threshold continued until unit 2 began to discharge tonically (Fig. 1B, midway through the record). As instructed, the subject relaxed the strength of contraction until only one of the two motor units continued to discharge tonically, and it was unit 1 that fell silent. This relaxation is evident in a decline in both force and EMG magnitude, especially evident once unit 1 stops discharging (best seen in the needle-EMG record of Fig. 1E). After 6 min of unit 2 tonic discharge, unit 1 was again recruited to discharge. Note the increase in force and EMG leading up to the resumption of unit 1 tonic discharge as the subject's contraction effort needed to maintain unit 2 in the tonic discharge mode was now increasing. This represents a complete rotation of motor-unit discharge, beginning with unit 1 alone, a brief period with both units discharging, then unit 2 alone, a second brief period of both units discharging, and a cessation of unit 2 discharge while unit 1 remained tonic. Toward the end of this record, the threshold for tonic discharge of unit 1 increased even further (as evidenced by higher extension force and surface EMG magnitudes), leading to the re-recruitment of unit 2. At this time, repeated attempts to silence one of the two motor units by relaxing wrist extensor contraction led to a cessation of unit 2 discharge in each case, while unit 1 continued to discharge tonically. That is, rotation did not recur in this unit pair. Although not evident in this example, such recurrence of rotation was seen in 1/3 of the unit pairs examined (note that this incidence of recurrence may well have been higher, but we often stopped data collection after completing a full rotation sequence, due to time constraints or subject fatigue).
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A strong phasic excitatory volley can temporarily disturb the recruitment order of motoneurons (Westad et al. 2003). In the 20% of trials showing rotation that were studied while applying either TMS or Ia stimulation, did these excitatory inputs distort or otherwise alter the excitability of the tonically active motor units? Examples illustrated in Fig. 2 address this question. Each of the three subpanels of Fig. 2 illustrates different trials in which unit 1 discharge was joined by unit 2 discharge, and unit 1 then fell silent (i.e., the 1st portion of a rotation episode). The stimuli being delivered were then discontinued for a number of seconds (evident by an absence of stimulus artifacts), and the subject was asked to increase the strength of contraction until another motor unit was recruited (at the curved arrows in the "EMG" panels of Fig. 2, A–C). In each of these examples, unit 1 was re-recruited through a higher contraction effort (evidenced by increased EMG, and an increased discharge rate of the tonically active unit 2). Thus the behavior of unit 1 shortly after falling silent during a rotation episode was similar whether or not TMS/Ia stimuli were being delivered, which was why these data were grouped together with those obtained without TMS or Ia stimulation.
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29% higher than at any of the other three time points examined, as illustrated in Fig. 3. Based on ANOVA followed by Tukey pair-wise comparisons, the mean value at T2 was significantly higher than at any of the other three time-periods examined (P < 0.001 for all 3 comparisons). None of the remaining three mean values were significantly different from one another (P > 0.5 for each). In other words, the increasing contraction effort needed to keep unit 1 tonic ultimately led to recruitment of unit 2, which now continued to discharge even though the subject partially relaxed the strength of contraction, resulting in lower mean surface EMG values and cessation of unit 1 discharge after the first portion of each rotation episode.
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2 analysis, there was no significant difference in the incidence of rotation by muscle [incidence of rotation for ECR, FCR, TA, and soleus was 75, 74, 70, and 71%, respectively (2 = 0.049; P = 1.00)]. |
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DISCUSSION |
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and expanded on by Westgaard and De Luca (1999). In the present study, rotation was noted only between motor units of similarly low threshold, it took many minutes of continuous motor-unit discharge before rotation occurred and appeared to be unaffected by low intensities of repetitive TMS or Ia stimulation. We believe that motor-unit rotation was due neither to movement of the electrode nor to changes in the task. Motor units 1 and 2 of the rotation pair routinely discharged simultaneously for brief periods of time during a steady isometric contraction, as illustrated in both Figs. 1 and 2. Based on averages of a motor unit's surface EMG "fingerprint" from different stages of a rotation episode, we are confident that the discrimination of needle-electrode waveform shapes was accurate, ruling out needle electrode movement as a basis for the rotation episodes seen.
From the present study, then, we found that rotation between motor-unit pairs was surprisingly common. An obvious question is: why haven't other investigators—with the exception of Westgaard and De Luca (1999)—seen rotation between motor unit pairs with this prevalence? Several explanations are possible. The first is study design: the goal of the present experiment was to maintain the discharge of only one motor unit at a constant, low rate for a prolonged period (i.e., 30 min). If the subject fails to maintain constant motor-unit discharge (e.g., allowing the tonic unit to fall silent for a few seconds), it is possible that the mechanisms leading to a steady increase in threshold (see following text) are balanced by a recovery. The original balance in thresholds between two motor units of near-identical recruitment threshold would be restored, and no rotation would be seen. This may explain why studies in which periods of motor unit discharge were brief (Adam and De Luca 2003) or firing rates were modulated on a cyclical basis (Griffin et al. 1998) failed to demonstrate rotation.
Because rotation occurs only between motor units of close recruitment threshold, another requirement for observing rotation is that muscle fibers included in the second, higher-threshold motor unit must lie within the recording region of the needle electrode. Based on this argument, one would expect a higher yield of rotation if experiments identical to those described in this report were carried out but with multiple recording needle electrodes placed within the target muscle. This would expand the volume of muscle being sampled simultaneously, while still allowing one to examine spike-triggered surface EMG for distinguishing between different motor units. We did not attempt such studies.
Mechanisms for rotation
There appear to be at least two competing mechanisms influencing motoneuron discharge probability once it has been recruited to discharge tonically. On the short term, a persistent inward current (PIC) at the dendritic level sets up once a motoneuron begins discharging, and this may lower by a significant amount the required current from extrinsic synaptic sources to maintain that motor unit discharging tonically. This current has been described in the cat, rat, and human motoneurons (Eken 1998; Gorassini et al. 2002; Heckman et al. 2005). The time frame for this event is measured in terms of seconds to minutes. This was evident in the present study by the diminished effort (i.e., lower surface EMG) (Calancie et al. 2001) needed to keep unit 2 tonic once it had been recruited.
Once the motor unit was tonic and over a more prolonged time frame, slow inactivation of Ca2+ and Na+ PICs may lead to gradually increasing requirements for additional synaptic current to keep the motoneuron discharging tonically (Heckman et al. 2005). Inactivation of persistent Ca2+ currents has been demonstrated in snail neurons with a long (10 s) time constant (Oyama et al. 1986). Its presence has also been shown in spinal motoneurons of the cat (Schwindt and Crill 1980) and in a modeled mouse motoneuron (Carlin et al. 2000). Inactivation of Na+ PICs could also lead to an increase in threshold (Lee and Heckman 2001). Other possible contributors to a gradual increase in threshold of a tonically active motor unit—leading to rotation—include a slow inactivation of Na+ channels (Miles et al. 2005; Vilin and Ruben 2001) and/or a slowing down of the transmembrane Na+-K+ pump. Indeed, Kiernan and colleagues suggested this to explain their observed increase in threshold of motor axons within the median nerve of normal human subjects after 10 min of 8-Hz stimulation (Kiernan et al. 2004). These values are well within the time frame of changes noted in the present study.
Conclusion
In conclusion, data from the present study demonstrate that during a prolonged and weak isometric contraction, the threshold of a motor unit increases such that rotation between motor-unit pairs of similar recruitment threshold is common within multiple muscles of both upper and lower limbs and is not specific just to postural muscles (Westgaard and De Luca 1999). This phenomenon does not appear to be preplanned centrally, as was proposed by Forbes (1922) but instead reflects the intrinsic (or local) organization of motoneuron pools innervating the muscles examined in this study. These pools have large numbers of motoneurons with similar recruitment thresholds receiving, within a given motoneuron pool, comparable synaptic drive. Using information theory, Senn and colleagues showed that during contractions, rotation between close neighbors (in terms of motor unit properties) introduces very little error in transfer of information, particularly among low-threshold units (Senn et al. 1997). Precision of force production, under these circumstances, would not be compromised significantly, while this pattern of motor-unit behavior would allow persons to carry on a contraction over longer periods of time. Hence, our observations seem entirely plausible with the idea put forth by Forbes, that motoneuron rotation is just one mechanism combating the cumulative effects of fatigue.
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GRANTS |
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FOOTNOTES |
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Address for reprint requests and other correspondence: B. Calancie, Dept. of Neurosurgery, 750 E. Adams St, IHP 1213, Syracuse, NY, 13210 (E-mail: calancib{at}upstate.edu)
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ABSTRACT
INTRODUCTION
