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1Graduate Program in Neuroscience, 2School of Physical Therapy, 3Department of Physiology and Pharmacology, The University of Western Ontario, London, Ontario, Canada
Submitted 26 September 2006; accepted in final form 30 March 2007
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ABSTRACT |
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INTRODUCTION |
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; Masani et al. 2003). The strength of this relationship reflects the importance of ankle plantarflexor activity in controlling AP sway.
During isometric contractions, the modulations in the discharge rates of concurrently active motor units have been shown to be correlated (Erim et al. 1999; Semmler and Nordstrom 1998). These common modulations in the firing rates of multiple motor units are believed to reflect a ‘common drive’ (De Luca et al. 1982), which is thought to demonstrate a level of efficiency in the organization of inputs to the motoneuron pool in that the motor units are controlled by a common drive rather than separate command signals (De Luca and Erim 1994). Although common drive has been observed in motor unit pairs within a muscle (De Luca et al. 1982; Semmler et al. 1997), it has been demonstrated also in motor unit pairs between homologous muscles in the trunk (Marsden et al. 1999) and in the lower limb (Mochizuki et al. 2006). Marsden and colleagues (1999) suggested that common drive allows axial muscles to function as a solitary entity during postural control.
The source of common drive is not known; although, it has been proposed that descending inputs provide for the common oscillations in motor output (De Luca and Erim 2002). Soleus motoneurones receive inputs from a number of descending systems, notably the vestibulospinal system (Grillner et al. 1970). In man, corticospinal projections to soleus motoneuron pools are thought to be relatively weak as compared with upper extremity muscles (Brouwer and Ashby 1990). For example, the extent of motor unit synchrony within the extensor digitorum muscle, a muscle with strong corticospinal innervation, was high (CIS = 0.7) (Keen and Fuglevand 2004), yet the within-muscle assessment of synchrony of soleus motor units during an isometric task was low (CIS = 0.34) (Mochizuki et al. 2005). Similarly, De Luca et al. (1982) reported high common drive coefficients (
> 0.6) within the FDI, whereas Mochizuki et al. (2006) found low common drive coefficients for motor unit pairs within a soleus muscle ( = 0.38) during isometric tasks. We sought to explore the influence of corticospinal inputs on the common modulation of motor unit discharge in postural tasks by having subjects sway voluntarily.
Common modulation of motor unit activity could be influenced by proprioceptive inputs as reductions in proprioceptive input have produced lower common drive values (Garland and Miles 1997). The role of proprioception on common modulation of motor unit discharge may be examined during the control of standing posture because of its role as a contributor of sensory information regarding the status of the ongoing control process. Proprioception plays a significant role in the control of standing posture because the removal of either vestibular or visual inputs produces no significant increases in postural sway (Dichgans and Diener 1989). However, the removal of proprioceptive inputs through ischemia increases the extent of postural sway at a frequency of 1 Hz (Mauritz and Dietz 1980).
In a previous paper (Mochizuki et al. 2006), we showed that the common modulation of soleus motor unit firing rates was lower during an isometric contraction than in a standing postural task. In the current study, we sought to manipulate proprioceptive input received by the soleus muscle as the body sways while maintaining upright posture. The purpose of the present paper is to determine the influence of cortical and proprioceptive inputs on the common modulation of concurrently active soleus motor units from the left and right legs during standing posture. We hypothesize that subcortical descending inputs and proprioceptive afferent inputs affect the common modulation of motor units bilaterally during standing.
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METHODS |
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Eight subjects (5 males and 3 females; height, 169.7 ± 11.3 cm; weight, 72.4 ± 17.5 kg; age 29.0 ± 7.2 yr) with no known neuromuscular disorders participated in this study after providing informed written consent. This study conformed to the standards established by the Declaration of Helsinki and was approved by the Review Board for Health Sciences Research Involving Human Subjects at the University of Western Ontario.
Experimental procedure
Experiment 1.
With the removal of vision, subjects must rely more on vestibular and proprioceptive signals to control standing posture. Thus this experiment involved altering the contribution of vision to postural control and assessing the effect of changing the sensory inputs mediating balance on common drive to soleus motoneurons bilaterally.
Eight subjects performed two, randomly ordered standing trials of 5-min duration with the eyes open and closed, separated by a brief rest period during which the subjects remained standing but could lean against a support. Allowing subjects to lean provided a brief rest while ensuring that the same motor units were recorded and that subjects kept the same foot positions during both tasks.
Subjects stood with their feet shoulder width apart on adjacent AMTI OR6-6 (Advanced Mechanical Technology, Watertown, MA) force platforms. For the duration of the trial, subjects stood with their arms hanging loosely at their sides with the head facing forward. Portions of this data set have been used in previous studies using different analytic techniques (Mochizuki et al. 2005, 2006).
Experiment 2.
By vibrating the Achilles tendon of one leg, a difference in the proprioceptive input received by the right and left soleus motoneuron pools was created. It has been shown previously that voluntary sway increases when the Achilles tendon is vibrated, more so when the eyes are closed as compared with when the eyes are open (Nakagawa et al. 1993). Therefore in the current study, we altered proprioceptive input during an eyes-closed postural task.
Six subjects stood with their eyes closed and with each foot on adjacent force platforms with vibrators (Wahl, Sterling, IL) fastened to the Achilles tendon of each leg. The vibrators were suspended on elastic cords, which hung from a metal frame located behind the subject. This set-up allowed the vibrators to move freely with the subject rather than acting as an anchor that would limit the COP excursions in the AP direction. The ends of the vibrators were kept in contact with the Achilles tendon by a Velcro strap that wrapped around the leg just proximal to the ankle joint. The dual vibrator set up was used as a control for ensuring that any changes in the COP induced by the weight of the vibrators was the same bilaterally.
The subjects stood quietly for 200 s, after which one of the vibrators (randomly chosen) was turned on. The vibrator stimulated the Achilles tendon at 100 Hz with a peak-to-peak displacement of 5 mm. The vibration continued for 200 s. Subjects continued to stand quietly after the vibration was turned off to determine if the motor unit behavior returned to the previbration state.
Experiment 3.
To increase corticospinal drive to the soleus motoneurone pool, subjects performed two voluntary tasks: voluntary sway and variable isometric force task. Both tasks had similar frequencies of oscillations in ankle plantarflexion force but differed in their postural demands and the type of muscle contraction (isometric vs. anisometric).
VOLUNTARY SWAY.
Six subjects participated in a task in which they were required to sway voluntarily while standing looking straight ahead, keeping their head still and eyes open. Their hands were at their sides, and each foot was positioned on adjacent force platforms. Subjects leaned forward slightly if single motor units were not detected in an electrode in quiet stance. The position at which a motor unit was recruited was taken as the most posterior position of sway. Subjects then gradually swayed forward over a 10-s period. The position reached at the end of the 10 s was taken as the most anterior position of sway, then the subjects swayed back over a 10-s period toward the posterior position. Subjects performed 10 full cycles for 
200 s. No feedback was provided to the subjects other than an auditory count of elapsed time over each half-cycle (i.e., a count from 1 to 10). A voluntary sway frequency of 0.05 Hz was used to avoid recruitment of additional motor units.
VARIABLE FORCE.
Subjects (n = 6) were seated in a chair, looking straight ahead, with their feet placed on separate force platforms and with their hips, knees, and ankles at 90° angles (Mochizuki et al. 2006). They performed a bilateral low-force isometric plantarflexion contraction against a rigid bar that was positioned over the distal thigh, just proximal to the patella and secured to a frame. Subjects gradually increased the plantarflexion force until a single motor unit was detected on each electrode. This level was taken as the lowest level of force produced during the trial. Subjects then gradually increased the force over a 10-s period. The subjects continued to increase and decrease the force at a frequency of 0.05 Hz for a total of 10 full cycles (200 s) and received auditory feedback regarding the elapsed time of each half-cycle. Subjects did not receive ongoing feedback regarding the motor unit activity. However, the experimenters monitored the recordings and if the subjects lowered the force too much, and derecruited the motor unit, subjects were asked to increase the force until the motor unit could be detected again. The vertical ground reaction force (Fz) from each force platform was used as an indication of plantarflexion force changes.
Data acquisition
Using a 16-bit acquisition system (Power 1401 with Spike2 software, Cambridge Electronic Design, Cambridge, UK), all signals were digitized on-line. All data were stored on an IBM Pentium III laptop computer (International Business Machines, Armonk, NY) for off-line analysis.
ELECTROMYOGRAPHY.
Single motor unit potentials were recorded intramuscularly using a pair of 50-µm stainless steel fine wires (California Fine Wire, Grover Beach, CA), in a bipolar configuration. The wires were fastened together at the tip using cyanoacrylate adhesive and then passed through a disposable 2-cm-long, 25-gauge hypodermic needle (Becton Dickinson). A hook of 1–2 mm in length was formed at the recording end of the electrode. The needle was used to insert the electrode into the soleus to a depth of 2 cm and then extracted, leaving the wire embedded within the muscle. All wire electrodes and hypodermic needles were sealed and autoclaved (AMSCO Autoclave) for 45 min at 120°C prior to use. The signals from the intramuscular electrodes were sampled at 25 kHz.
Surface EMG from the soleus (SOL), medial gastrocnemius (MG), and tibialis anterior (TA) muscles was recorded using bipolar Ag-AgCl electrodes (8 mm diam, 20-mm interelectrode distance). The EMG signals were amplified, filtered (10–1,000 Hz), sampled at 2,500 Hz and saved for off-line analysis. The root mean square (RMS) amplitude of the surface EMG was assessed for 10 s, sampled quarterly for the duration of the trial, and averaged between legs.
Four fine wire electrodes (2 on each leg) were inserted at approximately the same positions (15 cm proximal to the lateral malleolus) in the lateral aspect of each soleus muscle. Within each muscle, the electrodes were located 2–3 cm apart in a proximal-distal orientation. At the beginning of the trial, the position of the electrodes was adjusted as necessary to record single motor unit activity on as many of the four channels as possible. It was rare for all four electrodes to have clean recordings simultaneously; thus the number of bilateral motor unit pairs recorded in each subject varied. Once the best electrode positions were found, the electrodes were not moved again. In the postural task, normally only one motor unit could be analyzed per electrode. However, the lack of movement in the voluntary isometric task made it easier to analyze more than one motor unit per electrode.
FORCE PLATFORM MEASURES. Three signals from each force platform (Mx, My, Fz) were sampled at 500 Hz and saved for off-line calculation and analysis of the COP displacements in the AP direction.
Data analysis
MOTOR UNIT DISCHARGE CHARACTERISTICS. To evaluate the motor unit discharge characteristics during each task, the mean ISI and coefficient of variation (CV) of ISIs for each motor unit was calculated as the arithmetic mean of both legs.
COMMON DRIVE.
Single motor units were discriminated off-line using a template-matching algorithm (Spike2, version 4.15, Cambridge Electronic Design) that classified motor units according to their shape and amplitude. Motor unit spike trains were divided into 5- to 10-s-long epochs, provided that all interspike intervals (ISIs) within that epoch were between 50 ms and 2 x mean ISI (calculated over 20 s of data). ISIs of <50 ms were considered to result from misclassified spikes while the upper limit of 2 x mean ISI was used as a way of controlling for the skewed distribution produced as a result of excessively long ISIs (Andreassen and Rosenfalck 1980). This process was necessary because any gaps or extra spikes caused large erroneous deviations in the smoothed firing rate (see following text). If a section of the data within an epoch did not meet the aforementioned criteria, the entire epoch was discarded and the next 5- to 10-s epoch immediately after the discarded section was assessed. These criteria ensured that only sections of stable repetitive firing were analyzed, as indicated by a low coefficient of variation of ISI (Table 1).
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). Briefly, the smoothed time-varying firing rate of the motor unit was determined by centering a 600-ms-wide symmetrical raised cosine bell function sampled at 1,000 Hz to each classified action potential. This series of cosine functions produced a depiction of the motor unit firing rate for the duration of the trial. The mean firing rate was then removed using a zero-phase filter with a –3-dB low-frequency cutoff at 0.75 Hz. The common drive was calculated in motor unit pairs using the built in "waveform correlation" function for epochs meeting the preceding criteria. Each pair consisted of one motor unit from the left leg and one motor unit from the right leg. The correlation was determined by multiplying the two waveforms together on a point-by-point basis and summing the products. This sum was normalized to account for changes in waveform amplitudes and the number of points included in the correlation. This produced a single value. The reference waveform, arbitrarily chosen in these experiments as the left leg, moved to the next point and the process was repeated to produce the subsequent result. The entire process was repeated for all the result bins within ±0.5 s. The common drive coefficient was taken as the maximal value of the function lying within ±50 ms of time = 0 ms. The reported common drive value for each motor unit pair was the average of all epochs.
COP. COP excursions in the AP direction were determined using the vertical ground reaction force (Fz) and moment of force in the sagittal plane (Mx) as measured by the force platforms such that APCOP = Mx/Fz.
PHASES OF SWAY AND FORCE PRODUCTION. The COP position was divided into distinct phases (see Fig. 1 A). Using the DC-removed signals, Phase 1 was determined to be the portion of the signal from the most posterior (or lowest force) position to the neutral or mid-force position. Phase 2 was taken as the portion of the signal from neutral to the most anterior (or highest force) position. Phases 3 and 4 were the portions of the signal from most anterior (or highest force) to neutral and from neutral to most posterior (or lowest force), respectively. The phases of sway were also determined during quiet stance; however, because the oscillations in sway were smaller during quiet stance, the phases of sway were determined by assessing the mean position of the COP relative to neutral (a positive or negative value) and the slope of the excursion of the COP for the measured epoch (positive or negative). For the quiet stance (eyes open, experiment 1), voluntary sway and variable force tasks (experiment 3), common drive was assessed for each epoch. The common drive values were then categorized by phase to assess the mean common drive for each phase.
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Statistical analysis was performed using SPSS for Windows v11.0 (SPSS, Chicago, IL). Paired t-tests were used to determine whether common drive differed between the eyes open and eyes closed task and whether common drive differed before and during the application of vibration. The data did not meet the requirements to use parametric statistics for the comparison of common drive coefficients for the eyes open quiet standing task, voluntary sway, and variable force tasks across phases; thus Kruskal-Wallis H tests were used to ascertain whether differences in common drive occurred as a function of phase for each task (Portney and Watkins 2000). When these differences were significant, Mann-Whitney U tests were used to determine the phases across which the common drive coefficient differed. Two-way repeated-measures ANOVA was used to ascertain whether the mean ISI, coefficient of variation (CV) of ISI, and RMS of surface EMG in each task differed across tasks or phases. Unless stated otherwise, all values are presented as means ± SD, and P 
0.05 was used as the requirement for statistical significance.
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RESULTS |
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The removal of vision had no effect on the discharge characteristics of the motor units that were recorded (n = 56, 28 bilateral motor unit pairs). While standing with the eyes open (EO), the mean ISI for the soleus motor units was 131.4 ± 22.7 ms (Table 1). With the eyes closed (EC), the mean ISI was 132.5 ± 24.9 ms. There was no difference in the extent of common drive in bilateral motor unit pairs; the common drive for the EO condition was 0.51 ± 0.15 with an offset of –10.9 ± 21.0 ms and 0.51 ± 0.19 with a peak offset of –4.6 ± 22.0 ms for the EC condition.
On further inspection of the data, it became apparent that in approximately half of the motor unit pairs, the common drive in the EO condition was clearly greater than the EC (n = 13) and vice versa (n = 15). When the common drive was greater in EO than EC, the common drive coefficient was 0.53 ± 0.15 and 0.39 ± 0.17, respectively. When EC was greater than EO, the common drive was 0.62 ± 0.14 and 0.49 ± 0.16, respectively. This was related to the order of testing; when the common drive was greater in the EO condition, EO was performed first and when the EC was greater, the EC condition was performed first. Figure 2 shows the mean common drive data for each condition in the order of testing. A paired t-test revealed that there was a significant effect of order such that the common drive was lower for the task that was performed second (P = 0.007).
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With the eyes closed, the mean ISI for the soleus motor units averaged between legs was 151.1 ± 20.2 ms prior to the onset of vibration and 151.1 ± 25.0 ms during the vibration (Table 1). Separating the legs according to which one received the vibration revealed a systematic effect of vibration on the motor unit firing rate. Prior to vibration, the mean ISI for the motor units on the leg to be vibrated and the leg not vibrated were 151.0 ± 21.0 and 151.1 ± 20.0 ms, respectively. The mean CV of ISI for the vibrated leg was 16.9 ± 4.7 and 15.7 ± 4.7% for the nonvibrated leg. With the application of vibration, the mean ISI and CV of ISI for the vibrated leg became 146.3 ± 23.0 ms and 13.6 ± 3.5%, respectively, and 155.9 ± 26.5 ms and 16.2 ± 4.9%, respectively, for the nonvibrated leg. Two-way repeated-measures ANOVA revealed that vibration was associated with a decrease in the mean ISI on the vibrated leg and an increase in the mean ISI in the nonvibrated leg. Similarly, the CV of ISI decreased on the vibrated leg.
The common drive coefficient decreased significantly (P < 0.001) from 0.55 ± 0.16 to 0.45 ± 0.16 with the application of vibration (n = 23 motor unit pairs). The average peak offset for these pairs was –5.9 ± 20.0 ms prior to vibration and –0.5 ± 18.6 ms during vibration. The decrease in common drive was not attributable to an order effect because the common drive after the cessation of vibration returned to their previbration level ( = 0.55 ± 0.10, peak offset of 14.9 ± 21.3 ms). Although the motor units in experiment 2 discharged slower than in experiment 1 (Table 1), there was no significant difference in the common drive coefficient in the eyes closed condition between the two experiments. Figure 4 illustrates the changes in motor unit discharge with vibration.
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= 0.91 ± 0.03). With the application of vibration, the correlation in AP sway remained high ( = 0.89 ± 0.03) but was significantly lower (P = 0.004, paired t-test) than the correlations obtained without vibration. Vibration also induced a shift in the position of the mean COP such that the leg receiving the vibration moved 0.3 ± 0.9 cm posteriorly, whereas the COP of the leg not receiving vibration moved 1.0 ± 0.6 cm posteriorly. These findings indicate that alterations in proprioceptive inputs caused deterioration of the common drive between legs and adaptive responses in postural sway. Experiment 3: voluntary sway and variable force
In the voluntary sway condition (n = 20 motor unit pairs), the mean ISI for the soleus motor units was 138.8 ± 24.9 ms, similar to the EO natural sway condition in experiment 1 (Table 1). In the variable force condition (n = 24 motor unit pairs), the mean ISI was 146.1 ± 17.0 ms. There was no significant difference in the mean ISI between motor units recorded during voluntary sway and those during variable force. However, the mean common drive was significantly higher (P < 0.001) during voluntary sway ( = 0.34 ± 0.16) than in variable force tasks ( = 0.16 ± 0.13). The peak offset for the variable force and voluntary sway tasks were –3.8 ± 13.7 and 8.9 ± 41.9 ms, respectively. The common drive was significantly lower during both voluntary sway and variable force tasks than all other conditions of quiet standing in experiments 1 and 2.
Common drive was examined further by dividing the tasks into phases of sway. During voluntary sway, the mean ISI of the soleus motor units was lowest during phases 2 and 3 when the COP was in an anterior position and the CV of ISI was significantly higher in phase 1 as compared with phases 3 and 4 (Table 2, Fig. 1). The mean common drive coefficient also differed by phase (Fig. 5). Specifically, the common drive values for phases 1 and 2 (i.e., as COP moved anteriorly) were significantly higher than those of phases 3 and 4 (i.e., as COP moved posteriorly).
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The plantarflexion torque produced during the variable force task was estimated using the calibrated Fz signal obtained from the force platforms and a moment arm of 0.22 m taken as the distance from the ankle joint and the location of the COP on the force platforms. The mean plantarflexion torque calculated across subjects was 18.0 ± 3.2 Nm, and the range over which subjects varied their torque was 4.9 ± 1.9 Nm. Based on the MVC values for plantarflexion torque (10 Nm) reported by Kuchinad et al. (2004), the plantarflexion torque produced in the current study was equivalent to 12–18% MVC. Seven subjects performed both the voluntary sway and variable force tasks on the same day. Analysis of the surface EMG in these subjects revealed a trend toward higher EMG during the voluntary sway task than during the variable force task (P = 0.06). The surface EMG across all subjects and all tasks (Table 3) suggests that the force produced during the voluntary sway task was somewhat greater than the other tasks.
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DISCUSSION |
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Removal of vision does not change the extent of common drive
Because the control of standing posture requires the integration of visual, vestibular, and proprioceptive inputs, it was anticipated that the removal of vision would result in an increase in common drive between bilateral soleus motor units. This would occur either as a result of an increase on the reliance of the other sources of sensory input in the absence of vision or due to the increase in sway when the eyes are closed (Lucy and Hayes 1985).
There was no significant difference in common drive between eyes open and eyes closed, suggesting that vision has little impact on the common modulation of bilateral soleus motoneurones during postural tasks. However, there was a significant order effect, such that the extent of common drive was lower in the task that was performed second. This may have been the result of muscle fatigue that developed over the course of the postural tasks as suggested by the increase in the RMS amplitude of the soleus surface EMG. A pattern of increasing surface EMG has been found in submaximal muscle fatigue protocols (Bigland-Ritchie et al. 1986). Oda and Moritani (1995) showed that the correlation of motor activity between bilateral biceps brachii muscles decreased over the course of a fatiguing task. If a time of 10 min is estimated as a minimum preparation time for having the subject standing while the motor unit recordings are checked for quality and readjusted as necessary, and add another 10 min for data collection, subjects would have been producing a plantarflexion contraction of 25% MVC (Mochizuki et al. 2006) for 
20 min. Walton et al. (2002) utilized a protocol to induce fatigue of the plantarflexors involving an intermittent isometric contraction of 30% MVC which resulted in a time to fatigue of 17.6 min for sedentary individuals. Cresswell and Loscher (2000) performed a sustained 30% MVC and reported an endurance time of 7.5 min. The contraction level and time to fatigue are within the range reported in the present study.
Another possible explanation for the order effect observed in experiment 1 is that over time, a change in postural strategy occurred. One possibility may have been to change the postural strategy from one that was based primarily on ankle control to one that relied on both ankle and hip musculature. We did not record kinematics or EMG from the hip muscles that might have shed light on this possibility. Another strategy may have been to use increasing amounts of co-contraction about the ankle to maintain postural stability. The RMS amplitude of the surface EMG of the tibialis anterior and the soleus muscles displayed in Fig. 3 does not support this explanation.
Effect of proprioception on common modulation of bilateral motor unit firing rates
Vibrating one Achilles tendon during standing posture resulted in a decrease in the extent to which bilateral soleus motor units co-modulate their discharge rates. Tendon vibration stimulates muscle spindle Ia afferents (Roll et al. 1989), resulting in a decrease in the mean ISI and CV of ISI of the motor units in the vibrated leg. There are conflicting reports in the literature on the contribution of sensory feedback to common drive. In orbicularis oris muscle, Kamen and De Luca (1992) found that common drive was strong, even though that muscle lacks muscle spindles. On the other hand, Garland and Miles (1997) found that common drive was decreased in flexor digitorum profundus when the muscle tendon was disengaged, thereby impairing the normal proprioceptive feedback to the motoneurone pool. Proprioception appears to contribute to common drive in hand muscles and postural muscles that rely on proprioception for skilled activity.
Vibration of the triceps surae muscles in standing, when administered bilaterally, has resulted in posterior shifts of the COP ranging from 0.3 cm (Kavounoudias et al. 1999) to 1.0 cm (Hatzitaki et al. 2004). In the present study, unilateral vibration of the Achilles tendon resulted in a posterior excursion of the COP of 1.0 cm in the nonvibrated leg and 0.3 cm in the vibrated leg. This finding is consistent with Polonyova and Hlavacka (2001), who demonstrated that unilateral vibration of gastrocnemius muscle resulted in a backward and lateral body tilt away from the stimulated leg. In the present study, this shift in body tilt was expressed as a larger posterior shift of the COP of the nonvibrated leg (i.e., away from the stimulated leg). The results of experiment 3 indicated that common drive was lowest when the COP was most posterior and higher when swaying anteriorly (Fig. 4). Therefore vibration not only disrupts natural proprioceptive inputs but also moves the COP posteriorly where the common drive is low. The effect of vibration on common drive in the present study is consistent with the hypothesis that peripheral inputs are potent contributors to the common drive between soleus motoneurones during postural tasks.
The observation that common drive depends on the position of AP sway is also consistent with a role for proprioception in common drive. When the AP sway is anterior, the motor unit firing rate is higher, and conversely, when the AP sway is posterior, the motor unit firing rate is slower. The common drive is related to the sway, rather than the firing rate, because in the variable force task the firing rate is highest in phase 2 and lowest in phase 4, yet the common drive coefficient does not change among phases in the isometric task. We also showed previously that the common drive correlations were not associated with the firing rate of the motor unit in postural and voluntary isometric tasks (Mochizuki et al. 2006). There are several proprioceptive inputs that may change depending on the phase of AP sway. There could be more Ia afferent input during anterior postural sway. Recent work by Loram et al. (2004, 2005) indicated that the triceps surae muscle group paradoxically shortens as the standing individual leans forward, in association with "microfalls. " Even though the muscle is contracting concentrically during anterior sway, the abrupt changes in muscle length (microfalls) may result in rich proprioceptive activation of Ia afferents.
Alexander and Harrison (2002) showed that bilateral reflex control, likely via crossed monosynaptic reflex pathways, existed in the trapezius muscle. The authors suggested that these pathways may exist as a result of primary afferents that cross the midline to synapse with the contralateral motoneuron pool (Ritz et al. 1991), dendrites of motoneurons crossing the midline and synapsing with afferents on the contralateral side (Rose and Richmond 1981) or motoneurons that exit the spinal cord ipsilaterally that are located contralaterally (Abrahams and Keane 1984).
Cutaneous afferents may also contribute to common modulation in motor unit discharge. In cats, cutaneous afferents have been shown to exert bilateral effects on trunk muscle motoneurones (Wada et al. 1999). In human postural control studies, the removal of cutaneous information by anesthesia applied to the feet resulted in modest increases in measures of COP (Fitzpatrick et al. 1994). When cutaneous and mechanoreceptor information is intact, the distribution of the receptive fields and directional sensitivity of the receptors modulated according to the position and direction of the stimulus (Kennedy and Inglis 2002). Given the phasic nature of postural sway, it is conceivable that proprioceptive inputs from muscle spindle and cutaneous afferents to soleus motoneurones modulate according to the postural task. Indeed, Aniss and colleagues (1990) showed that inputs from muscle spindles, Golgi tendon organs, and cutaneous afferents all contributed to postural muscle activation during stance. These inputs were later thought to impart their effects on the postural musculature through an ankle joint proprioceptive reflex that remained intact even in the absence of vestibular and visual inputs (Fitzpatrick et al. 1992).
Common modulation of motor unit discharge during voluntary contractions
Common drive was greater in the voluntary sway task than in the isometric variable force task, but in both voluntary tasks, common drive was lower than during quiet stance. Even though the same motor units were not recorded in both the voluntary sway and variable force tasks, we were recording from low-force motor units in both tasks with the motor units discharging near the minimal firing rate (Bellemare et al. 1983). Furthermore, the discharge characteristics were not markedly different from motor units in experiment 1 (for voluntary sway) and experiment 2 (for variable force) in which the motor unit pairs were matched between tasks. Thus the common drive to soleus motor units during volitional force production was lower than that observed during different conditions of quiet stance. Although speculative, we suggest that an explanation for this observation is based on differences between task requirements. Quiet standing may be a task that requires less higher order processing (i.e., cortical activity) than swaying voluntarily, thus there may be a stronger reliance on subcortical inputs to the common drive to bilateral motor-unit pairs. The voluntary sway task may shift the balance of descending inputs, whereby there is more corticospinal input than in natural sway. The noncortical descending inputs (i.e., vestibulo- or reticulospinal) may be more important in postural control than cortical inputs. Further work is required to assess the subcortical contributions of common drive to soleus motoneurone pools directly during balance control.
Potential sources of subcortical bilateral inputs should be considered. Carr and colleagues (1994) speculated that bilateral bulbospinal projections contributed to correlated multi-unit EMG in the trunk and face. Reticulospinal activation via the acoustic startle reflex has been shown to produce correlated bilateral activation and modulation of deltoid and biceps brachii EMG in humans (Grosse and Brown 2003), whereas bilateral projections from the lateral vestibular nuclei to soleus motoneurons have been observed in the cat (Shinoda et al. 1986). Furthermore, unilateral caloric stimulation of the vestibular apparatus in humans was shown to produce bilateral triceps surae EMG responses (Mano et al. 1976). These descending bilateral projections may influence the bilateral common modulations in motor unit discharge in the soleus muscle. On the other hand, corticospinal projections seem to have limited influence, given our previous findings that the incidence of motor unit synchrony in bilateral soleus motor unit pairs is low (Mochizuki et al. 2005).
Conclusions
These findings illustrate that common modulation of motor unit discharge in bilateral motor unit pairs is task dependent. These results implicate proprioceptive and subcortical inputs in providing common inputs to the motoneurone pools of the soleus muscles bilaterally during postural tasks.
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GRANTS |
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Address for reprint requests and other correspondence: S. Jayne Garland, School of Physical Therapy, Rm 1588, Elborn College, University of Western Ontario, London, ON N6G 1H1, Canada (E-mail: jgarland{at}uwo.ca)
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) and eyes-closed (
) tasks. Regardless of the task, the task performed 2nd displayed significantly lower common drive. *, significant difference from 1st task, P = 0.007.
) and tibialis anterior (
) surface EMG measured quarterly over both tasks. Data are presented to illustrate the order effect; hence in the 1st and 2nd tasks, data are combined for eyes-open and –closed tasks. The values represent the average of the right and left muscles and are expressed as means ± SE.
). +, significantly different from phases 1–3 (quiet stance); 
, significantly different from phase 1 (quiet stance); *, significantly different from phases 1 and 2 (voluntary sway). Data presented as means ± SE.