OPTIMAL CONTROL OF the quadriceps is essential for. Motor Unit Synchronization of the Vasti Muscles in Closed and Open Chain Tasks

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1 716 Motor Unit Synchronization of the Vasti Muscles in Closed and Open Chain Tasks Rebecca Mellor, Mphty, Paul W. Hodges, PhD ABSTRACT. Mellor R, Hodges PW. Motor unit synchronization of the vasti muscles in closed and open chain tasks. Arch Phys Med Rehabil 2005;86: Objectives: To investigate motor unit synchronization between medial and lateral vasti and whether such synchronization differs in closed and open chain tasks. Design: Electromyographic recordings of single motor unit action potentials were made from the vastus medialis obliquus (VMO) and multiunit recordings from vastus lateralis during isometric contractions at 30 of knee flexion in closed and open chain conditions. Setting: Laboratory. Participants: Five volunteers with no history of knee pain (age, y). Interventions: Not applicable. Main Outcome Measure: The degree of synchronization between motor unit firing was evaluated by identifying peaks in the electromyographic averages of the vastus lateralis, triggered from motor unit action potentials in the VMO, and the proportion of power in the power spectral density of the triggered average at the firing frequency of the reference motor unit. The proportion of cases in which there was significant power and peaks in the triggered averages was calculated. Results: The proportion of trials with peaks in the triggered averages of the vastus lateralis electromyographic activity was greater than 61.5% in all tasks, and there was a significantly greater proportion of cases where power in the spectrum was greater than 7.5% (P.01) for the closed chain condition. Conclusions: There was a high proportion of synchronized motor units between the 2 muscles during isometric contractions, with evidence for greater common drive between the VMO and vastus lateralis in closed chain tasks. This has implications for rehabilitation because it suggests that closed chain tasks may generate better coordination between the vasti muscles. Key Words: Exercise therapy; Motor activity; Muscles; Rehabilitation by American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation OPTIMAL CONTROL OF the quadriceps is essential for normal function of the knee. In particular, coordination of the medial and lateral forces of the vasti is critical for control of alignment and stability of the patellofemoral joint. One strategy to simplify this control may be for the central nervous system (CNS) to provide a degree of common input to the vasti From the Division of Physiotherapy, University of Queensland, Brisbane, Australia. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit on the author(s) or on any organization with which the author(s) is/are associated. Reprint requests to Paul W. Hodges, PhD, Div of Physiotherapy, University of Queensland, Brisbane, Queensland 4072, Australia. p.hodges@shrs.uq.edu.au /05/ $30.00/0 doi: /j.apmr muscles. Recently, we showed that synchronous firing is common between motor units in the vastus medialis obliquus (VMO) and vastus lateralis muscle components of the quadriceps group. 1 However, how this degree of synchronization differs between functional contexts is not known. Motor unit synchronization is defined as the increased tendency for motor units to discharge within a few milliseconds of each other more often than would be expected because of chance and can be quantified by techniques such as crosscorrelation of the individual discharge times of motor unit pairs. 2,3 The degree of motor unit synchronization can provide some indication about the organization of synaptic input to motoneurons during voluntary motor tasks. 4 Differences in muscle function (eg, prehension and postural control) are reflected by different neural control mechanisms, and it appears from most studies of motor unit synchronization that it is greatest within muscles involved in postural control and stability. For example, Marsden et al 5 showed coherence between motor unit pairs located in the paraspinal muscles ipsilaterally and bilaterally at low frequencies but not bilaterally between the interossei of the hand. The lack of common drive between the right and left interossei muscles could allow for skilled independent control of the 2 hands, whereas its presence in the paraspinals may allow the axial skeleton to act more as a functional unit during postural control. Several studies have found that the degree of synchronization between muscles may be task specific. Semmler et al, 6 using cross-correlation and coherence analysis of single motor unit pairs, found differences in the degree of common inputs received by the motoneurons between postural, shortening, and lengthening contractions of a hand muscle. Semmler and Nordstrom 7 also used cross-correlation of motor unit pairs in the first dorsal interosseous (FDI) muscle of weightlifters, musicians, and untrained subjects to examine the effect of habitual physical activity on motor unit synchronization. During isometric abduction of the FDI, they found greatest strength of synchronization in the muscles of the weightlifters and least in the musicians, showing how different skilled activities require different degrees of common input. Bremner et al 8 also found that the degree of synchronization between hand muscles depends on the task performed, reflecting the different levels of separate control necessary for prehension. By using crosscorrelation analysis, Gibbs et al 9 found greatest synchronization between the discharge of motoneuron pools innervating muscle pairs in the lower limb that were anatomically and functionally related, especially during the postural tasks of balancing and standing. Halliday et al, 10 by using both timeand frequency-domain analysis of the coupling between the electromyographic activity from pairs of leg muscles, found that firing of motor units in different muscles is only weakly coupled during walking, which may provide a basis for the great adaptability of the human gait pattern. These data suggest that the CNS coordinates motor unit activity differently during postural and movement tasks. Because the quadriceps contract in a weight bearing or closed chain situation during stance and balance, one functional consideration is whether motor unit synchronization

2 GREATER VASTI COMMON DRIVE IN CLOSED CHAIN TASKS, Mellor 717 Fig 1. Experimental setup. (A) Electrode placement, denoting fine-wire electrodes within the muscles and the monopolar needle electrode. (B) Subject position for open chain condition. (C) Subject position for closed chain condition. Abbreviations: VLd, distal vastus lateralis placement; VLp, proximal vastus lateralis placement. differs between open chain tasks (non weight bearing, in which the distal end of the extremity is free to move) and closed chain tasks (weight bearing, involving 1 joint, in which the distal end extremity is fixed). 11 Both closed and open chain exercises are also commonly prescribed for the quadriceps in rehabilitation of several knee conditions. Thus, the aim of this study was to determine whether there are differences in the degree of motor unit synchronization between the VMO and lateral vasti muscles in closed and open chain tasks. In prescribing appropriate exercise therapy, it is important to understand the mechanisms of motor control and the strategies used by the CNS to control the patellofemoral and tibiofemoral joints. METHODS Participants Five volunteers (3 men, 2 women; mean age standard deviation [SD], y) participated in the study. Subjects were included if they had no history of knee pain or pain elsewhere in the lower limb and were excluded if they had any neurologic disorder. The study was approved by the Institutional Medical Research Ethics Committee and all procedures were conducted in accord with the Declaration of Helsinki. Electromyographic Activity Electromyographic recordings were made from single motor units in the VMO by using a monopolar needle electrode a inserted within the muscle belly, approximately 4mm superior and 3mm medial to the superomedial patella border, and referred to a surface electrode b (20-mm Ag/AgCl disk) placed 10mm lateral to the needle insertion point (fig 1A). Multiunit recordings were made from the vastus lateralis using nonselective fine-wire intramuscular electrodes fabricated from 75 m Teflon-coated stainless steel wire c with 15mm of Teflon removed to record from a large population of motor units. A single wire was inserted into a hypodermic needle (0.5 25mm) and its tip bent back 3mm to form a hook. Once the electrodes were inserted into standardized sites (distal vastus lateralis 100mm superior and 70mm lateral to the superior border of the patella, angled 15 to a line connecting the superior pole of the patella and the anterior superior iliac spine; proximal vastus lateralis 100mm more proximally along the muscle belly), the needle was withdrawn, leaving the wire in place. These intramuscular electrodes were each referred to a surface electrode, and a ground electrode was placed over the anterior tibia about 100mm distal to the inferior pole of the patella (see fig 1A). A pair of surface electrodes was also placed proximal and distal to the monopolar needle, in parallel with the muscle fibers of the VMO, at an angle of 55 to the longitudinal axis of the femur. 12 This was done to record the characteristic shape of the motor unit action potential (MUAP) by generating an average of the surface electromyographic recording, triggered from the firing of the reference motor unit in the VMO. This would ensure that recordings from a motor unit were not

3 718 GREATER VASTI COMMON DRIVE IN CLOSED CHAIN TASKS, Mellor Fig 2. (A) Raw data from a representative subject obtained from recordings in the closed chain condition. Inset depicts the morphology of the reference MUAP recorded from the monopolar needle in the VMO. (B) Average of the rectified proximal vastus lateralis electromyographic data, triggered from the reference VMO motor unit, in the closed chain condition. (C) Example of PSD, obtained from an average of vastus lateralis electromyographic data, triggered from the VMO reference motor unit. The power in the spectrum at the frequency of firing of the VMO reference unit (indicated by the dotted line) is expressed as a percentage of the total power in the spectrum. Abbreviations: VLd, vastus lateralis, distal recording; VLp, vastus lateralis, proximal recording; VMOmn, vastus medialis obliquus, monopolar needle recording. duplicated between trials. Electromyographic data were preamplified 1000 times close to the body, amplified another 2 times, band-pass filtered between 20Hz and 2kHz, and sampled at 5kHz by using a Power 1401 d and Spike2 software. e Procedure Subjects sat with their trunk supported and one knee flexed at 30 from full extension over a stable frame. In the open chain condition, a strap was fixed around the ankle so that knee extension could be performed isometrically against resistance (fig 1B). In the simulated closed chain condition, a strap was placed around the foot so the subject could push down through the leg, extending the knee against the fixed resistance (fig 1C). The monopolar needle was inserted into the VMO and positioned within the muscle to optimize the recording of a single motor unit. The subject gently contracted the quadriceps isometrically for 200 seconds, while maintaining the firing of the target motor unit at a steady rate throughout, using auditory and visual feedback. The position of the needle was adjusted between trials to record from individual motor units. Our aim was to record from 10 motor units in both the open chain and closed chain conditions for each subject. Data Analysis MUAPs from the VMO recording were identified by using a spike-sorting algorithm e that uses waveform shape to discriminate action potentials (fig 2A). Because accurate discrimination is difficult to achieve unless action potentials have clearly different shapes and there is a high signal to noise ratio, all data were inspected offline to ensure that the triggers coincided with distinct motor units. Once sorted, the mode of the firing rate was identified from the inverse of the interval histogram. The unit was then used to trigger averages of the rectified and unrectified vastus lateralis electromyographic recordings. Any motor units in the vastus lateralis that fire together with the reference motor unit in the VMO should appear as a peak in the average (fig 2B). A peak was defined as present when the electromyographic amplitude was greater than 3 SDs from the mean baseline electromyographic amplitude of the triggered average. 13 When a peak was present, we measured the peak width (in milliseconds) and the peak amplitude (in terms of the number of SDs from the mean baseline electromyographic activity). A narrower peak width and greater amplitude are likely to indicate less variability in coupling between the firing of motor units in each muscle, and thus closer synchronization between firing of units in the 2 muscles. However, it is important to recognize that these parameters will also be affected by the size of the MUAP. For the averages of the unrectified electromyographic activity, only the proportion of trials with a peak was calculated, not the peak characteristics. Data were also evaluated in the frequency domain, by calculating the power spectral density (PSD) of the rectified vastus lateralis averages (fig 2C). We used this analysis to estimate the

4 GREATER VASTI COMMON DRIVE IN CLOSED CHAIN TASKS, Mellor 719 Table 1: Percentage of Trials (motor units) in Which Peaks Were Identified in the Electromyographic Averages, and the Percentage of Trials with Greater Than 7.5% of the Energy in the Power Spectrum at the Frequency of Firing of the Motor Unit Chain-Task Muscle Unrectified Peak (%) Rectified PSD 7.5% Closed Distal vastus lateralis Proximal vastus lateralis Open Distal vastus lateralis Proximal vastus lateralis degree to which vastus lateralis electromyographic activity was modulated at the frequency of firing of the VMO motor unit. Because the PSD was calculated from the average triggered from the firing of the VMO motor unit, this measure reflects the degree of modulation of vastus lateralis activity that is coupled to that of the VMO, and not the general firing of the vastus lateralis units. Thus, the measure provides an indication of the general common drive to the motor unit pools. The power in the spectrum at the frequency of firing of the VMO reference unit was calculated as a proportion of the total power. We calculated the proportion of trials in which the power in the spectrum at the firing frequency of the reference motor unit was greater than 7.5%. That percentage was chosen because our previous study results indicated that power above that level does not occur between muscles in different parts of the body in which synchronization would not be expected to occur. Statistical Analysis Statistical analysis was performed by using the software package Statistica. f Data were analyzed in terms of the prevalence of peaks in the rectified and unrectified averages, the peak characteristics (width, amplitude) of the rectified averages, the power in the PSD at the instantaneous frequency of the reference unit, and also the proportion of recordings with power in the spectrum greater than 7.5% of the total power. The parameters were compared by using a factorial analysis of variance, and the chi-square test was used to determine differences between the proportion of cases with significant power. Alpha level was set at.05. RESULTS When subjects extended their knee against resistance in both the open and closed chain tasks there was a high degree of synchronization between motor unit firing in the medial and lateral vasti muscles. Table 1 shows the percentage of cases in which peaks were seen in the unrectified and rectified vastus lateralis averages, and the percentage of cases in which the power in the spectrum at the frequency of firing of the reference VMO motor unit was greater than 7.5%. Spike-Triggered Averages There was no significant difference between the open and closed chain tasks in terms of the characteristics of the peaks in the rectified averages. The mean width of the peaks in the rectified averages for distal and proximal vastus lateralis was ms and ms in the closed chain condition and ms and ms in the open chain condition. The mean amplitudes (number of SDs above the mean baseline electromyographic activity) of the peaks in the rectified averages for distal and proximal vastus lateralis were and for the closed chain condition and and in the open chain condition. The proportion of peak amplitudes greater than 3 SDs above the mean in the closed chain condition for both distal and proximal vastus lateralis was.71 and.74, respectively, and in the open chain condition it was.74 and.72. PSD Analysis Although there was no difference in the number of trials with a peak in the rectified and unrectified triggered averages between tasks, there was a significantly greater number of trials in the closed chain condition that had a large percentage of power at the frequency of firing of the reference motor unit compared with the open chain condition (P.01) (fig 3). The lack of a difference in the characteristics of the peaks in the triggered averages between tasks, but greater proportion of units with greater power at the frequency of firing of the VMO motor unit, suggests a greater degree of generalized common input to the 2 motoneuron pools, without specifically leading to near-synchronous firing. The mean power in the spectrum at the frequency of firing of the reference motor unit, expressed as a percentage of total power, was 10%; it was 9% for distal and proximal vastus lateralis in the closed chain condition and 7% and 6% in the open chain condition. DISCUSSION Our findings in this study indicate that a high degree of synchronization exists between motor units in the medial and lateral vasti muscles during isometric knee extension efforts. Furthermore, the data indicate that the degree of common drive, although not leading to significantly greater near-simul- Fig 3. Percentage of trials with power in the PSD at the firing frequency of the reference motor unit that is greater than 7.5% of total power, indicating a significantly greater number of trials (*P.01) for the closed chain condition.

5 720 GREATER VASTI COMMON DRIVE IN CLOSED CHAIN TASKS, Mellor taneous firing, may be greater in closed chain than in open chain tasks. Methodologic Considerations Commonly, cross-correlation analyses are used to quantify motor unit synchronization; they involve recordings with 2 intramuscular electrodes to sample from a discrete pair of motor units. This is difficult to repeat between trials, and a large sample of motor unit pairs is usually needed to give a reliable estimate of overall motor unit synchrony because strength of synchronization varies for different motor unit pairs in the same muscle. 2,4 In this study, we compared the relationship of the firing of 1 motor unit in the reference muscle to a large population of motor units in the second muscle, thereby increasing the chance of detection of the coupled firing of motor units in the 2 muscles. However, this technique requires further consideration. First, the amplitude and duration of the peaks in the averages are influenced by several factors that must be considered when interpreting results, such as variation in latencies, size and duration of the action potentials, proximity to the recording electrode, and level of background electromyographic noise. 13 However, a major factor affecting the width of the peak is the degree of variation in relative latency of the firing of the coupled motor units. That is, greater intertrial variation will tend to spread the peak. Second, recordings made with the nonselective electrodes in the vastus lateralis could be influenced by cross talk from the VMO, in which case the peak could simply indicate a triggered average of the reference motor unit in the vastus lateralis recording. To ensure that the peaks we observed in the triggered electromyographic averages were not because of cross talk between muscles, we did 2 additional trials in a previous study. 1 In the first, fine-wire recordings were made from the distal portion of the adjacent semitendinosus hamstring muscle. Its proximity to the VMO is similar to that of vastus lateralis; therefore, it is likely to have a similar volume conduction of cross talk. However, because it is an antagonist muscle in this task, it is unlikely to have synchronous activity. Identical analysis was performed by using the VMO monopolar needle recordings as the reference motor unit. No peaks were seen in any of the triggered averages of the hamstring muscle recordings, indicating that there was no cross talk. 1 In the second study, 14 coherence analysis between the VMO and vastus lateralis recordings did not indicate broad spectrum coherence, which would be expected if there was cross talk. An additional consideration is that the differences in the measures of the peak characteristics between the 2 conditions did not reach statistical significance because of the small number of subjects and the degree of variability between subjects and between motor units within a subject. This is consistent with a previous study 15 that reported large differences in motor unit synchrony between subjects. However, the data from this study indicate differences in proportion of power in the PSD despite the small subject number. The simulated weight-bearing position used in this study may also have inherent problems. The position of the subject was not changed so that hip and knee position between tasks was standardized, and movement of the monopolar needle within the muscle during recordings was avoided. In addition, it would be more difficult to control the firing of a single motor unit in a standing position because shifts in center of gravity would alter levels of muscle activity. Although the simulated action fulfilled the criteria of a closed chain task, full weight bearing may generate more functional patterns of muscle activation and might give a more accurate representation of the different responses of the CNS to the different tasks. A further factor to consider is the generalizability of these results to differing knee angles. Other studies have found differences in electromyographic activity of the quadriceps at different knee angles, 16,17 although there are discrepancies between many of the findings. However, it is not possible to relate these gross electromyographic findings to measures of synchronization. Preliminary studies (R Mellor and PW Hodges, unpublished data, 2003) suggest that there is no difference in the degree of motor unit synchronization at 0, 30, and 60 of knee flexion, at least for low effort contractions. However, this may differ with increasing levels of muscle activation. Functional Significance of Synchronization Motor unit synchronization has been investigated in different muscles by using either single MUAP (spike) trains 4,18 or multiunit recordings. 19 It has been argued that functionally related muscles may be activated according to organized, fixed patterns, 20 which are important for stabilization, balance, and movement control. As mentioned, the varying degrees of synchronization between different muscles may reflect how neural control differs between functionally distinct activities. For instance, studies 5,9 have indicated that motor unit synchronization is greatest between muscles involved in postural control and stability. One mechanism for this, in which presynaptic axons branch to innervate several motoneurons both within and between muscles, may help to simplify motor control by contributing to the formation of functional muscle synergies. Notably, Gibbs et al 9 argued that synchrony is dependent on functional, in addition to anatomic, relationships between the motoneuron pools, and that the underlying motor command is directed toward producing patterns of movement, rather than the control of individual muscles or motoneurons. The greater degree of common drive to the medial and lateral vasti during closed chain tasks shown by the PSD data in this study concurs with these previous findings. The vasti are situated in the same anatomic compartment, contributing to the same joint action, and because most postural, balancing, and stability functions of the quadriceps occur in the weight bearing or closed chain situation, the greater degree of synchronization was not surprising. Closed Chain Exercises in Rehabilitation Closed chain exercises are used extensively in rehabilitation for a variety of knee conditions and are considered preferable to open chain exercises for several reasons. Because they involve the hip, knee, and ankle, general coordination and strength are improved, which contributes to more complete restoration of function. Numerous studies have used kinematic, kinetic, and electromyographic data to investigate knee forces and muscle activity during open and closed kinetic chain exercises and have found significant differences. Closed chain exercises produce greater quadriceps and hamstring cocontraction and greater magnitudes of compressive forces across the knee, although the magnitude of the cocontraction activity depends on trunk position relative to the knee, contraction force, knee joint angle, 21 and type of exercise. For example, Escamilla et al 22 found that open chain exercise produced greater rectus femoris activity, whereas closed chain exercise produced greater vasti muscle activity. Because closed kinetic chain exercises largely affect forces at the tibiofemoral and patellofemoral joints, any incoordination in the contraction of the vasti muscles may increase

6 GREATER VASTI COMMON DRIVE IN CLOSED CHAIN TASKS, Mellor 721 patellofemoral joint forces, which could eventually lead to pain. Patellofemoral pain is a common condition, and several factors contribute to its development. One is abnormal lateral tracking of the patella, and the concept that an imbalance in the medial and lateral forces on the patella may be because of altered neural drive is becoming increasingly accepted. 23 There remain discrepancies in the literature, however, several authors 24,25 have identified a delay in onset of electromyographic activity of the VMO in voluntary tasks in people with patellofemoral pain. In addition, preliminary data (R Mellor and PW Hodges, unpublished data, 2004) indicates that the proportion of synchronized units between medial and lateral vasti muscles is reduced in people with patellofemoral pain, compared with that in people without knee pain. Stensdotter et al 26 have shown that recruitment patterns alter in the different heads of the quadriceps muscles between closed and open chain tasks. They found that the onset of surface electromyographic activity of the medial and lateral vasti was more simultaneous in the closed chain task. Therefore, it is logical that the use of closed chain exercises, which produce more simultaneous activation of the different muscles comprising the quadriceps, is encouraged in rehabilitation of this condition. However, correspondence in the time of initiation of electromyographic activity is not the same as motor unit synchronization. Evidence for synchronization is important as an indicator of common drive to the motoneuron pools, and the distribution of input from this common drive can help balance and coordinate the activity of these 2 muscles. CONCLUSIONS This study has shown a greater degree of coupling between the medial and lateral vasti muscles during closed chain tasks. Because this may contribute to greater coordination between the muscles, it provides another logical rationale for using this form of exercise in the rehabilitation of patellofemoral pain. References 1. Mellor R, Hodges P. Relationship between motor unit activity of medial and lateral vasti muscles. In: Lord SR, Menz HB, editors. Proceedings of the International Society for Postural and Gait Research XVIth Conference; 2003 Mar 23-27; Sydney (Aust). p Semmler JG, Nordstrom MA. A comparison of cross-correlation and surface EMG techniques used to quantify motor unit synchronization in humans. J Neurosci Methods 1999;90: Sears TA, Stagg D. Short-term synchronization of intercostal motoneurone activity. J Physiol 1976;263: Datta AK, Stephens JA. Synchronization of motor unit activity during voluntary contraction in man. J Physiol 1990;422: Marsden JF, Farmer SF, Halliday DM, Rosenberg JR, Brown P. The unilateral and bilateral control of motor unit pairs in the first dorsal interosseous and paraspinal muscles in man. J Physiol 1999;521(Pt 2): Semmler JG, Kornatz KW, Dinenno DV, Zhou S, Enoka RM. Motor unit synchronisation is enhanced during slow lengthening contractions of a hand muscle. J Physiol 2002;545(Pt 2): Semmler JG, Nordstrom MA. Motor unit discharge and force tremor in skill- and strength-trained individuals. Exp Brain Res 1998;119: Bremner FD, Baker JR, Stephens JA. Effect of task on the degree of synchronization of intrinsic hand muscle motor units in man. J Neurophysiol 1991;66: Gibbs J, Harrison LM, Stephens JA. Organization of inputs to motoneurone pools in man. J Physiol 1995;485(Pt 1): Halliday DM, Conway BA, Christensen LO, Hansen NL, Petersen NP, Nielsen JB. Functional coupling of motor units is modulated during walking in human subjects. J Neurophysiol 2003;89: Brindle TJ, Nyland J, Ford K, Coppola A, Shapiro R. Electromyographic comparison of standard and modified closed-chain isometric knee extension exercises. J Strength Cond Res 2002;16: Gilleard W, McConnell J, Parsons D. The effect of patellar taping on the onset of vastus medialis obliquus and vastus lateralis muscle activity in persons with patellofemoral pain. Phys Ther 1998;78: Fortier PA. Use of spike triggered averaging of muscle activity to quantify inputs to motoneuron pools. J Neurophysiol 1994;72: Hansen NL, Hansen S, Christensen LO, Petersen NT, Nielsen JB. Synchronization of lower limb motor unit activity during walking in human subjects. J Neurophysiol 2001;86: Bremner FD, Baker JR, Stephens JA. Correlation between the discharges of motor units recorded from the same and from different finger muscles in man. J Physiol 1991;432: Becker R, Awiszus F. Physiological alterations of maximal voluntary quadriceps activation by changes of knee joint angle. Muscle Nerve 2001;24: Brownstein BA, Lamb RL, Mangine RE. Quadriceps torque and integrated electromyography. J Orthop Sports Phys Ther 1985;6: Farmer SF, Swash M, Ingram DA, Stephens JA. Changes in motor unit synchronization following central nervous lesions in man. J Physiol 1993;463: Carr LJ, Harrison LM, Stephens JA. Evidence for bilateral innervation of certain homologous motoneurone pools in man. J Physiol 1994;475: Nashner LM. Fixed patterns of rapid postural responses among leg muscles during stance. Exp Brain Res 1977;30: Wilk KE, Escamilla RF, Fleisig GS, Barrentine SW, Andrews JR, Boyd ML. A comparison of tibiofemoral joint forces and electromyographic activity during open and closed kinetic chain exercises. Am J Sports Med 1996;24: Escamilla RF, Fleisig GS, Zheng N, Barrentine SW, Wilk KE, Andrews JR. Biomechanics of the knee during closed kinetic chain and open kinetic chain exercises. Med Sci Sports Exerc 1998;30: Grabiner MD, Koh TJ, Draganich LF. Neuromechanics of the patellofemoral joint. Med Sci Sports Exerc 1994;26: Cowan SM, Bennell KL, Hodges PW, Crossley KM, McConnell J. Delayed onset of electromyographic activity of vastus medialis obliquus relative to vastus lateralis in subjects with patellofemoral pain syndrome. Arch Phys Med Rehabil 2001;82: Voight ML, Weider DL. Comparative reflex response times of vastus medialis obliquus and vastus lateralis in normal subjects and subjects with extensor mechanism dysfunction. Am J Sports Med 1991;19: Stensdotter AK, Hodges PW, Mellor R, Sundelin G, Hager-Ross C. Quadriceps activation in closed and in open kinetic chain exercise. Med Sci Sports Exerc 2003;35: Suppliers a. TECA, Oxford Instruments, Manor Way, Old Woking, Surrey, GU22 9JU, UK. b. Grass Telefactor; Central Neurophysiology Supplies, Unit 10, 116 McCredie Rd, Guildford, NSW 2161, Australia. c. A-M Systems Inc, PO Box 850, Carlsborg, WA d. Neurolog, 37 Hydeway, Welwyn Garden City, Hertfordshire, AL7 3BE, England. e. Cambridge Electronic Design, Science Park, Milton Rd, Cambridge CB4 0FE, England. f. Statistica version 5; Statsoft Inc, 2300 E 14th St, Tulsa, OK

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