Summary. Motor-unit activity in m. biceps brachii, m. brachialis and an. brachioradialis during isometric con- tractions has been compared with motor-unit activity.
Exp Brain Res (1990) 81:567-572
9 Springer-Verlag1990
Differences in coordination of elbow flexor muscles in force tasks and in movement tasks A.A.M. Tax, J.J. Denier van der Gon, and C.J. Erkelens Department of Medical and Physiological Physics, University of Utrecht, P.O. Box 80000, 3508 TA Utrecht, The Netherlands Received September 6, 1989/Accepted February 22, 1990
Summary. Motor-unit activity in m. biceps brachii, m. brachialis and an. brachioradialis during isometric contractions has been compared with motor-unit activity during slow voluntary (extension and flexion) movements made against external loads. During these slow movements the recruitment threshold of m. biceps motor units is considerably lower than it is during isometric contractions but the recruitment threshold of both m. brachialis and m. brachioradialis motor units is considerably higher. For all three elbow flexor muscles the motor-unit firing frequency seems to depend on the direction of movement: the firing frequency is higher during flexion movements (3 deg/s) and lower during extension movements ( - 3 deg/s) than during isometric contractions. The relative contribution of the biceps to the total exerted flexion torque during slow voluntary movements is estimated to increase from 36% to about 48% and that of the brachialis/ brachioradialis is estimated to decrease from 57% to about 45% compared to the relative contribution o f these muscles during isometric contractions. This difference in the relative contribution of the three major elbow flexor muscles is shown to be caused by differences in the central activation in force tasks and movement tasks. Key words: M o t o r unit - Recruitment threshold - Synergism - Movement control - Muscle coordination Human
Introduction There is increasing evidence that the coordination of (synergistic) muscles is task-dependent. For instance, the concept of task groups (Loeb 1985) as a functional compartmentalisation of the motor apparatus has been demonstrated in the biarticular sartorius muscle in the cat (Hoffer et al. 1980 and 1987) during locomotion. An additional study in the cat indicates that for rapid ankle Offprint requests to- A.A.M. Tax (address see above)
extension gastrocnemius motor units are recruited whereas for the phase of ankle extension during stepping soleus motor units are recruited (Smith et al. 1980). Taskdependent synergism has also been shown in humans. In the m. biceps brachii different motor-unit populations are activated for isometric force tasks in flexion and supination direction (ter Haar Romeny et al. 1982; v. Zuylen et al. 1988). Furthermore, the contribution of the biceps to the total exerted flexion torque at the wrist is shown to be higher in slow isotonic movements than in isometric contractions (Tax et al. 1989). A preliminary investigation of a few motor units of the m. brachialis suggested that the m. brachialis probably contributes less to the exerted total flexion torque during slow voluntary movements. The aim of this study is to investigate the coordination of the three main elbow flexor muscles, i.e. the m. biceps brachii, the m. brachialis and the m. brachioradialis, in force tasks and movement tasks. The motor-unit behaviour of the m. biceps brachii has also been investigated during a force task while movements were imposed on the subject's forearm (Tax et al. 1990). Under this condition and in isometric contractions the recruitment levels and the initial firing frequencies of the biceps motor units appeared to be similar. From these results it was concluded that the observed different behaviour of the biceps in voluntary isotonic movements is caused by differences in the central activation of the motoneurone pool in movement tasks and in force tasks. In this study too imposed movement experiments are carried out but our aim here is to investigate the extent te which the above conclusion holds for the m. brachialis and the m. brachioradialis.
Methods Experiments were performed on six normal (5 male, 1 female) subjects who had given informed consent and who had no known history of neurological or motor disorder. The experimental set-up, the EMG recording and data analysis have been described previously (Tax et al. 1989and 1990).Therefore only a short description will be given here.
568 The subject was seated in a dentist's chair. The right arm of the subject was 80 deg abducted and supported under the elbow joint. The wrist was tightly fixed in a wrist-holder. This wrist-holder was fastened to a device which allowed movements of the forearm in flexion/extension direction. Torques exerted at the wrist were measured in three dimensions independently: flexion/extension and supination/pronation of the forearm, and exorotation/endorotation of the humerus. By means of a torque motor torques could be applied to the subject's forearm in flexion/extension direction. The position in flexion/extension direction (resolution 0.04 deg) is given as the angle between the upper arm and the forearm. Full extension corresponds to 180 deg. The position of the forearm in supination/ pronation direction was fixed in the neutral position between full supination and full pronation.
EMG recording and data analyses Motor-unit activity in m. biceps brachii (both the long head and the short head), m. brachialis and m. brachioradialis was examined by means of intramuscular EMG recordings (Nylon-coated fine-wire electrodes). Bipolar recordings were amplified and band-pass filtered (typically 320 Hz-32 kHz). The EMG signals from the elbow flexor muscles, 'the signals of the torques in three dimensions and the position signal in flexion/extension direction were stored for off-line analysis. In this off-line analysis both the recruitment threshold and the initial firing frequency of the motor units were determined. The initial firing frequency was defined as the number of action potentials during the first second after recruitment.
Experimental protocol Motor-unit behaviour is studied under three different conditions: 'isometric' contractions, 'voluntary movement' (both with constant and increasing load) and 'imposed movement'.
Isometric contractions Under this condition the device in which the wrist-holder was fixed was fastened in such a way that no movement was possible in any direction. The forearm was 100 deg flexed. The subject was asked to slowly increase the isometric flexion torque up to typically 20% of the maximum voluntary contraction (MVC).
Voluntary movement At the start of each voluntary flexion/extension movement trial the forearm of the subject was 110 deg/90 deg flexed. The subject was requested to relax his arm completely.
Constant preload (isotonic). The torque, applied at the wrist in extension direction by the torque motor, was increased gradually up to a certain level and then it was kept constant within 0.15 Nm by means of an electronic force-feedback circuit. The subject was then asked to move his forearm from 90 deg to 110 deg (extension movement) or from 110 deg to 90 deg (flexion movement) at a prescribed constant velocity of 3 deg/s. For different preloads we ascertained whether the motor unit under investigation was active during the movement. Increasing preload. In three sessions the subject was asked first to start moving his forearm in flexion direction at a prescribed constant velocity of 3 deg/s. After the onset of the movement the preload was increased gradually by means of the electronic force-feedback circuit. Therefore, in order to obey the instruction to make a flexion movement of constant velocity the subject had to increase the exerted flexion torque during the movement. We ensured that the
motor unit under investigation was recruited near an elbow angle of 100 deg by timing the onset of the increase in preload and/or by adjusting the increase in the preload per second.
Imposed movement A microprocessor controlled the torque motor in such a way that movements could be imposed on the subject's forearm at a constant velocity (3 deg/s). For this purpose we used the method of position feedback. During imposed extension movements the forearm of the subject was moved from 90 deg to 110 deg and during imposed flexion movements from 110 deg to 90 deg. During these imposed movements the subject was instructed to increase the exerted flexion torque from the relaxed state (0 Nm) to typically 20% MVC. The 'isometric' trials were carried out both at the beginning and at the end of each session. In between, usually either the batch of voluntary movement trials against a constant load (nine sessions) or the batch of voluntary movement trials against an increasing load (three sessions) was carried out in random order. In five additional sessions m. brachialis and m. brachioradialis motor-unit behaviour was investigated during imposed movements. In all experiments the subject was instructed not to exert torques in supination/pronation or in exorotation/endorotation direction. Trials that did not satisfy this condition were not included in the analysis.
Results I n this s t u d y m o t o r - u n i t b e h a v i o u r is s t u d i e d in the m. biceps brachii, the m. b r a c h i a l i s a n d the m. b r a c h i o r a dialis. O f the m. biceps brachii it is o n l y the m o t o r units o f the ' s u m m i n g u n i t ' t y p e (ter H a a r R o m e n y et al. 1984) which are c o n s i d e r e d , i.e. m o t o r units t h a t are recruited by exerting t o r q u e s b o t h in flexion d i r e c t i o n a n d s u p i n a t i o n direction. These m o t o r units m a k e u p the m a j o r i t y o f all m o t o r units in the biceps. O f the m. brachialis a n d the m. b r a c h i o r a d i a l i s b o t h k n o w n m o t o r - u n i t types are considered (v. Z u y l e n et al. 1988), i.e. m o t o r units w h o s e flexion t h r e s h o l d is i n d e p e n d e n t o f the level o f exerted s u p i n a t i o n / p r o n a t i o n t o r q u e a n d m o t o r units w h o s e flexion t h r e s h o l d increases with increasing s u p i n a t i o n / p r o n a t i o n torque. A s a n e x a m p l e o f the relative a c t i v a t i o n o f e l b o w flexor muscles the r e c r u i t m e n t b e h a v i o u r o f a s i m u l t a n e o u s l y r e c o r d e d biceps a n d b r a c h i o r a d i a l i s m o t o r unit is s h o w n in Fig. 1 for i s o m e t r i c c o n t r a c t i o n s a n d for v o l u n t a r y i s o t o n i c flexion a n d extension m o v e m e n t s . T h e average isometric r e c r u i t m e n t t h r e s h o l d s o f the b r a c h i o r a d i a l i s a n d biceps m o t o r unit are 4.5 +_0.3 N m a n d 8.0 ___0.2 N m respectively. T h e r e c r u i t m e n t t h r e s h o l d d u r i n g v o l u n t a r y m o v e m e n t s is defined as the level o f flexion t o r q u e t h a t d e m a r c a t e s the t o r q u e levels for which the m o t o r unit was active or inactive d u r i n g the m o v e m e n t . F i g u r e 1 shows t h a t the e s t i m a t e d r e c r u i t m e n t t h r e s h o l d is higher for the b r a c h i o r a d i a l i s m o t o r unit a n d lower for the biceps m o t o r unit d u r i n g b o t h slow v o l u n t a r y isotonic flexion a n d extension m o v e m e n t s t h a n d u r i n g i s o m e t r i c c o n t r a c t i o n s . T h e increase a n d decrease in the r e c r u i t m e n t t h r e s h o l d o f the b r a c h i o r a d i a l i s a n d biceps m o t o r unit respectively is such t h a t their r e c r u i t m e n t o r d e r d u r i n g v o l u n t a r y m o v e m e n t s is frequently the reverse o f their r e c r u i t m e n t o r d e r d u r i n g isometric c o n t r a c t i o n s . This reversal o f r e c r u i t m e n t o r d e r never o c c u r r e d d u r i n g the isometric trials which
569 indicates that the relative activation of these two m o t o r units depends on the required task: isometric contraction or slow voluntary movement 9 F o r the m. brachioradialis m o t o r unit the firing frequency behaviour during 'isometric' and both 'isotonic' flexion and extension movement trials is shown in Fig. 2. In the case of the 'isometric' trials the recruitment threshold is plotted as a function o f the firing frequency at recruitment. Different combinations of recruitment threshold and initial firing frequency in both kinds o f isotonic movements are plotted too. Figure 2 shows again that the brachioradialis m o t o r unit is active at lower torque levels during 'isometric' contractions than during
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Fig. 1. Average recruitment behaviour of a brachioradialis (filled circle) and a biceps (open circle) motor unit for 'isometric' contractions and for voluntary 'isotonic' flexion (3 deg/s) and extension ( - 3 deg/s) movements
'isotonic' movements. In addition, the firing frequency is slightly higher during 'isotonic' flexion movements and lower during 'isotonic' extension movements than it is during isometric contractions. Motor-unit activity in voluntary isotonic flexion movements m a y be derived from voluntary flexion movements against an increasing preload (Tax et al. 1990). The latter experiments allow the recruitment and firing frequency behaviour of all discernible m o t o r units showing in a particular intramuscular EMG-recording to be determined much more quickly than the laborious isotonic experiments. Therefore, in this study three additional flexion movement experiments against an increasing load are carried out. In general, all brachioradialis (n = 9) as well as all brachialis (n = 26) m o t o r units investigated in this study (voluntary movements against either a constant or an increasing preload) show a recruitment behaviour and firing frequency behaviour similar to those of the brachioradialis m o t o r unit described in the previous paragraph 9 The behaviour of the biceps m o t o r units ( n = 15) observed in these experiments is in good agreement with results reported before (see Tax et al. 1989 and the Discussion). F o r three subjects, from whom we were able to record motor-unit activity in all three flexor muscles, the estimated recruitment threshold of the m. brachialis, the m. brachioradialis and the m. biceps m o t o r units is plotted for voluntary flexion movements (against either a constant preload or an increasing preload) against their average 'isometric' recruitment threshold in Fig. 3. Linear regression analysis is used to fit on the one hand the brachialis/brachioradialis data and on the other hand the
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Fig. 2. Data obtained from the same brachioradialis motor unit as in Fig. 1. Combinations of the recruitment threshold and the (initial) firing frequency at recruitment are plotted for 'isometric' contractions (filled squares) and both 'isotonic' flexion (filled circles) and extension (open circles) movements
Fig. 3. Joint recruitment data of m. biceps (filled squares), m. brachialis (open circles) and m9 brachioradialis (filled circles) gathered from seven experiments (subjects TT, CE and JS). For each investigated motor unit the estimated recruitment threshold for slow voluntary flexion movements (against either a constant or an increasing preload) is plotted against the average isometric recruitment threshold9 Linear regression analysis is used to fit the brachialis/brachioradialis data and the biceps data
570 biceps data. The slope of the brachialis/brachioradialis fit is 1.29+0.03 whereas the slope of the biceps fit is 0.77 +0.02. A slope equal to one would indicate that the recruitment threshold of a motor unit is independent of the kind of trial considered here. It can be concluded that the difference in the recruitment threshold of the elbow flexor muscles during flexion movements (against either a constant or an increasing preload) and isometric contractions is proportional to the isometric recruitment threshold. The mean increase in firing frequency during voluntary flexion movements compared to the firing frequency during 'isometric' contractions was !.6 + 0.9 Hz for the m. biceps motor units and 1.0_+0.2 Hz for the brachialis/brachioradialis motor units. No significant correlation was found between the increase in the firing frequency and the 'isometric' recruitment threshold. For the 14 brachialis motor units (three subjects) that were investigated during imposed movements the average recruitment threshold during imposed flexion movements is plotted against the average isometric recruitment threshold in Fig. 4. Linear regression analysis is used to fit these data. The slope of the fitted line is 0.98 _+0.04. This means that the over-all recruitment behaviour of the m. brachialis motor units is similar for imposed flexion movements and isometric contractions. The same conclusion holds when the recruitment threshold for imposed extension movements is compared to the recruitment threshold for isometric contractions. The recruitment behaviour of the only brachioradialis motor unit in our sample revealed the same behaviour as described for the brachialis motor units. We have shown that the initial firing frequency of the brachialis and brachioradialis motor units is higher during slow voluntary flexion movements and lower during slow voluntary extension movements than during isometric contractions. However, no such differences in the initial firing frequency occur during the imposed movement
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Fig. 4. For the 14 brachialis motor units the average recruitment threshold during imposed flexion movements is plotted against the average isometric recruitment threshold. Linear regression analysis is used to fit the data
experiments. In fact, all motor units (12) of which we were able to determine the firing frequency reliably showed no differences in the initial firing frequency for imposed flexion and extension movements (0.1 +_0.3 Hz). We conclude therefore that the over-all firing frequency behaviour of the investigated motor units is similar for isometric contractions and for both imposed flexion and extension movements.
Discussion
The recruitment behaviour of motor units in the m. biceps brachii on the one hand and in the m. brachialis and the m. brachioradialis on the other hand is rather different for voluntary movements under external loads and for isometric contractions. In contrast to the recruitment threshold of the biceps motor units the recruitment threshold of both m. brachialis and m. brachioradialis motor units is higher during slow voluntary flexion and extension movements than during isometric contractions. The decrease (biceps) and increase (brachialis and brachioradialis) are proportional to the isometric threshold torque level (see Fig. 3) of the motor units. This demonstrates that the recruitment order within these muscles is generally maintained. In addition, the motor-unit firing frequency of these three elbow flexor muscles depends on the direction of movement (for the biceps, see Tax et al. 1989). The firing frequency is higher for slow voluntary flexion movements and lower for slow voluntary extension movements than for isometric contractions. Two main conclusions can be drawn from these results. First of all, one single activation parameter (total synaptic drive?) cannot account for the motor-unit activity observed during the isometric contractions and during the voluntary movements. The similar recruitment order within each flexor muscle does however indicate a homogeneous activation of the different flexor motoneurone pools under these conditions. But the initial firing frequency of the motoneurones can be adjusted rather independently: the motoneurones seem to possess several different 'modi operandi' related to the required task. This means that the relative contribution of the two force-grading mechanisms, namely the recruitment of motor units and the modulation of their firing frequency, is task dependent. Secondly, the coordination of the three synergistic elbow flexor muscles is different for isometric contractions and slow voluntary movements: the activation during very slow voluntary movements (3 deg/s) is shifted somewhat from the brachialis and brachioradialis motoneurone pools to the motoneurone pool of the biceps in comparison to the activation during isometric contractions. In other words, there is a significant difference in the relative contribution of the brachialis/brachioradialis and the biceps to the total exerted flexion torque at the wrist in force tasks and in slow movement tasks. The movement trials (against both a constant and an increasing load) were carried out in a small range of about 20 deg all around the reference position. The motor-unit activity, while the forearm was passing through the reference position, was compared to the isometric motor-unit
571 activity in that position. In this way the effect of the forcelength relation on our results is negligible. The effect of the force-velocity relation does not play an important role in our experiments either. If the difference in the motor-unit behaviour during voluntary movements and isometric contractions is due to this muscle property, then one would expect this difference to appear in all flexor muscles. However, the motor-unit behaviour of both the brachialis and the brachioradialis is quite different from the motorunit behaviour of the biceps during slow voluntary movements. Furthermore, the motor-unit behaviour of the three elbow flexor muscles is very similar for isometric contractions and imposed movements (Tax et al. 1990 and Fig. 4). This means that the same motor units are responsible for equal amounts of flexion torque in the following conditions: isometric flexion contraction, flexion contraction during imposed flexion movements (3 deg/s) and flexion contraction during imposed extension movements ( - 3 deg/s). This shows again that the influence of the force-velocity relation is negligible, as was to be expected from the very low velocities in our experiments. For low torque levels ( < 10 Nm) we were able, in the case of three subjects, to determine the motor-unit behaviour of the three major elbow flexor muscles both during voluntary movement tasks and during isometric force tasks. The average recruitment behaviour (see Fig. 3) and the average firing frequency behaviour (see Results) of this sample of motor units during isometric contractions and voluntary flexion movements (against a constant and an increasing load) can be used to estimate the different relative contributions of the elbow flexor muscles under both conditions. Consider the situation where a subject is exerting a flexion torque of X Nm while making a voluntary flexion movement. From Fig. 3 it can be determined that during an isometric contraction of X/0.77 Nm the same biceps motor units will be active. The relative contribution of the m. biceps, the m. brachialis/m, brachioradialis and the m. pronator teres to the total exerted isometric flexion torque at the wrist was estimated to be 36%, 57% and 7% (Jorgensen et al. 1971; v. Zuylen et al. 1988; Jongen et al. 1989). Therefore, if the recruitment behaviour alone were taken into account these active biceps motor units would contribute a torque of 0.36X/0.77 = 0 . 4 7 X N m to the total exerted flexion torque of X Nm during slow voluntary flexion movements. In the same way the contribiation of the brachialis/brachioradialis can be estimated to be 0.57X/1.29 = 0.44X Nm. Thus, the relative contribution of the three major elbow flexor muscles is decreased from 36 + 57 = 93% during isometric contractions to 47 + 44 = 91% during voluntary flexion movements. If one takes into consideration the additional contribution of the m. pronator teres (despite the fact that no data of this small muscle are available) it seems obvious that the observed increase in initial firing frequency (about 1 Hz for the three flexor muscles) should be responsible for only a few per cent of the total exerted flexion torque during slow voluntary flexion movements. This seems in reasonable agreement with experimental findings. F r o m Kernell et al. (1983, see their Fig. 2) it can be estimated that, for the slow motor units of the m. peroneus longus in the cat,
the maximum slope of the force-frequency relation is about 5%/Hz. In addition, the range of frequencies for which the force output of the motor units is frequencydependent is rather small. In general a considerable number of active motor units is not firing at a frequency in that range (for instance, those motor units that have already reached saturation frequency). So the effect of the observed increase in initial firing frequency on the exerted muscle force is probably at most a few per cent. Therefore, if the relative contribution to the total exerted flexion torque during slow voluntary flexion movements and isometric contractions are compared it is found that the relative contribution of the biceps is increased from 36% (isometric) to about 48% (voluntary movement) whereas the relative contribution of the brachialis/brachioradialis is decreased from 57% (isometric) to about 45% (voluntary movement). Because the biceps is a biarticular muscle it will also exert a higher torque in the shoulder joint during voluntary movements around the elbow joint than during isometric contractions. Since this torque is certainly not counteracted by the m. triceps (Tax et al. 1989), other muscles acting around the shoulder joint must account for the stabilisation of the upper arm. As was already shown for the m. biceps brachii (Tax et al. 1990), the behaviour of motor units in the m. brachialis and m. brachioradialis for torque tasks in flexion direction is independent of whether the contraction is made under isometric conditions or during imposed movements. Therefore, it is not the movement itself that causes the different motor-unit behaviour of the three elbow flexor muscles in slow voluntary movements (against both a constant and an increasing load). From these results it can be concluded that the c~ and/or motoneurone pools of the elbow flexor muscles are differently activated by central sources in force tasks and in slow movement tasks. It is still not clear which neural mechanisms are involved in this different central activation of the flexor motoneurone pools. But, it is known that serotonergic raphe-spinal and noradrenergic coerulusspinal projections are able to change both the excitability and the firing frequency of the motoneurones (Conway et al. 1988). In the case of our experiments this could mean that the different flexor motoneurone pools might receive different monoaminergic input during voluntary movements and isometric contractions.
References
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