Differences in coordination of elbow flexor muscles in force tasks and in movement tasks

Summary Motor-unit activity in m. biceps brachii, m. brachialis and m. 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 of 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.     

Coordination and inhomogeneous activation of human arm muscles during isometric torques

1. In this study we have recorded the activity of motor units of the important muscles acting across the elbow joint during combinations of voluntary isometric torques in flexion/extension direction and supination/pronation direction at different angles of the elbow joint. 2. Most muscles are not activated homogeneously; instead the population of motor units of muscles can be subdivided into several subpopulations. Inhomogeneous activation of the population of motor units in a muscle is a general finding and is not restricted to some multifunctional muscles. 3. Muscles can be activated even if their mechanical action does not contribute directly to the external torque. For example, m. triceps is activated during supination torques and thus compensates for the flexion component of the m. biceps. On the other hand, motor units in muscles are not necessarily activated if their mechanical action contributes to a prescribed torque. For example, there are motor units in the m. biceps that are activated during flexion torques, but not during supination torques. 4. The relative activation of the muscles depends on the elbow angle. Changing the elbow angle affects the mechanical advantage of different muscles differently. In general, muscles with the larger mechanical advantage receive the larger input. 5. We have calculated the relative contributions of some muscles to isometric torques. These contributions depend on the combination of the torques exerted. 6. Existing theoretical models on muscle coordination do not incorporate subpopulations of motor units and therefore need to be amended.     

Coordination of arm muscles during flexion and supination: application of the tensor analysis approach

In order to obtain a good understanding of the coordination of the motor system several problems have to be solved. Two major issues are: (1) that muscles do not form an orthogonal coordinate system, and (2) that the number of muscles that may contribute to a movement in general exceeds the number of degrees of freedom of the movement. The latter allows the movement to be executed by an infinite variety of muscle activations. A theoretical solution to these problems has been elaborated by Pellionisz and Llinás. However, convincing experimental support for this theory is still lacking. In this paper the theory has been applied to the activation of arm muscles which contribute to flexion/extension and supination/pronation of the arm. Motor unit activity was recorded with fine wire electrodes. As reported in previous papers, the recruitment threshold of motor units in arm muscles during isometric contraction depends on a combination of forces in flexion and supination directions. This dependence is characteristic for motor units in a single muscle, but is very different for motor units in different muscles. The theoretical results are in good agreement with the behavior of the recruitment threshold for flexion, which decreases (such as m. biceps brachii), or increases (such as for m. brachialis and m. brachioradialis) with force in supination direction. The theory also correctly predicts how the recruitment threshold for motor units changes as a function of the angle between forearm and upper arm. These results give firm support to the hypothesis that the central nervous system uses a tensorial approach for the activation of the motor system, as originally proposed by Pellionisz and Llinás.     

Relation between torque history, firing frequency, decruitment levels and force balance in two flexors of the elbow

By means of intramuscular electromyographic recordings, we studied the firing frequencies and recruitment/decruitment thresholds of individual motor units in two elbow flexors, the biarticular biceps brachii muscle and the monoarticular brachioradialis muscle. Subjects had to perform isometric contractions with increasing elbow flexion torque until a specific peak torque level was reached. The torque level was kept constant for 6 s during which firing frequencies were measured. Then the torque was decreased to a lower level and, after 3 s, firing frequencies were again measured for 6 s. By repeating this procedure, the torque level was decreased stepwise until the motor unit under study stopped firing. The last level before the unit stopped firing was considered to be the decruitment torque level. We measured the firing frequency at recruitment and decruitment, the torque- frequency relationship and the recruitment and decruitment torque thresholds after various levels of peak torque. In the biceps, both the firing frequencies at a specific torque level and the decruitment torque level itself were independent of the peak torque. In the brachioradialis, however, firing frequencies at a specific torque level decreased and decruitment torque levels increased after subjects generated higher peak torques. Thus, in this muscle firing frequencies as well as decruitment thresholds show hysteresis effects. The result indicates a shift of force from the brachioradialis muscle during recruitment to the biceps muscle during decruitment. This shift is smaller than was concluded from previous studies in which decruitment threshold levels for the brachioradialis muscle were assumed to be independent of force history. Moreover, we found that in both muscles decruitment firing frequencies were lower than recruitment frequencies and they were independent of the peak torque level. In order to analyse the effect of the peak torque level on the distribution of force over the two muscles, we performed a model study in which we simulated the activation-frequency relation of two elbow flexors: a biceps-like and brachioradialis-like muscle, each contributing equally to the elbow torque during recruitment. In addition, we analysed how the different behaviour of the biceps and the brachioradialis during decruitment alters their contribution to the total torque production and how this redistribution is caused. The model study shows that the shift in contribution to the total torque is not constant during the relaxation phase and is not caused by a simple mechanism like a shift of activation from one muscle to another. Furthermore, changes limited to the muscle in which hysteresis is present do not seem to be sufficient to explain the experimental results. Received: 19 October 1998 / Accepted: 14 June 1999     

Differences in the activation of m. biceps brachii in the control of slow isotonic movements and isometric contractions

Summary We have compared muscle activation in the control of slow isotonic movements and isometric contractions. Specific attention has been given to the contribution of the two force-grading mechanisms, the recruitment of motor units and the modulation of firing frequency in motor units that have already been recruited. The recruitment order of the m. biceps motor units under study was the same during isometric contractions and slow isotonic movements. However, the recruitment thresholds of the m. biceps units were considerably lower for both isotonic flexion and extension movements, even at velocities as low as 2 deg/s, than for isometric contractions. Furthermore, firing frequency at recruitment was found to depend on the motor task: at recruitment the motoneurone starts firing with a higher firing frequency during isotonic flexion movements and a lower firing frequency during isotonic extension movements than during isometric contractions. Two main conclusions can be drawn from these results. First of all, the concept of one single activation parameter (total synaptic drive?) cannot account for the motor-unit behaviour observed during our experiments: the relative contribution of the two forcegrading mechanisms is different for different tasks. Secondly, the distribution of activity among flexor motoneurone pools is different for isometric contractions and isotonic movements.     

The effect of muscle pain on elbow flexion and coactivation tasks

The effects of muscle pain on movement can easily be observed in daily life routines. However, the influence of muscle pain on motor control strategies has not been fully clarified. In this human experimental study it was hypothesized that muscle pain affects the motor control of elbow flexion movements, in different combinations of range of motion and target size, by decreased agonistic muscle activity and increased antagonistic muscle activity with consequent implications on kinematic parameters. The effects of experimentally induced muscle pain on movement strategy for: (1) small and large range of motion (ROM) elbow flexion movements towards a wide target, (2) large ROM flexion movements towards a narrow and wide target, and (3) subsequent coactivation of agonistic and antagonistic muscles to elbow flexion were assessed. Muscle pain induced by injections of hypertonic saline (1 ml, 5.8%) in either m. biceps brachii or m. triceps brachii caused similar effects on the movements. For low accurate movements the initial (100 ms) integrated electromyographic (EMG) activity of m. biceps brachii was decreased during muscle pain. In contrast, integrated EMG of the entire m. biceps brachii burst was decreased by muscle pain only for small ROM at a low accuracy, which also showed decreased EMG activity of m. triceps brachii and m. brachioradialis, together with increased activity of m. trapezius. Finally, high accurate movements and post-movement coactivation were generally not modulated by muscle pain. In summary, the present study shows that acute muscle pain can perturb the motor control strategy, which might be highly important in occupational settings where such a change may need compensatory actions from other muscles and thereby eventually contribute to the development of musculoskeletal pain problems.     

Elbow torques and EMG patterns of flexor muscles during different isometric tasks.

This paper examines the torque responses and EMG activity levels in four muscles acting at the elbow joint during different combinations of one- and two- degree of freedom isometric torque production (single and dual tasks, respectively). Flexor and supinator/pronator torques and surface EMG signals from m. biceps brachii, m. brachialis, m. brachioradialis and m. triceps brachii were measured in 16 male subjects while they performed maximal effort isometric contractions of pure flexion, pure supination, pure pronation, combined flexion and supination and combined flexion and pronation. In the single tasks, the torque responses were consistent with task requirements, but the dual task results were surprising in that flexor torque levels were reduced as compared to pure flexion, while supinator/pronator torque levels were as high or higher than in pure supination or pronation. Muscle activity levels varied with task, and could not always explain the differences observed in torque responses. These data are discussed within the framework of subpopulations of task-specific motor units within each muscle. The implications of such task-specific muscle units are related to musculoskeletal modelling and previous EMG - torque relationships found at the elbow.     

Modulation of corticospinal excitability dependent upon imagined force level

Motor imagery is defined as the mental execution of a movement without any muscle activity. In the present study, corticospinal excitability was assessed by motor evoked potentials (MEPs) when the subjects imagined isometric elbow flexion at various force levels. Electromyography was recorded from the right brachioradialis, the biceps brachii and the triceps brachii muscles. First, the maximum voluntary contraction (MVC) of elbow flexion was recorded in each subject. Subjects practiced performing 10, 30 and 60 % MVC using visual feedback. After the practice, MEPs were recorded during the imagery of elbow flexion with the forces of 10, 30 and 60 % MVC without any feedback. After the MEPs recording, we assigned subjects to reproduce the actual elbow flexion force at 10, 30 and 60 % MVC. The MEPs amplitudes in the brachioradialis and biceps brachii in the 60 % MVC condition were significantly greater than those in the 10 % MVC condition (p < 0.05). These findings suggest that the enhancement of corticospinal excitability during motor imagery is associated with an increase in imagined force level.     

Group III and IV muscle afferents differentially affect the motor cortex and motoneurones in humans

The influence of group III and IV muscle afferents on human motor pathways is poorly understood. We used experimental muscle pain to investigate their effects at cortical and spinal levels. In two studies, electromyographic (EMG) responses in elbow flexors and extensors to stimulation of the motor cortex (MEPs) and corticospinal tract (CMEPs) were evoked before, during, and after infusion of hypertonic saline into biceps brachii to evoke deep pain. In study 1, MEPs and CMEPs were evoked in relaxed muscles and during contractions to a constant elbow flexion force . In study 2, responses were evoked during elbow flexion and extension to a constant level of biceps or triceps brachii EMG , respectively. During pain, the size of CMEPs in relaxed biceps and triceps increased (by ∼47% and ∼56%, respectively; P < 0.05). MEPs did not change with pain, but relative to CMEPs, they decreased in biceps (by ∼34%) and triceps (by ∼43%; P < 0.05). During flexion with constant force, ongoing background EMG and MEPs decreased for biceps during pain (by ∼14% and 15%; P < 0.05). During flexion with a constant EMG level, CMEPs in biceps and triceps increased during pain (by ∼30% and ∼26%, respectively; P < 0.05) and relative to CMEPs, MEPs decreased for both muscles (by ∼20% and ∼17%; P < 0.05). For extension, CMEPs in triceps increased during pain (by ∼22%) whereas MEPs decreased (by ∼15%; P < 0.05). Activity in group III and IV muscle afferents produced by hypertonic saline facilitates motoneurones innervating elbow flexor and extensor muscles but depresses motor cortical cells projecting to these muscles.     

Motor unit recruitment strategy changes with skill acquisition

The modifications of motor unit recruitment strategy due to skill acquisition was determined in the elbow flexor-extensor muscles of normal human subjects. The median frequency of the power density spectra of the electromyograms recorded from the biceps and triceps muscles during a 3-s linear increase in flexion force in the range of 0–100% maximal voluntary contraction (MVC) was calculated for each subject, every 2 weeks over a total 6-week period during which subjects practiced linear flexion force increase three times a week. Electromyograms were recorded with two pairs of electrodes of different size and electrode spacing. It was shown that skill acquisition due to the 360 practice trials over the 6-week period caused an increase in the initial motor unit recruitment phase of the agonist's force generation cycle from about 0–65% MVC to about 0–85% MVC. The increase in the recruitment range was gradual and statistically significant for the measurements made every 2 weeks. The reccruitment range of the antagonist triceps demonstrated a minor, but statistically insignificant, decrease over the same training period. There was a minor, but statistically significant, advantage of using small electrodes and inter-electrode spacing. It was concluded that skill acquisition, due to repeated functional use of a muscle in the same contraction mode, results in a slower, prolonged recruitment of motor units in the initial segment of the force generation cycle, thereby allowing a more precise and accurate control of the increments of force increase. Such conclusions reinforce the concept advocating the plasticity of motor unit control according to the functional demands imposed on the muscle. The results have significant implications in the design of various athletic, occupational and rehabilitation training modalities for optimal performance of various movement functions.     

The relation between the surface electromyogram and muscular force.

1. Motor units in the first dorsal interosseus muscle of normal human subjects were recorded by needle electrodes, together with the surface electromyogram (e.m.g.). The wave form contributed by each motor unit to the surface e.m.g. was determined by signal averaging. 2. The peak-to-peak amplitude of the wave form contributed to the surface e.m.g. by a motor unit increased approximately as the square root of the threshold force at which the unit was recruited. The peak-to-peak duration of the wave form was independent of the threshold force. 3. Large and small motor units are uniformly distributed throughout this muscle, and the muscle fibres making up a motor unit may be widely dispersed. 4. The rectified surface e.m.g. was computed as a function of force, based on the sample of motor units recorded. The largest contribution of motor unit recruitment occurs at low force levels, while the contribution of increased firing rate becomes more important at higher force levels. 5. Possible bases for the common experimental observation that the mean rectified surface e.m.g. varies linearly with the force generated by a muscle are discussed. E.m.g. potentials and contractile responses may both sum non-linearly at moderate to high force levels, but in such a way that the rectified surface e.m.g. is still approximately linearly related to the force produced by the muscle.     

Antagonist muscle activation preceding rapid flexion movements of the elbow joint in human subjects

Our study was designed to look for interactions between fast movements and pre-existing voluntary tonic motor activity when both motor acts employ the same muscles. Five normal subjects performed a continuous sequence of two motor tasks about their right elbow joint: A tonic isometric extension (slowly increasing or decreasing) against a force transducer, followed immediately after a "go" tone by a fast isotonic flexion. The position of the lower arm was recorded using a search coil system. Signals (force, position, and surface EMGs of triceps and biceps brachii muscles) were A/D converted and sampled at 1 kHz. A premovement silence in the tonically active triceps muscle (extensor) usually preceded the fast flexion movement if the triceps' tonic force was either constant or decreased slowly. If the tonic triceps activity had been increasing before the fast flexion began, this classical picture disappeared, and the premovement silence was replaced by a phasic premovement excitation. Subjects were unaware of this transient EMG and force increase in the unintended direction. Our results demonstrate unconscious reciprocal interactions between commands governing evolving movements (and tuning the motor system accordingly) and those concerned with ongoing motor acts.     

Reductions in recruitment force thresholds in human single motor units by successive voluntary contractions

Summary Recruitment force thresholds of biceps brachii single motor units were studied in 4 male subjects before and after an isometric muscle contraction, passive muscle stretch, or following successive muscle contractions, muscle stretches or during alternations between muscle stretches and muscle contractions. Isometric muscle contractions of 5 s duration decreased subsequent single motor unit force thresholds. These force thresholds could usually be reset at or near precontraction force threshold values by passive muscle stretch induced by elbow extension. Single motor units showing reduced force thresholds following contraction were momentarily derecruited during and/or after muscle stretch. Successive muscle stretches alone did not significantly alter single motor unit force thresholds. In contrast, single motor unit recruitment force thresholds during successive weaker contractions were progressively lowered. Intercontraction muscle stretches maintained the single motor unit force thresholds at or near the initial force threshold level. The mechanism(s) underlying a muscle contraction-induced lowering of single motor unit force thresholds may reside in stretch reflex pathways.     

Motor unit recruitment in human medial gastrocnemius muscle during combined knee flexion and plantarflexion isometric contractions

Previous work on multifunctional muscle has suggested that motor unit recruitment during a combined force task is the result of an interactive effect of weighted inputs acting simultaneously on the motoneuron pool. The present study shows that a similar effect describes motor unit activation in a two-joint muscle as forces are combined at both proximal and distal attachments. The recruitment thresholds of single motor units in medial gastrocnemius muscle were determined during combined knee flexion and plantarflexion isometric contractions. Slow isometric ramp contractions in knee flexion were produced while maintaining various background levels of plantarflexion force. The combination of knee flexion and plantarflexion forces at which a motor unit initially discharged was used to characterize recruitment as represented by the slope of the regression line fit to the individual data points. Each subject completed two experiments; one at each of two knee joint angles, with the ankle joint fixed at 90°. The effect of knee angle was assessed by comparing the slopes of the regression lines that characterized motor unit recruitment at each knee angle. Motor units in medial gastrocnemius were recruited when the linear sum of the forces exerted in plantarflexion and knee flexion exceeded a certain threshold of combined force. Specifically, the apparent force threshold of recruitment in knee flexion decreased as the level of force maintained in plantarflexion increased. Further, evidence is provided indicating that the linear relationship describing recruitment in two-joint muscle is dependent upon joint angle. The basis for the alteration in force threshold is thought to be related to changes in muscle length and mechanical advantage which might adjust the relative weighting of inputs that determine muscle activation patterns. These results indicate a possible common strategy employed by the nervous system in coordinating the activation of motor units to perform a specific task.     

Simulation linking EMG power spectra to recruitment and rate coding.

For muscles, a graded increase in motor unit size, with the number of fibres in the motor units forming an arithmetic progression, leads to a model consistent with experimental findings. This model has been combined with electrical signal characteristics of activated muscle fibres and the signal attenuation due to the spread of the electrical signal to bipolar surface electrodes. For the biceps brachii this electromechanical model links motor unit recruitment, rate coding and frequency shifts in the surface EMG power spectra. Derived data suggests that motor unit degeneration results in an abnormally large high frequency EMG component.     

Motor unit recruitment strategy of knee antagonist muscles in a step-wise,increasing isometric contraction

The purpose of this study was to determine if differences exist between the control strategies of two antagonist thigh muscles during knee flexion and extension muscular coactivation. Surface myoelectric signal (MES) of the quadriceps (rectus femoris) and the hamstrings (semitendinosus) were obtained from both muscles while performing step-wise increasing contractions during flexion and extension with the knee at 1.57 rad of flexion (90 degrees). The median frequency of the power density spectrum, which is related to the average muscle fiber action potential conduction velocity and therefore to motor unit recruitment, was calculated from each MES. The results suggest that, in all the subjects tested, when the muscle acts as antagonist most motor units are recruited up to 50% of the maximal voluntary force, whereas when the muscle acts as antagonist motor units are recruited up to 40% of the maximal voluntary force. The force range past 40–50% of the maximal force is also characterized by differences between the agonist/antagonist.     

Maximal isometric force and neural activity during bilateral and unilateral elbow flexion in humans

We investigated maximal isometric force and electromyographic (EMG) activity of the biceps brachii muscle during rapid bilateral (BL) and unilateral (UL) elbow flexion in 11 right-handed subjects. The BL exhibited a deficit in force for both arms and more so for the right than the left arm during the rising phase of force generation. The EMG of the left biceps brachii muscle was similar during UL and BL, but for the right arm EMG was lower during BL than during UL for the rising phase of force generation. The BL to UL ratio of mean power frequency of the EMG was lower for the right than for the left arm. The data would suggest that the relatively small BL strength was associated with a equally small EMG and a shift to a lower mean power frequency especially for the fast motor units of the dominant muscle.     

Discharge characteristics of biceps brachii motor units at recruitment when older adults sustained an isometric contraction

The purpose of this study was to compare the discharge characteristics of motor units recruited during an isometric contraction that was sustained with the elbow flexor muscles by older adults at target forces that were less than the recruitment threshold force of each isolated motor unit. The discharge times of 27 single motor units were recorded from the biceps brachii in 11 old adults (78.8 ± 5.9 yr). The target force was set at either a relatively small (6.6 ± 3.7% maximum) or large (11.4 ± 4.5% maximum) difference below the recruitment threshold force and the contraction was sustained until the motor unit was recruited and discharged action potentials for about 60 s. The time to recruitment was longer for the large target-force difference (P = 0.001). At recruitment, the motor units discharged repetitively for both target-force differences, which contrasts with data from young adults when motor units discharged intermittently at recruitment for the large difference between recruitment threshold force and target force. The coefficient of variation (CV) for the first five interspike intervals (ISIs) increased from the small (18.7 ± 7.9) to large difference (35.0 ± 10.2%, P = 0.008) for the young adults, but did not differ for the two target force differences for the old adults (26.3 ± 14.7 to 24.0 ± 13.1%, P = 0.610). When analyzed across the discharge duration, the average CV for the ISI decreased similarly for the two target-force differences (P = 0.618) in old adults. These findings contrast with those of young adults and indicate that the integration of synaptic input during sustained contractions differs between young and old adults.     

Muscular fatigue and rate of tension development

Summary The effects of long-term fatigue upon maximal force and peak rate of tension development (PRTD) (dF/dt max) are studied in man (elbow flexors), in the rat (pseudo-isolated gastrocnemius muscle) and in the frog (isolated sartorius muscle). The muscles are fatigued by voluntary anisometric anisotonic contractions against an elastic resistance in man, and by maximal tetanic contractions in the frog and the rat. In man, the excitation level of the muscle is controlled by the integrated surface EMG of the biceps brachii. In the animals, the muscles are stimulated by a neurostimulator. The PRTD and the maximal isometric force are measured during fatigue tests.In man, frog and rat, the maximal voluntary isometric torque or the maximal force and the PRTD decrease initially more or less rapidly according to the power developed during the fatigue process, and then less rapidly. The relationship between PRTD and maximal force is linear in the animals and curvilinear in man.The variations of maximal force and PRTD are discussed in relation to the level of excitation of the muscles and of the composition in different motor units types and their spatio-temporal recruitment. From a biomechanical point of view, it seems necessary to study the behavior of the series elastic component during the evolution of long term fatigue.     

Strategies for muscle activation during isometric torque generation at the human elbow

1. We studied the patterns of electromyographic (EMG) activity in elbow muscles of 14 normal human subjects. The activity of five muscles that act in flexion-extension and forearm supination-pronation was simultaneously recorded during isometric voluntary torque generation, in which torques generated in a plane orthogonal to the long axis of the forearm were voluntarily coupled with torques generated about the long axis of the forearm (i.e., supination-pronation). 2. When forearm supination torques were superimposed on a background of elbow flexion torque, biceps brachii activity increased substantially, as expected; however, brachioradialis and brachialis EMG levels decreased modestly, a less predictable outcome. The pronator teres was also active during pure flexion and flexion coupled with mild supination (even though no pronation torque was required). This was presumably to offset inappropriate torque contributions of other muscles, such as the biceps brachii. 3. When forearm supination torque was superimposed on elbow extension torque, again the biceps brachii was strongly active. The pronator teres also became mildly active during extension with added pronation torque. These changes occurred despite the fact that both the pronator and biceps muscles induce elbow flexion. 4. In these same elbow extension tasks, triceps brachii activity was also modulated with both pronation or supination loads. It was most active during either supination or pronation loads, again despite the fact that it has no mechanical role in producing forearm supination-pronation torque. 5. Recordings of EMG activity during changes in forearm supination-pronation angle demonstrated that activation of the biceps brachii followed classic length-tension predictions, in that less EMG activity was required to achieve a given supination torque when the forearm was pronated (where biceps brachii is relatively longer). On the other hand, EMG activity of the pronator teres did not decrease when the pronator was lengthened. Triceps EMG was also more active when the forearm was supinated, despite its having no direct functional role in this movement. 6. Plots relating EMG activity in biceps brachii, brachialis, and brachioradialis at three different forearm positions revealed that there was a consistent positive near-linear relationship between brachialis and brachioradialis and that biceps brachii is often most active when brachioradialis and brachialis are least active. 7. We argue that, for the human elbow joint at least, fixed muscle synergies are rather uncommon and that relationships between muscle activities are situation dependent.(ABSTRACT TRUNCATED AT 400 WORDS)