The fatigability of two agonistic muscles in human isometric voluntary submaximal contraction: an EMG study

Summary The recruitment and firing rate of biceps brachii (BB) and brachioradialis (BR) motor units (MUs) were studied in the course of fatiguing isometric contractions at 20%–30% of maximal voluntary contraction (MVC). MU recruitment generally occurred throughout the maintained contraction and was similar for BB and BR muscles. Newly recruited MUs started to discharge in the form of bursts, the duration of which increased until a continuous rhythmical firing was achieved. Within each burst, the first interval between two consecutive discharges was usually the shortest. MU threshold was lowered just after the limit time of the maintained contraction. The MU's firing rate either increased or remained stable as a function of the elapsed time. It is concluded that (1) in fatiguing isometric contractions at 20%–30% MVC contractile failure is mainly compensated for by MU recruitment and a lowered MU threshold and (2) differences between in surface changes in the electromyogram of BB and BR muscles cannot easily be explained by related differences in MU firing rate and recruitment.     

Motor unit recruitment and rate coding in response to fatiguing shoulder abductions and subsequent recovery

The purpose of the present study was to investigate motor unit (MU) recruitment and firing rate, and the MU action potential (MUAP) characteristics of the human supraspinatus muscle during prolonged static contraction and subsequent recovery. Eight female subjects sustained a 30° shoulder abduction, requiring 11–12% of maximal voluntary contraction (MVC), for 30 min. At 10 and 30 min into the recovery period, the shoulder abduction was repeated for 1 min. The rating of perceived exertion for the shoulder region increased to “close to exhaustion” during the prolonged contraction, and the surface electromyography (EMG) recorded from the deltoid and trapezius muscles showed signs of local muscle fatigue. From the supraspinatus muscle, a total of 23,830 MU firings from 265 MUs were identified using needle electrodes. Of the identified MUs, 95% were continuously active during the 8-s recordings, indicating a low degree of MU rotation. The mean (range) MU firing rate was 11.2 (5.7–14.5) Hz, indicating the relative force contribution of individual MUs to be larger than the overall mean shoulder muscle load. The average MU firing rate remained stable throughout the prolonged abduction, although firing rate variability increased in response to fatigue. The average concentric MUAP amplitude increased by 38% from the beginning (0–6 min) to the end (24–29 min) of the contraction period, indicating recruitment of larger MUs in response to fatigue. In contrast, after 10 min of recovery the average MU amplitude was smaller than seen initially in the prolonged contraction, but not different after 30 min, while the MU firing rate was higher during both tests. In conclusion, MU recruitment plays a significant role during fatigue, whereas rate coding has a major priority during recovery. Furthermore, a low degree of MU rotation in combination with a high relative load at the MU level may imply a risk of overloading certain MUs during prolonged contractions. Accepted: 6 June 2000     

Motor unit firing behavior in human arm flexor muscles during sinusoidal isometric contractions and movements

Simultaneous recordings of action potentials (APs) of multiple single motor units (MUs) were obtained in brachialis and biceps (caput breve) muscles during sinusoidally modulated isometric contractions of elbow flexor muscles and during sinusoidal flexion/extension movements in the elbow against a preload in the extension direction. The results show that MUs typically fire in one short burst for each sinusoidal cycle. The mean phase lead of the bursts of APs relative to a sinusoidally modulated isometric torque in the elbow joint or relative to sinusoidal movements in the elbow increases gradually with frequency. The increase of the mean phase lead during isometric contractions was very similar for all MUs and could be explained well by modeling the force production of MUs with a second-order linear low-pass system. For sinusoidal flexion/extension movements each MU reveals a specific, reproducible phase lead as a function of frequency. However, there is a large variability in phase behavior between MUs. Also, the modulation of the firing rate for sinusoidal isometric contractions versus sinusoidal movements appeared to be different for various MUs. In simultaneous recordings some MUs clearly revealed a larger firing rate in each burst for movements relative to isometric contractions, whereas other MUs revealed a smaller firing rate. This suggests that some MUs are preferentially activated during movements whereas others are preferably activated during isometric contractions. The results demonstrate task-dependent changes in the relative activation of MUs within a single muscle for sinusoidal isometric contractions and movements. Received: 18 November 1996 / Accepted: 3 April 1997     

Discharge properties of primate forearm motor units during isometric muscle activity

Activity of single motor units (MUs) was recorded in forelimb muscles of rhesus macaques while they generated isometric ramp-and-hold torques about the wrist. Multiunit electromyographic (EMG) activity was recorded from 10-12 identified flexor and extensor muscles of the wrist and digits with implanted EMG wire electrodes. Single MUs from these muscles were recorded with a remotely controlled tripolar microelectrode array. The parent muscle of each MU was determined by compiling MU-triggered averages of multiunit EMGs. The MU firing patterns during the isometric task were determined from response histograms aligned with change in torque. At moderate torque levels, MUs (n = 86) exhibited four types of discharge patterns during the ramp-and-hold trajectory: phasic-tonic (23%), tonic (33%), decrementing (39%), and phasic (5%). Phasic-tonic MUs exhibited a phasic burst of activity during the torque ramp which exceeded the firing rate during the static hold period. Both phasic-tonic and tonic MUs exhibited a constant mean firing rate during the hold period; the discharge of decrementing MUs gradually decreased during the static hold. Phasic MUs fired only during the change in force. The relation between MU firing rate and torque was investigated as the monkeys generated responses of different levels of static torque during the hold period. Mean firing rate during the hold was found to be proportional to static torque up to moderate torque levels, where it reached a maximum. In the linear range, the mean rate-torque slope was 3.4 +/- 1.9 imp/s per 10(5) dyn . cm (n = 9).     

The influence of experimental muscle pain on motor unit activity during low-level contraction

In the present study we compared motor unit (MU) activity in a painful extensor carpi ulnaris (ECU) muscle to that of a pain-free control. According to the pain adaptation model the activity of the painful ECU muscle may be inhibited and its antagonist activity increased during wrist extension performed as a pre-defined low-force ramp. The pre-defined low force may then be maintained by increased activity in the pain-free synergist muscles such as the extensor carpi radialis (ECR) muscle. Nine females (31–47 years old) participated in the study. Maximal voluntary contraction (MVC) of the wrist extensors was performed. A catheter was inserted into the ECU muscle to allow the injection of hypertonic saline to evoke muscle pain, and a concentric needle was inserted for the recording of MU activity. Surface electromyograms were recorded from a synergist and an antagonist (ECR and flexor carpi radialis) to the painful ECU muscle. A force ramp of isometric wrist extensions up to 10% MVC, with a force increase of 1% MVC · s⁻¹, were performed followed by 60 s of sustained contraction at 10% MVC. The number of MUs recruited was almost identical for baseline and with pain, and no effect of experimental muscle pain was found on the properties of the MUs (amplitude, area) or their firing characteristics (mean firing rate, firing variability) during low-force ramp contraction. During the sustained 10% MVC, no effect of pain was found for concentric or surface EMG of the forearm muscles. At low force levels no pain-induced modulations were found in MU activity, when the mechanical condition was similar to that of a control situation. Accepted: 30 May 2000     

Effect of experimental muscle pain on motor unit firing rate and conduction velocity

The aim of this human study was to investigate the relationship between experimentally induced muscle pain intensity (i.e., amount of nociceptive activity) and motor unit (MU) firing decrease and MU conduction velocity (CV). In 12 healthy subjects, nociceptive afferents were stimulated in the right tibialis anterior muscle by three intramuscular injections of hypertonic saline (0.2, 0.5, and 0.9 ml) separated by 140 s. The subjects performed six isometric contractions (20 s long) at 10% of the maximal voluntary contraction during the experimental muscle pain. The same set of six contractions was performed without any infusion before the painful condition on the right leg. The procedure was repeated for the left leg with infusion of isotonic (nonpainful) saline. Intramuscular and surface electromyographic (EMG) signals were collected to assess MU firing rate and CV. The firing rate of the active MUs [range: 7.4-14.8 pulses/s (pps)] did not change significantly in the three control conditions (without infusion for the right and left leg and with infusion of isotonic saline in the left leg). There was, on the contrary, a significant decrease (on average, mean +/- SE, 1.03 +/- 0.21 pps) of the firing rates during the painful condition. Moreover, MU firing rates were inversely significantly correlated with the subjective scores of pain intensity. Single MU CV was 3.88 +/- 0.03 m/s (mean +/- SE, over all the MUs) with no statistical difference among any condition, i.e., the injection of hypertonic saline did not alter the muscle fiber membrane properties of the observed MUs. Progressively increased muscle pain intensity causes a gradual decrease of MU firing rates. This decrease is not associated with a change in MU membrane properties, indirectly assessed by CV. This study demonstrates a central inhibitory motor control mechanism with an efficacy correlated to the nociceptive activity.     

Human motor unit activity during concentric and eccentric movements

Single motor units (MUs) activity was investigated in human m. biceps brachii during movements against an elastic load. A total of sixty-five MUs were studied by means of subcutaneously placed fine-wire branched electrodes. Subjects were asked to perform active shortening and lengthening of the muscle with approximately constant velocities at two different speeds--slow and fast. Both recruitment (RT) and decruitment (DT) thresholds of MU were found to be lower in movement with higher velocity. The recruitment order of MUs was approximately one and the same during concentric movements with a different but constant velocity. The firing onset of MUs is organized so that the peak of the first twitch contraction occurs at approximately the same force level irrespective of how fast the movement is. In contrast, during the eccentric movements the peak of the last twitch contraction of MU occurs at different torque levels depending on the velocity. The decruitment of the MUs during eccentric movement was in a reverse order to their recruitment during concentric movements. Generally, at one and the same velocity the RT of a given MU was lower than DT. Nevertheless, the peaks of the first and the last twitch contractions during concentric and eccentric movements with one and the same velocity occurred at approximately one and the same torque level.     

Influence of the interimpulse interval on the propagation velocity of the motor unit potentials

The influence of the rate of firing of separate human motor units (MUs) from m. biceps brachii on the propagation velocity of the extraterritorial MU potentials was investigated. The experiments were carried out under normal physiological conditions--different level of isometric voluntary activity and different rate of firing--respectively. The subjects succeeded to keep 3-5 different levels of relatively constant rate of firing with mean value of the interimpulse intervals ranging from 67.8 to 183.2 ms. Wire subcutaneous branched electrodes and conventional bipolar wire electrodes were used to separate potentials from single motor units and as a trigger to average surface electromyographic (EMG) signals. MUs with superficially and deep lying muscle fibers were investigated. The propagation velocity of the potentials of superficially lying MUs was calculated from the time shift between the EMG signals picked up by means of two monopolar surface electrodes placed along the direction of the muscle fibers. For deep lying MUs the changes in the propagation velocity were estimated indirectly by the changes in the duration of the extraterritorial MU potentials. No systematic relationship between the rate of firing and the velocity of propagation was found.     

Task-related behaviour of motor units in the human temporalis muscle

Muscle activity patterns in some complex human jaw muscles appear to be task sensitive. However, it is presently uncertain how changes in motor task affect motor unit (MU) behaviour in the human temporalis muscle. In this study, activity was recorded from 40 MUs in the anterior region of the muscle. The lowest sustainable firing frequency (LSFF) was reached by slow increases and decreases in firing rate, then firing was maintained at the lowest possible rate without significant pauses. An array of consecutive interspike intervals (ISI) were sampled digitally and used to measure the LSFF for each task associated with the MU. In a controlled paradigm, MU reflex inhibition was measured during the performance of different tasks. Single electrical pulses of non-noxious intensity were delivered to the gingiva near the maxillary canine tooth. During continuous MU firing at a controlled firing frequency of 10 Hz, series of pulses were delivered with increasing delays, after preselected spikes. The MUs fired continuously during the performance of 1–4 postural and tooth-contact tasks. There were significant differences in LSFFs between tasks in those MUs associated with multiple tasks. In the reflex study, all MUs were inhibited, but the magnitude of the inhibition was highly task dependent. Thus, both LSFF and reflex inhibition of temporalis MUs appear to vary with the motor task and are sensitive to the position of the jaw and the direction and location of tooth contact along the tooth row. This behaviour most likely reflects task-related changes in output from orofacial and muscle afferents.     

Decomposition of surface EMG signals

This report describes an early version of a technique for decomposing surface electromyographic (sEMG) signals into the constituent motor unit (MU) action potential trains. A surface sensor array is used to collect four channels of differentially amplified EMG signals. The decomposition is achieved by a set of algorithms that uses a specially developed knowledge-based Artificial Intelligence framework. In the automatic mode the accuracy ranges from 75 to 91%. An Interactive Editor is used to increase the accuracy to > 97% in signal epochs of about 30-s duration. The accuracy was verified by comparing the firings of action potentials from the EMG signals detected simultaneously by the surface sensor array and by a needle sensor. We have decomposed up to six MU action potential trains from the sEMG signal detected from the orbicularis oculi, platysma, and tibialis anterior muscles. However, the yield is generally low, with typically < or = 5 MUs per contraction. Both the accuracy and the yield should increase as the algorithms are developed further. With this technique it is possible to investigate the behavior of MUs in muscles that are not easily studied by needle sensors. We found that the inverse relationship between the recruitment threshold and the firing rate previously reported for muscles innervated by spinal nerves is also present in the orbicularis oculi and the platysma, which are innervated by cranial nerves. However, these two muscles were found to have greater and more widespread values of firing rates than those of large limb muscles.     

10 Hz periodic component influences lower frequency component of the physiological tremor at low force levels

A positive correlation has been reported between the amplitudes of the 10 Hz and lower frequency components of the physiological tremor (PT) at low force levels, though the generation mechanisms based on motor unit (MU) firing properties are different. This study aimed to investigate the causal relation between these fluctuations. A computer simulation was performed to alter the fluctuation intensity, which enabled manipulation of MU firing properties. Two types of MU contributions to synchronization activity were considered to influence the intensity of the 10 Hz PT: (1) number of MUs involved in synchronization and (2) synchrony between MUs. The impact of oscillatory excitatory input from the central nervous system on the generation of the 10 Hz PT was also evaluated. The results showed that the lower frequency fluctuation (LF fluctuation) was influenced by the number of MUs contributing to the 10 Hz PT amplitude. The synchrony between MUs and the oscillatory excitatory input had no influence on the LF fluctuation. In conclusion, MU synchronization in a certain frequency range increased the fluctuations not only at the synchronizing frequency but also at lower frequencies, and the number of MUs involved in synchronization was a plausible factor to explain the correlation between the 10 Hz and LF fluctuations.     

Correlation-based decomposition of surface electromyograms at low contraction forces

The paper studies a surface electromyogram (SEMG) decomposition technique suitable for identification of complete motor unit (MU) firing patterns and their motor unit action potentials (MUAPs) during low-level isometric voluntary muscle contractions. The algorithm was based on a correlation matrix of measurements, assumed unsynchronised (uncorrelated) MU firings, exhibited a very low computational complexity and resolved the superimposition of MUAPs. A separation index was defined that identified the time instants of an MU's activation and was eventually used for reconstruction of a complete MU innervation pulse train. In contrast with other decomposition techniques, the proposed approach worked well also when the number of active MUs was slightly underestimated, if the MU firing patterns partly overlapped and if the measurements were noisy. The results on synthetic SEMG show 100% accuracy in the detection of innervation pulses down to a signal-to-noise ratio (SNR) of 10 dB, and 93±4.6% (mean± standard deviation) accuracy with 0 dB additive noise. In the case of real SEMG, recorded with an array of 61 electrodes from biceps brachii of five subjects at 10% maximum voluntary contraction, seven active MUs with a mean firing rate of 14.1 Hz were identified on average.     

Comparison of F-waves of motor unit action potentials activated during voluntary contraction

The system for classifying F-waves was developed to study the properties of F-wave and to compare single motor unit (MU) F-waves with motor unit action potentials (MUAPs) activated during voluntary contraction. The F-waves evoked by submaximal stimulation as well as the EMG signals during voluntary contraction at 6 levels of 10-100% of maximum voluntary contraction (MVC) were measured in the tibialis anterior muscles of 3 healthy volunteers. Nine channel F-wave waveforms in a selected electrode array were classified using a template-matching method. After the detection procedure of MUAPs in voluntary EMG signals, the MUAPs were also classified by the same method. Most of the F-waves (88.4%) were composed of a single MUAP. The numbers of MU classified from single MU F-waves in 3 subjects were 12, 12 and 15, and the numbers of MU classified from the voluntary EMG signals at 6 contraction levels were 20, 27 and 24, respectively. A total of 26 single MU F-waves were identified with the MUs extracted from the data during voluntary contractions. The results suggest that the F-waves are composed of a population of the MUs, which are recruited at a wide range of contraction levels. The classification procedures of F-waves and voluntary EMG signals have made it possible to recognize the same MU in both signals and to analysis the firing thresholds of F-waves.     

Task dependence of human masseter motor unit reflex behaviour

Summary Motor unit (MU) firing frequency is an important determinant of reflex inhibition in the human jaw muscles. Masseter MUs may be driven steadily by various intraoral tasks, but their lowest sustainable firing frequency varies according to task. In this study we examined the effect of task on masseter MU reflex behaviour under controlled conditions, in which the prestimulus MU firing frequency and stimulation were constrained. All MUs tested were inhibited by a non-noxious electrical stimulus applied to the oral mucosa, but there were significant differences in the magnitude of single MU inhibition depending on the task employed to drive the MUs. It appears that single masseter MU reflex behaviour can alter according to task, even when the prestimulus excitation of the masseter motoneuron pool is apparently constant. This suggests that masseter MU reflex behaviour may be modulated by task-related peripheral afferent input.     

Physiology of the fasciculation potentials in amyotrophic lateral sclerosis: which motor units fasciculate?

We set out to study whether in amyotrophic lateral sclerosis (ALS) fasciculation potentials (FPs) arise from the most excitable motor units (MUs). We studied 70 patients with ALS and 18 subjects with benign fasciculation syndrome (BFS). Of the 56 eligible ALS patients, 31 had signs of reinnervation in the right first dorsal interosseous muscle selected for study, and 25 did not. Two needle electrodes were placed in different MUs in each studied muscle. We defined the most excitable MU as that first activated by minimal voluntary contraction. In muscles without reinnervation, the recording site with most frequent FPs had a higher probability of showing the first recruited MU (p < 0.001). No significant difference was found in other patients or in BFS subjects. In very early affected muscles, fasciculating MUs are the most likely to be recruited volitionally. This probably represents hyperexcitability at lower motor neuronal level.     

Motor unit firing during and after voluntary contractions of human thenar muscles weakened by spinal cord injury

Spinal cord injury may change both the distribution and the strength of the synaptic input within a motoneuron pool and therefore alter force gradation. Here, we have studied the relative contributions of motor unit recruitment and rate modulation to force gradation during voluntary contractions of thenar muscles performed by five individuals with chronic (>1 yr) cervical spinal cord injury. Mean +/- SD thenar unit firing rates were low during both steady-level 25% (8.3 +/- 2.2 Hz, n = 27 units) and 100% maximal voluntary contractions (MVCs, 9.2 +/- 3.1 Hz, n = 23 units). Thus modest rate modulation, or a lack of it in some units, was seen despite an average fourfold increase in integrated surface electromyographic activity and force. During ramp contractions, units were recruited at 5.7 +/- 2.5 Hz, but still only reached maximal firing rates of 12.8 +/- 4.9 Hz. Motor units were recruited up to 85% of the maximal force achieved (14.6 +/- 5.6 N). In contrast, unit recruitment in control hand muscles is largely complete by 30% MVC. Thus, during voluntary contractions of thenar muscles weakened by cervical spinal cord injury, motor unit rate modulation was limited and recruitment occurred over a wider than usual force range. Those motor units that were stopped voluntarily had significantly lower derecruitment versus recruitment thresholds. However, 8 units (24%) continued to fire long after the signal to end the voluntary contraction at a mean frequency of 5.9 +/- 0.8 Hz. The forces generated by this prolonged unit activity ranged from 0.3 to 7.2% maximum. Subjects were unable to stop this involuntary unit activity even with the help of feedback. The mechanisms that underlie this prolonged motor unit firing need to be explored further.     

Number and size of motor units in thenar muscles

The number and size of motor units (MUs) in the thenar muscles of 10 fresh adult cadavers (33-74 years old) were estimated by histological methods. The average number of MUs was 161 +/- 26 and the MU size was 93 +/- 11.5. Adductor pollicis showed a significantly greater MU size. The number of MUs in our histological study was in agreement with the number reported in previous studies using multiple point stimulation, the method currently used in the clinical investigation of neuromuscular disorders.     

Proportional enlargement of motor units after partial denervation of cat triceps surae muscles.

1. To determine the capacity of motoneurons to increase their motor unit (MU) size by collateral sprouting and to assess this capacity in relation to the size of the motor nerve, we partially denervated soleus, lateral gastrocnemius (LG), and medial gastrocnemius (MG) muscles in adult and neonatal cats. Isometric force and extracellular nerve potentials were recorded from > or = 7% of the remaining MUs, 2.5-18 mo later. S1 or L7 roots were sectioned unilaterally and the number of remaining MUs was quantified by use of charge and force measurements. 2. The mean unit force increased inversely with MU number in partially denervated muscles, but the increase was less than predicted for extensive denervations (> or = 90%). The same enlargement of MU size occurred whether muscles were partially denervated in neonatal or adult animals. 3. The force distribution of MUs in partially denervated muscles was similar to normal but was shifted to larger force values in direct proportion to the extent of partial denervation (PD). All MUs increased in size by the same factor to preserve the normal force distribution. 4. Normal size relationships among force, contractile speed, and axon potential amplitude were observed for MUs in partially denervated muscles. Because changes in muscle fiber size could not account for the increase in unit force, these data show that increase in MU size, with respect to unit force and innervation ratio (muscle fibers per motoneuron), is proportional to the size of the motor nerve. 5. Enlargement of MU size in partially denervated muscles did not have a retrograde effect on nerve fiber caliber because axon potential amplitude and conduction velocity were not changed after PD. 6. Under conditions of extensive PD (> 85%), regenerated nerves from the cut spinal root reinnervated the gastrocnemius muscles. It is likely that nerves supplied muscle fibers that were not innervated by sprouts from nerves in the uncut root as well as displacing sprouts from terminals in extensively enlarged MUs. 7. We conclude that all motoneurons within a motor pool compensate for partial nerve injuries by collateral sprouting and that enlargement of MU size is a function of motor nerve size, consistent with Henneman's size principle.     

"Facial" and standard concentric needle electrodes are not interchangeable

Motor unit action potentials (MUAPs) were recorded using a standard concentric needle (SCN), a "facial" concentric needle (FCN) and a monopolar needle (MN) in the biceps brachii and first dorsal interosseous manus muscles of 7 normal subjects. For each muscle, the MUAP durations were similar for all electrodes. However, the FCN electrode more frequently registered high-amplitude MUAPs compared to the SCN electrode. Hence, the FCN and SCN needles should not be considered interchangeable in assessment of EMG signal amplitude. Although, the pattern of changes in amplitude and duration on FCN and MN recordings is similar, the electrodes have different uptake areas.     

EMG activation patterns during force production in precision grip. III. Synchronisation of single motor units

Motor unit (MU) synchronisation during isometric force production in the precision grip was analysed in five subjects performing a visually guided steptracking motor task with three different force levels. With this aim multi-unit electromyographic (EMG) activity of 14 intrinsic and extrinsic finger muscles from 15 experimental sessions was decomposed into the potentials of single MUs. The behaviour of 62 intrinsic and 30 extrinsic MUs in the motor task was quantified. Most MUs displayed a positive correlation between firing rate and grip force. Compared to MUs in extrinsic muscles, intrinsic MUs had steeper regression lines with negative intercepts indicating higher force sensitivity and higher recruitment thresholds. A cross-correlation analysis was performed for 69 intra- and 166 intermuscular MU pairs while steady grip force was exerted at the three force levels. Synchronisation, for at least one force level, was found in 78% of the intra- and 45% of the intermuscular pairs. The occurrence of synchronisation was not stable over the force range tested. Factors influencing the fluctuations in occurrence and strength of synchronisation were investigated. Force increase was not paralleled by increased synchronisation; in contrast, in most MU pairs, especially intermuscular pairs, synchronisation occurred preferentially at the lower force levels. The recruitment threshold appeared to play a determining role in synchronisation: the more similar the thresholds of two MUs, the greater the probability of them being synchronised at this force level. Synchronised MUs fired on average at a lower frequency than non-synchronised ones. Finally, synchronisation at the multi-unit EMG level does not indicate that all underlying MUs are synchronised, nor does the absence of temporal coupling at the multi-unit level indicate that none of the MUs is synchronised.