Activity of single motor units in attention-demanding tasks: firing pattern in the human trapezius muscle

Activity of single motor units in relation to surface electromyography (EMG) was studied in 11 subjects in attention-demanding work tasks with minimal requirement of movement. In 53 verified firing periods, single motor units fired continuously from 30 s to 10 min (duration of the experiment work task) with a stable median firing rate in the range of 8–13 Hz. When the integrated surface EMG were stable, the motor units identified as a rule were continuously active with only small modulations of firing rate corresponding to low-amplitude fluctuations in surface EMG. Marked changes in the surface EMG, either sudden or gradual, were caused by recruitment or derecruitment of motor units, and not by modulations of the motor unit firing rate. Motor unit firing periods (duration 10 s-35 s) in low-level voluntary contractions (approximately 1%–5% EMG_max) performed by the same subjects showed median firing rates (7–12 Hz) similar to the observations in attention-related activation.     

Influence of motor units recruitment and firing rate on the soundmyogram and EMG characteristics in cat gastrocnemius

The separate contributions of the recruitment level and of the firing rate of the motor units on the soundmyogram and electromyogram time domain parameters were investigated during stimulation of the motor nerve of the cat gastrocnemius muscle. Upon orderly increase in the number of active motor units at a fixed firing rate, both the peak to peak amplitude (P-P_max) and the root mean square (RMS) of the sound myogram increased. At full recruitment the increase in firing rate from 2.5 to 50 Hz induced an exponential decline in the P-P_max. The RMS, however, followed this trend only from 15 to 50 Hz while showing an increase from 2.5 to 10 Hz. During simultaneous changes of recruitment and firing rate, the effect of increasing the number of motor units on the P-P_max and RMS is dampened by the increasing firing rate. The peak to peak amplitude of the EMG compound action potential increased with the number of active motor units. Moreover, its amplitude was not influenced by the firing rate. The EMG RMS, however, increases as a function of the firing rate. The results indicate that both the number and the firing rate of the active motor units contribute to the determination of the soundmyogram characteristics. Moreover, the peculiar changes of the soundmyogram time domain properties, compared to the ones of the EMG, allow one to differentiate the influence of the motor units number and firing rate on the electrical and mechanical performance of the muscle when stimulated.     

Motor unit activation patterns during concentric wrist flexion in humans with different muscle fibre composition

Muscle activity was recorded from the flexor carpi radialis muscle during static and dynamic-concentric wrist flexion in six subjects, who had exhibited large differences in histochemically identified muscle fibre composition. Motor unit recruitment patterns were identified by sampling 310 motor units and counting firing rates in pulses per second (pps). During concentric wrist flexion at 30% of maximal exercise intensity the mean firing rate was 27 (SD 13) pps. This was around twice the value of 12 (SD 5) pps recorded during sustained static contraction at 30% of maximal voluntary contraction, despite a larger absolute force level during the static contraction. A similar pattern of higher firing rates during dynamic exercise was seen when concentric wrist flexion at 60% of maximal exercise intensity [30 (SD 14) pps] was compared with sustained static contraction at 60% of maximal voluntary contraction [19 (SD 8) pps]. The increase in dynamic exercise intensity was accomplished by recruitment of additional motor units rather than by increasing the firing rate as during static contractions. No difference in mean firing rates was found among subjects with different muscle fibre composition, who had previously exhibited marked differences in metabolic response during corresponding dynamic contractions. It was concluded that during submaximal dynamic contractions motor unit firing rate cannot be deduced from observations during static contractions and that muscle fibre composition may play a minor role. Accepted: 5 May 1998     

Firing rates of motor units in human vastus lateralis muscle during fatiguing isometric contractions.

We investigated the firing rate of motor units in the vastus lateralis muscle in five healthy young men (mean = 21.4 yr, SD = 0.9) during a sequence of isometric constant-torque contractions repeated to exhaustion. The contractions were sustained at 20% of the maximal voluntary level, measured at the beginning of the test sequence. Electromyographic (EMG) signals were recorded via quadrifilar fine-wire electrodes and subsequently decomposed into their constituent motor unit action potentials to obtain the motor unit firing times. In addition, we measured the whole muscle mechanical properties during the fatigue task using electrical stimulation. The firing rate of motor units first decreased within the first 10-20% of the endurance time of the contractions and then increased. The firing rate increase was accompanied by recruitment of additional motor units as the force output remained constant. The elicited twitch and tetanic torque responses first increased and then decreased. The two processes modulated in a complementary fashion at the same time. Our data suggest that, when the vastus lateralis muscle is activated to maintain a constant torque output, its motoneuron pool receives a net excitatory drive that first decreases to compensate for the short-lived potentiation of the muscle force twitch and then increases to compensate for the diminution of the force twitch. The underlying inverse relationship between the firing rate and the recruitment threshold that has been reported for nonfatigued contractions is maintained. We, therefore, conclude that the central nervous system control of vastus lateralis motor units remains invariant during fatigue in submaximal isometric isotonic contractions.     

Effects of Barbell Deadlift Training on Submaximal Motor Unit Firing Rates for the Vastus Lateralis and Rectus Femoris

Previous investigations that have studied motor unit firing rates following strength training have been limited to small muscles, isometric training, or interventions involving exercise machines. We examined the effects of ten weeks of supervised barbell deadlift training on motor unit firing rates for the vastus lateralis and rectus femoris during a 50% maximum voluntary contraction (MVC) assessment. Twenty-four previously untrained men (mean age  = 24 years) were randomly assigned to training (n = 15) or control (n = 9) groups. Before and following the intervention, the subjects performed isometric testing of the right knee extensors while bipolar surface electromyographic signals were detected from the two muscles. The signals were decomposed into their constituent motor unit action potential trains, and motor units that demonstrated accuracy levels less than 92.0% were not considered for analysis. One thousand eight hundred ninety-two and 2,013 motor units were examined for the vastus lateralis and rectus femoris, respectively. Regression analyses were used to determine the linear slope coefficients (pulses per second [pps]/% MVC) and y-intercepts (pps) of the mean firing rate and firing rate at recruitment versus recruitment threshold relationships. Deadlift training significantly improved knee extensor MVC force (Cohen''s d = .70), but did not influence force steadiness. Training had no influence on the slopes and y-intercepts for the mean firing rate and firing rate at recruitment versus recruitment threshold relationships. In agreement with previous cross-sectional comparisons and randomized control trials, our findings do not support the notion that strength training affects the submaximal control of motor units.     

The role of motor unit rate modulation versus recruitment in repeated submaximal voluntary contractions performed by control and spinal cord injured subjects.

The relative roles of motor unit firing rate modulation and recruitment were evaluated when individuals with cervical spinal cord injury (SCI) and able-bodied controls performed a brief (6 s), 50% maximal voluntary contraction (50% MVC; target contraction) of triceps brachii every 10 s until it required maximal effort to achieve the target force. Mean (+/-SD) endurance times for SCI and control subjects were 34+/-26 and 15+/-5 min, respectively, at which point significant reductions in maximal triceps force had occurred. Twitch occlusion analysis in controls indicated that force declines resulted largely from peripheral contractile failure. In SCI subjects, triceps surface EMG and motor unit potential amplitude declined in parallel suggesting failure at axon branch points and/or alterations in muscle membrane properties. The force of low threshold units, measured by spike-triggered averaging, declined in SCI but not control subjects, suggesting that higher threshold units fatigued in controls. Central fatigue was also obvious after SCI. Mean (+/-SD) MVC motor unit firing rates declined significantly with fatigue for control (24.6+/-7.1 to 17.3+/-5.1Hz), but not SCI subjects (25.9+/-12.7 to 20.1+/-9.7Hz). Unit firing rates were unchanged during target contractions for each subject group, but with the MVC rate decreases, units of SCI and control subjects were activated intensely at endurance time (88% and 99% MVC rates, respectively). New unit recruitment also maintained the target contractions although it was limited after SCI because many descending inputs to triceps motoneurons were disrupted. This resulted in sparse EMG, even during MVCs, but allowed the same unit to be recorded throughout. These EMG data showed that both unit recruitment and rate modulation were important for maintaining force during repeated submaximal intermittent contractions of triceps brachii muscles performed by SCI subjects. Similar results were found for control subjects. Muscles weakened by SCI may therefore provide a useful model in which to directly study motor unit rate modulation and recruitment during weak or strong voluntary contractions.     

Does the frequency content of the surface mechanomyographic signal reflect motor unit firing rates? A brief review.

The purpose of this review is to examine the literature that has investigated the potential relationship between mechanomyographic (MMG) frequency and motor unit firing rates. Several different experimental designs/methodologies have been used to address this issue, including: repetitive electrical stimulation, voluntary muscle actions in muscles with different fiber type compositions, fatiguing and non-fatiguing isometric or dynamic muscle actions, and voluntary muscle actions in young versus elderly subjects and healthy individuals versus subjects with a neuromuscular disease(s). Generally speaking, the results from these investigations have suggested that MMG frequency is related to the rate of motor unit activation and the contractile properties (contraction and relaxation times) of the muscle fibers. Other studies, however, have reported that MMG mean power frequency (MPF) does not always follow the expected pattern of firing rate modulation (e.g. motor unit firing rates generally increase with torque during isometric muscle actions, but MMG MPF may remain stable or even decrease). In addition, there are several factors that may affect the frequency content of the MMG signal during a voluntary muscle action (i.e. muscle stiffness, intramuscular fluid pressure, etc.), independent of changes in motor unit firing rates. Despite the potential influences of these factors, most of the evidence has suggested that the frequency domain of the MMG signal contains some information regarding motor unit firing rates. It is likely, however, that this information is qualitative, rather than quantitative in nature, and reflects the global motor unit firing rate, rather than the firing rates of a particular group of motor units.     

Evidence of self-sustained motoneuron firing in young and older adults.

Motoneurons demonstrate a type of self-sustained firing behavior that seems to be produced by a prolonged period of depolarization caused by intrinsic long-term changes in the motoneuron. Such self-sustained firing behavior has previously been reported in human motor units. The purpose of the present study was to investigate the occurrence of self-sustained firing behavior in older adults. Eight young (mean age 24 yrs) and eight older (mean age 73 yrs) individuals participated in the investigation. While subjects produced light dorsiflexion contractions, a brief vibration stimulus was applied to the tibialis anterior muscle. Motor unit recordings were also obtained from the tibialis anterior muscle. Self-sustained firing behavior was evidenced by the appearance of new motor unit recruitment following vibration, even as the motor units that fired before the vibratory stimulus maintained a steady firing rate. The proportion of motor units exhibiting self-sustained firing activity was similar in both young and older adults (approx. 23% of trials). We conclude that self-sustained firing behavior is a ubiquitous phenomenon that does not seem to be affected by the aging process.     

Single motor unit activity in the diaphragm of cat during pressure breathing

In this study we analyzed the breath-by-breath activity of single motor units in the diaphragm slip of allobarbital-anesthetized cats during quiet breathing and during continuous positive- and negative-pressure breathing. Our objective was to determine whether single motor units, on the basis of their activities, can be separated into discrete subpopulations or whether they fall on a continuum analogous to that of motor units of hindlimb muscles. The firing profiles of each unit were characterized for each pressure level by the onset and peak firing frequencies, onset latency, duration of firing, number of impulses per breath, and minimal frequency, when appropriate. Units with shorter onset latencies had higher peak frequencies, longer firing durations, and increased firing frequencies than did units with longer onset latencies. These comparative relationships persisted even though the activity of every motor unit was altered during pressure breathing. During positive-pressure breathing onset latencies were lengthened, and durations of firing were shortened with little change in onset or peak frequencies. Late units might be silenced. During negative-pressure breathing onset latencies were shortened, and durations of firing were lengthened, sufficiently in some cases to fill the expiratory pause. In addition, previously inactive units were recruited late in inspiration for short, relatively high frequency bursts during inspiration. The results support the concept that the phrenic motoneuron pool is comprised of three discrete subpopulations.     

Motor unit firing behavior during prolonged 50% MVC dorsiflexion contractions in young and older adults

The purpose of this study was to investigate changes in motor unit firing behavior during prolonged contractions in young and older adults. Motor unit activity was recorded from the tibialis anterior of 16 subjects (8 young and 8 older), while they performed isometric dorsiflexion at 50% MVC until task failure. Mean motor unit firing rate, the standard deviation (SD), and coefficient of variation (CV) of the interspike intervals, and number of doublet discharges were calculated for a total of 52 motor units, tracked for an average of 92.9 ± 68.6 s. There was no age-related difference in the time to task failure. A modest decline in firing rate was observed in 71% of the motor units, with no significant age-related difference. The SD and CV of the interspike interval had a positive slope in 65% and 69% of the motor units, respectively, with no significant age-related differences. The number of doublet discharges remained stable throughout the contraction. Both groups exhibited motor unit dropout (discharge cessation) during the contraction. Thus, a fatiguing task producing modest changes in firing rate in young and older adults is accompanied by an appreciable increase in firing rate variability. The incidence of doublet discharges is not increased during fatiguing contractions.     

Effect of the tendon reflex on the silent period of motor units in man

The behavior of motor units functioning under different conditions was investigated during the patellar reflex. The reflex was elicited during regular firing of the motor units in connection with weak sustained voluntary effort without postural change. Under these conditions the firing rate of the motor units serves as a statistical characteristic of threshold: during the maintenance of an assigned level of contraction the mean firing rate of the low-threshold motor units was higher. The greater the mean spontaneous interspike interval of the motor units, the longer the duration of their silent period after reflex muscular contraction. The duration of the silent period of single motor units in many cases exceeded the longest duration of the aggregated silent period on the electromyogram. The instant frequency (the difference between the reciprocals of the mean interspike interval and silent period) was used as a measure of inhibitory action on the motoneuron. Positive correlation was observed between the change in the instant frequency and the spontaneous firing rate of the motor units. Within the population examined, those motoneurons whose frequency was higher (low-threshold) were more inhibited. The combination of spinal factors evoking inhibition of the motoneurons after the tendon reflex and the excitatory supraspinal influences causing recruiting of the motoneurons during voluntary contraction proved more effective under the conditions investigated for the same motoneurons.     

Response linearity determined by recruitment strategy in detailed model of nictitating membrane control

Many models of eyeblink conditioning assume that there is a simple linear relationship between the firing patterns of neurons in the interpositus nucleus and the time course of the conditioned response (CR). However, the complexities of muscle behaviour and plant dynamics call this assumption into question. We investigated the issue by implementing the most detailed model available of the rabbit nictitating membrane response (Bartha and Thompson in Biol Cybern 68:135-143, 1992a and in Biol Cybern 68:145-154, 1992b), in which each motor unit of the retractor bulbi muscle is represented by a Hill-type model, driven by a non-linear activation mechanism designed to reproduce the isometric force measurements of Lennerstrand (J Physiol 236:43-55, 1974). Globe retraction and NM extension are modelled as linked second order systems. We derived versions of the model that used a consistent set of SI units, were based on a physically realisable version of calcium kinetics, and used simulated muscle cross-bridges to produce force. All versions showed similar non-linear responses to two basic control strategies. (1) Rate-coding with no recruitment gave a sigmoidal relation between control signal and amplitude of CR, reflecting the measured relation between isometric muscle force and stimulation frequency. (2) Recruitment of similar strength motor units with no rate coding gave a sublinear relation between control signal and amplitude of CR, reflecting the increase in muscle stiffness produced by recruitment. However, the system response could be linearised by either a suitable combination of rate-coding and recruitment, or by simple recruitment of motor units in order of (exponentially) increasing strength. These plausible control strategies, either alone or in combination, would in effect present the cerebellum with the simplified virtual plant that is assumed in many models of eyeblink conditioning. Future work is therefore needed to determine the extent to which motor neuron firing is in fact linearly related to the nictitating membrane response.     

Spectral analysis of muscular sound during isometric contraction of biceps brachii

The frequency content of muscular sound (MS), detected by placing a contact sensor transducer over the belly of the biceps brachii during 10 isometric contractions of 4 s each [10-100% of maximal voluntary contraction (MVC)] in seven sedentary men, was analyzed by the maximum entropy spectral estimation and the fast Fourier transform methods. With increasing %MVC, the power spectrum of the MS enlarges and tends to be multimodal beyond 30% MVC. Independent of the method, the mean frequency is approximately 11 Hz at the lower tasks, and then it increases up to 15 Hz at 80% MVC and to 22 Hz at 100% MVC. When the effort is increased the relative power in the 15- to 45-Hz bandwidth (range of firing rate of the motor units with fast-twitch fibers) from 20% reaches 55% of the power in the 6- to 45-Hz bandwidth (firing rate range of motor units with slow- and fast-twitch fibers). Our results obtained by the two different modeling approaches confirm the reliability of the sound signal. Moreover, it appears that from the MS the motor unit activation pattern can be retrieved.     

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.     

Amplitude and spectral characteristics of biceps Brachii sEMG depend upon speed of isometric force generation.

In the present study the influence of speed of contraction on the interplay between recruitment and firing rate of motor units (MUs) was assessed. The surface electromyographic (sEMG) signal was recorded in nine healthy subjects from the right biceps brachii using a linear electrode array during ramp isometric contractions (from 0 to 100% of the maximal voluntary force, MVC) at 5, 10, and 20% MVC s(-1) (ramp phase), followed by 10 s of sustained MVC (hold phase). The median frequency (MDF), Root Mean Square (RMS) and conduction velocity (CV) of sEMG, were computed on adjacent epochs covering a force range of 5% MVC each. Full motor unit recruitment (FMUR) point was assessed as the force level at which MDF reached its maximum value; the MDF decay during the hold phase was taken as an index of localized muscle fatigue. At 5% MVC s(-1), FMUR was reached at 52.3% MVC. At 10%MVC s(-1) FMUR was achieved at 58% MVC; while at 20% MVC s(-1) FMUR point was located at 77% MVC, being statistically different from 5 and 10% MVCs(-1) ramps (p<0.05). The MDF decay was steeper at higher speed. CV modifications mirrored those reported for MDF. The RMS increased in a curvilinear fashion and the maximum value was always attained during the hold phase. Our findings suggest that MU recruitment strategies are significantly related to the speed of contraction even in a single muscle.     

A Simulation Study to Examine the Effect of Common Motoneuron Inputs on Correlated Patterns of Motor Unit Discharge

The influence of common oscillatory inputs to the motoneuron pool on correlated patterns of motor unit discharge was examined using model simulations. Motor unit synchronization, in-phase fluctuations in mean firing rates known as ‘common drive’, and the coefficient of variation of the muscle force were examined as the frequency and amplitude of common oscillatory inputs to the motoneuron pool were varied. The amount of synchronization, the peak correlation between mean firing rates and the coefficient of variation of the force varied with both the frequency and amplitude of the common input signal. Values for ‘common drive’ and the force coefficient of variation were highest for oscillatory inputs at frequencies less than 5 Hz, while synchronization reached a maximum when the frequency of the common input was close to the average motor unit firing rate. The frequency of the common input signal for which the highest levels of synchronization were observed increased as motoneuron firing rates increased in response to higher target force levels. The simulation results suggest that common low-frequency oscillations in motor unit firing rates and short-term synchronization result from oscillatory activity in different bands of the frequency spectrum of shared motoneuron inputs. The results also indicate that the amount of synchronization between motor unit discharges depends not only on the amplitude of the shared input signal, but also on its frequency in relation to the present firing rates of the individual motor units.     

An EMG study of functional cortico-motoneuronal connections in humans.

We set out to decompose the EMG signal into its constituent motor unit action potential components to track motor unit firing rates with a high degree of accuracy and extract their average firing rate. We were able to show that this average firing rate tracks the subject's force trajectory from beginning to end. We propose that this average firing rate is a volitional control signal pointing to the existence of a 'volitional unit'. This volitional unit has to do with the projection of a group of functionally related cortico-motoneurons on a group of spinal motoneurons in the motoneuronal pool of a muscle. Our study of motor unit firing patterns during their steady state showed that spinal motoneurons respond to a descending central input in a Gaussian manner. We have further shown that the central drive itself, as represented by the average firing rate of the active motor units, also displays a Gaussian firing behavior. We have also described the existence of a 'translation factor', highly correlated to the motor unit size, which is unique to each spinal motoneuron and determines the motoneuronal response, and its resulting firing rate, to the descending inputs. As for force generation, we have shown that expressing the twitch force of a motor unit in a dynamic fashion using the 'electrotwitch' concept of firing rate x macro area, approximates motor unit force output better and accounts for firing rate related force changes more effectively than force estimates based on the mechanical twitch.     

Motor unit behavior during clonus.

Medial gastrocnemius surface electromyographic activity and intramuscular electromyographic activity were recorded from six individuals with chronic cervical spinal cord injury to document the recruitment order of motor units during clonus. Four subjects induced clonus that lasted up to 30 s while two subjects induced clonus that they actively stopped after 1 min. Mean clonus frequency in different subjects ranged from 4.7 to 7.0 Hz. Most of the 166 motor units recorded during clonus (98%) fired once during each contraction but at slightly different times during each cycle. Other motor units fired during some clonus cycles (1%) or in bursts (1%). When 59 pairs of units were monitored over consecutive clonus cycles (n = 5-89 cycles), only 8 pairs of units altered their recruitment order in some cycles. Recruitment reversals only occurred in units that fired close together in the clonus cycle. These data demonstrate that orderly motor unit recruitment occurs during involuntary contractions of muscles paralyzed chronically by cervical spinal cord injury, providing further support for the importance of spinal mechanisms in the control of human motor unit behavior.     

Motor unit recruitment for dynamic tasks: current understanding and future directions

Skeletal muscle contains many muscle fibres that are functionally grouped into motor units. For any motor task there are many possible combinations of motor units that could be recruited and it has been proposed that a simple rule, the ‘size principle’, governs the selection of motor units recruited for different contractions. Motor units can be characterised by their different contractile, energetic and fatigue properties and it is important that the selection of motor units recruited for given movements allows units with the appropriate properties to be activated. Here we review what is currently understood about motor unit recruitment patterns, and assess how different recruitment patterns are more or less appropriate for different movement tasks. During natural movements the motor unit recruitment patterns vary (not always holding to the size principle) and it is proposed that motor unit recruitment is likely related to the mechanical function of the muscles. Many factors such as mechanics, sensory feedback, and central control influence recruitment patterns and consequently an integrative approach (rather than reductionist) is required to understand how recruitment is controlled during different movement tasks. Currently, the best way to achieve this is through in vivo studies that relate recruitment to mechanics and behaviour. Various methods for determining motor unit recruitment patterns are discussed, in particular the recent wavelet-analysis approaches that have allowed motor unit recruitment to be assessed during natural movements. Directions for future studies into motor recruitment within and between functional task groups and muscle compartments are suggested.     

Synchronization of motor units and its simulation in parallel feedback system

Comparison of the discharge patterns of soleus motor units with associated changes in force exerted by foot during quiet stance have already demonstrated the following facts. In the initial stage of standing, the motor units exhibited stationary and asynchronous discharges. The force showed a sporadic presence of the high frequency oscillation in the 8–10 Hz band. After five to ten minutes of standing, the firing rate of individual motor unit discharges increased to about 10 spikes/sec and discharges of each motor unit were synchronized and phase-locked to each of the accompanying force oscillation. During this transitional stage, the discharges of motor units were characterized by spike dropouts from an otherwise regular spike train. To simulate the changes in the discharge characteristics, we have proposed a parallel feedback model of the stretch reflex arc. This was made of multiple -motoneurons, motor units and muscle spindles. And motor units interact each other through group Ia afferent signals. As a result of simulation, motor units were found to exhibit stationary and asynchronous discharges when feedback gain was kept small. With an increase of feedback gain, the firing rate of individual motor units increased and finally the discharges of them were synchronized. During this transitional stage, the spike dropouts were observed in accordance with the experimental results. The neuronal mechanism of synchronization may partly be explained by the interactions of motor neurons through the above stated parallel feedback system.