The pain-induced decrease in low-threshold motor unit discharge rate is not associated with the amount of increase in spike-triggered average torque.

OBJECTIVE: Activation of nociceptive afferents decreases motor unit discharge rates in static contractions. There is also evidence that during experimental muscle pain the motor unit twitch force increases, which has been hypothesized to compensate for the decrease in discharge rate to maintain constant force. This study examined whether there is an association between the magnitude of change in motor unit discharge rate and the amount of increase in the spike-triggered average torque during experimental muscle pain. METHODS: Sixteen subjects performed three constant-torque isometric ankle dorsi-flexions at 10% of the maximal force (MVC) alternated with two contractions at constant discharge rate of a target motor unit, before and following injection of 0.5 ml of hypertonic (painful) or isotonic (control) saline into the tibialis anterior muscle. RESULTS: The discharge rate of the target unit at 10% MVC decreased following injection of hypertonic saline (P<0.05; mean+/-SD, before: 9.9+/-1.3 pulses per second, pps; after injection: 8.9+/-1.0 pps). The peak of the spike-triggered average torque increased with pain (P<0.05; before: 0.56+/-0.55 mNm; during pain: 0.95+/-1.02 mNm) but the increase was not correlated with the decrease in discharge rate (R=0.08). Propagation velocity and action potential peak-to-peak amplitude did not change with pain. CONCLUSIONS: The pain-induced modifications in the estimated motor unit twitch torque (1) were not caused by changes in muscle fiber action potential, and (2) were not associated with the decrease in discharge rate. SIGNIFICANCE: Maintenance of constant force during static painful contractions is not explained by a matching between changes in contractile and control motor unit properties.     

Muscle fiber conduction velocity related to stimulation rate

Muscle fiber conduction velocity in human biceps brachii muscle, produced by voluntary contraction and by contraction owing to microstimulation of a single motor unit, was measured with surface array electrodes. The conduction velocity of the fibers in the motor unit was calculated from the conduction time of the motor unit action potential along the electrode array and the electrode separation. With voluntary contraction, a conduction velocity of 4.25 +/- 0.43 m/sec (mean +/- S.D., n = 68) was obtained. In recording the surface EMG, the mean firing rate of the motor unit was 15.8 imp/sec (range 6-24 imp/sec). Significantly slower conduction velocity of 3.69 +/- 0.33 m/sec (mean +/- S.D., n = 56) was found after microstimulation (P less than 0.001). The higher the stimulation rate the higher was the conduction velocity. With increasing stimulus rates of 5, 10, 20 and 40 c/sec, the mean and S.D. of the conduction velocity were 3.74 +/- 0.33 m/sec (2.1% increase in the mean value to 1 c/sec stimulus rate), 4.16 +/- 0.37 m/sec (13.6%), 4.35 +/- 0.54 m/sec (18.8%) and 4.80 +/- 0.49 m/sec (31.1%), respectively. The firing rate for voluntary contraction was in the same range of the one obtained with 10-20 c/sec electrical stimulation, conduction velocity was the same in the two conditions. We conclude that measurement of muscle fiber conduction velocity should also be standardized with muscle fiber firing rate.     

Wave properties of action potentials from fast and slow motor units of rats

The purpose of this study was to identify the frequency, conduction velocity, and wavelength of fast and slow motor unit action potentials (MUAPs) from mixed mammalian muscle. Stimulation and blocking pulses to the sciatic nerve produced varying recruitment patterns (confirmed by force measurements) of fast and slow motor units of the medial gastrocnemius of six rats. Myoelectric signals from the muscle were resolved into their intensity in time and frequency space. Slow MUAPs had a mean frequency (+/- SEM) of 183 +/- 8 Hz, conduction velocity of 3.5 +/- 0.6 m s(-1), and wavelength of 19 mm. Fast MUAPs had a mean frequency of 369 +/- 11 Hz, conduction velocity of 6.7 +/- 0.5 m s(-1), and wavelength of 18 mm. Frequency and conduction velocity, but not wavelength, were significantly different between the fast and slow MUAPs. The distinct wave properties of fast and slow MUAPs can thus be used to distinguish action potentials from these motor units, and could be used to determine patterns of motor unit recruitment during locomotion.     

Dependence of the paired motor unit analysis on motor unit discharge characteristics in the human tibialis anterior muscle

The paired motor unit analysis provides in vivo estimates of the magnitude of persistent inward currents (PIC) in human motoneurons by quantifying changes in the firing rate (ΔF) of an earlier recruited (reference) motor unit at the time of recruitment and derecruitment of a later recruited (test) motor unit. This study assessed the variability of ΔF estimates, and quantified the dependence of ΔF on the discharge characteristics of the motor units selected for analysis. ΔF was calculated for 158 pairs of motor units recorded from nine healthy individuals during repeated submaximal contractions of the tibialis anterior muscle. The mean (SD) ΔF was 3.7 (2.5)pps (range -4.2 to 8.9 pps). The median absolute difference in ΔF for the same motor unit pair across trials was 1.8 pps, and the minimal detectable change in ΔF required to exceed measurement error was 4.8 pps. ΔF was positively related to the amount of discharge rate modulation in the reference motor unit (r2 = 0.335; P<0.001), and inversely related to the rate of increase in discharge rate (r2 = 0.125; P<0.001). A quadratic function provided the best fit for relations between ΔF and the time between recruitment of the reference and test motor units (r2 = 0.229, P<0.001), the duration of test motor unit activity (r2 = 0.110, P<0.001), and the recruitment threshold of the test motor unit (r2 = 0.237, P<0.001). Physiological and methodological contributions to the variability in ΔF estimates of PIC magnitude are discussed, and selection criteria to reduce these sources of variability are suggested for the paired motor unit analysis.     

Normal and myopathic propagation of surface motor unit action potentials

With the aid of a computer-assisted multichannel EMG system, the propagation of motor unit action potentials is analysed during isometric voluntary muscular contraction under normal and myopathic conditions. A linear array of 30 surface electrodes is fixed above the biceps brachii muscle, parallel to the longitudinal muscle axis and centered over the end-plate zone. The EMG is simultaneously recorded on all channels and displays the propagation of surface potentials on both sides of the innervation band. The mean muscle fibre conduction velocity is computed by a cross-correlation technique. Five adult patients in a late stage of progressive muscular dystrophy show a highly altered propagation behaviour of motor unit action potentials without a time shift between potentials of adjacent electrodes. A mathematical model is described which predicts such a behaviour and suggests that it must be due to a pathological longitudinal spread of end-plates in this patient group. In 5 boys with Duchenne muscular dystrophy and only moderate impairment of the biceps muscle the mean muscle fibre velocity was reduced (2.81 +/- 0.34 m/sec) compared to 17 healthy subjects (4.42 +/- 0.37 m/sec). Each myopathic patient examined could be separated clearly from the group of healthy subjects on the basis of the surface EMG analysis.     

Myoelectric manifestations of fatigue during exposure to hypobaric hypoxia for 12 days

Lack of oxygen, as occurs at high altitude (HA), leads to a number of adaptive processes in muscle, but their precise nature is unclear. To better understand mechanisms of adaptations of the neuromuscular system to HA, we collected surface electromyographic (EMG) signals during a 12-day stay at 5,050 m above sea level (SL). The aim was to investigate the effect of hypobaric hypoxia on muscle-fiber membrane and motor-unit control properties. Surface EMG signals were recorded from the dominant biceps brachii muscle of six subjects at HA and 3 months after their return to SL. Supramaximal electrical stimuli (25 HZ) were delivered and voluntary isometric contractions at 40 and 80% of maximal voluntary torque were performed in 10 experimental sessions at HA and in 3 at SL. Maximal isometric torque was not altered at HA. Surface EMG spectral frequencies at the beginning of the voluntary contractions were greater at HA than SL. The rates of change of spectral frequencies and conduction velocity during the voluntary contractions were significantly larger at HA than SL. No differences in EMG variables were observed in the electrically elicited contractions. The maximal torque and surface EMG variables did not depend on the day of measure at HA. It was concluded that acute exposure to hypobaric hypoxia does not significantly affect the muscle-fiber membrane properties but does impact motor-unit control properties. This provides new insights in the understanding of motor control in extreme conditions of oxygen reduction, with relevance for sport and rehabilitation medicine, and may also explain the pathophysiological adaptations of the neuromuscular system occurring in such disorders as chronic obstructive pulmonary disease.     

Muscle fiber conduction velocity and contractile properties estimated from surface electrode arrays.

Using an array of surface electrodes set 5 mm apart, we estimated the conduction velocities of muscle fibers during submaximal voluntary isometric contraction of human first dorsal interosseous muscle. The conduction velocity obtained by the averaging method ranged from 3.2 to 5.0 m/sec with a mean of 4.2 m/sec. Twitch tensions in the muscle detected during voluntary isometric contractions ranged from 0.31 to 5.97 g with a mean of 2.75 g based on an averaging method triggered by surface myoelectric signals. Threshold forces of the motor units varied from 120 to 930 g. The rise time of the force developed by isometric adduction ranged from 36.0 to 75.4 msec, with a mean of 55.4 msec. The conduction velocity of the muscle fiber showed a high correlation with the twitch (r = 0.71, n = 50; P less than 0.001) and threshold (r = 0.52, n = 50; P less than 0.001) forces, but a low one with rise time (r = -0.32, n = 50; P less than 0.05). The use of the averaging method with surface electrode arrays, especially for voluntary isometric contractions, shows that motor unit conduction velocity and contractile properties are functionally correlated.     

Incidence of F waves in single human thenar motor units.

F-wave generation, axon conduction velocities, and contractile properties were compared in 44 healthy individual human thenar motor units. Force and muscle action potentials were recorded when single motor axons were stimulated intraneurally about 10 cm proximal to the elbow. Each stimulus usually evoked only one electromyographic (EMG) potential. However, in seven units (16%), a single stimulus elicited an F wave in response to 1.7 +/- 1.6% (mean +/- SD) of the stimuli applied. Axon conduction velocity proximal to the site of stimulation was faster than distal conduction velocity (72.7 +/- 8.0 m/s versus 64.2 +/- 10.5 m/s). Distal conduction velocities, twitch forces, and contraction times were similar for units that did and did not generate F waves. Thus, no obvious subset of thenar motor units generated F waves. These results provide valuable baseline information on F waves that can be used to assess changes in axon conduction, motor unit contractile properties, and motoneuron excitability in disease.     

Two-dimensional spatial distribution of surface mechanomyographical response to single motor unit activity

In order to better understand the mechanisms of generation of mechanomyography (MMG) signals, the two-dimensional distribution of surface MMG produced by the activity of single motor units was analyzed by a novel two-dimensional recording method. Motor unit action potentials were identified from intramuscular electromyographic (EMG) signals and used to trigger the averaging of MMG signals detected over the tibialis anterior muscle of 11 volunteers with a grid of 5x3 accelerometers (20-mm inter-accelerometer distance). The intramuscular wires were inserted between the first and second accelerometer in the middle column of the grid, proximal to the innervation zone. The subjects performed three contractions with visual feedback of the intramuscular EMG signals. In each contraction, a new motor unit was recruited at the minimum stable discharge rate (mean+/-S.D., N = 11 subjects, 7.3+/-2.3 pulse/s), resulting in torque of 2.4+/-2.8% of the maximal voluntary contraction (MVC), 4.6+/-2.7% MVC, and 6.3+/-3.1% MVC (all different, P < 0.01). For 23 out of 33 detected motor units, it was possible to extract the motor unit surface acceleration map (MUAM). A negative MUAM peak (-2.7+/-2.2 mm/s2) was detected laterally and a positive MUAM peak (4.1+/-2.4 mm/s2) medially (P < 0.001). The time-to-peak was shorter in the medial part of the muscle (2.9+/-0.4 ms) than in the other locations (3.4+/-0.5 ms, P < 0.001). The double integrated signals (muscle displacement) indicated negative deflection in the lateral part and inflation close to the tibia bone. The maps of acceleration showed spatial dependency in single motor unit MMG activities. The technique provides a new insight into motor unit contractile properties.     

Variability of motor unit discharge and force fluctuations across a range of muscle forces in older adults

Variability of motor unit discharge is a likely contributor to the greater force fluctuations observed in old adults at low muscle forces. We sought to determine whether the variability of motor unit discharge rate underlies the fluctuations in force during steady contractions across a range of forces in young (n = 11) and old (n = 14) adults. The coefficient of variation (CV) for discharge rate and force were measured during a force-matching task as the first dorsal interosseous muscle performed isometric contractions. The recruitment thresholds of the 78 motor units ranged from 0.04% to 34% of maximal voluntary contraction (MVC) force. The CV for discharge rate ranged from 7.6% to 46.2% and was greater (P < 0.05) for old adults (21.5% +/- 7.7%) than young adults (17.3% +/- 8.1%). Although the CV for force was similar for young and old subjects (2.53% +/- 1.6%) across all target forces, it was greater for old adults at the lowest forces. Furthermore, there was a positive relation (r2 = 0.20, P < 0.001) between the CV for force and the CV for discharge rate across the range of recruitment thresholds. This relation was significant for old adults (r2 = 0.30, P < 0.001), but not for young adults (r2 = 0.06, P > 0.05). Thus, the normalized variability (CV) of motor unit discharge was greater in old adults and was related to the amplitude of force fluctuations across a broader range of forces than previously examined. These findings underscore the contribution of variability of motor unit activity to motor output in normal human aging.     

Sensory group Ia proximal conduction velocity

The fastest median and ulnar velocities derived by recording motor and mixed nerve action potentials, F waves, H-reflexes, and somatosensory evoked potentials (SEPs) were compared. H-reflex recording was facilitated by employing selective group Ia excitation during voluntary muscular contraction. Mixed nerve, SEP, and H velocities, considered to predominantly reflect group Ia conduction, measured 63.2 +/- 3.2 m/sec, 63.4 +/- 4.5 m/sec, and 67.2 +/- 4.3 m/sec, respectively, between the wrist and elbow. Conventional motor conduction velocity was significantly slower (58.3 +/- 5.1 msec), but F velocity, which although nonuniform is also a measure of motor conduction, was 68.4 m/sec. Mean F latency was considered more reliable and representative than minimum F latency. F and H velocities accelerated proximally by 4.5 m/sec. They complement each other when evaluating motor and sensory group Ia conduction. The H-reflex and SEP use identical stimulus characteristics and when simultaneously recorded allow direct comparison of the fastest conducting peripheral and central sensory pathways.     

Jitter in the muscle fibre.

Direct stimulation of muscle fibres with a regular 10 Hz rate, three computer generated random rhythms and a sequence of voluntary discharges was used to quantify the interdischarge interval (IDI) dependent jitter due to velocity recovery function (VRF). This jitter was found to depend on conduction time and strength of VRF, but not on propagation velocity. The results suggest that in the usual jitter study in voluntarily activated muscle fibre pairs, with moderately irregular discharge rate and interpotential intervals below 3 ms the IDI dependent jitter contributes on average less than 10 microseconds, but can be so large as to produce false abnormal values at more irregular rates, longer interpotential intervals and pronounced differences in VRF. It can be effectively removed by mathematical algorithms or, better still, by using electrical stimulation.     

Velocity recovery function of the compound muscle action potential assessed with doublet and triplet stimulation

Normative values of muscle fiber conduction velocity depend on the conditions in which conduction velocity is measured due to the velocity recovery function (VRF) of muscle fibers. In this study the VRF of the compound muscle action potential (CMAP) was assessed following doublet and triplet stimulation in order to investigate the effect of repetitive muscle activation on muscle fiber conduction velocity. The VRF from doublet and triplet activation showed a peak of 4.6%-15.0% and 6.4%-25.9%, respectively, which is not significantly different. The VRF of the CMAP with doublet stimulation had a plateau between 25-75 ms, similar to that reported for single muscle fibers, and changed as a consequence of previous activation. The VRFs with doublet and triplet stimulation were different for interstimulus intervals in the range of 12-250 ms, where the triplet resulted in a plateau of supernormal conduction velocity. The VRF of the triplet could be explained by linear summation of the effects from doublet stimulations only for small distances between the two conditioning stimuli. These results provide new information on the adaptation of membrane properties of muscle fibers to repetitive activation. Changes in CMAP properties due to repeated activation may influence the accuracy of techniques based on CMAP recordings, such as collision methods.     

Electromechanical changes during electrically induced and maximal voluntary contractions: Surface and intramuscular EMG responses during sustained maximal voluntary contraction

Changes in the electrical activity of the human gastrocnemius and soleus muscles during fatiguing maximal plantar flexions were studied with computer-aided EMG frequency power spectral analysis and intramuscular spike amplitude-frequency histogram analysis. In some experiments, brief supramaximal nerve stimulations of 80 Hz were given at 15-s intervals during sustained maximal voluntary contractions (MVCs). Multiple muscle biopsy samples were also obtained from the gastrocnemius muscle for fiber type determination. The surface EMG frequency spectral analysis showed a highly significant reduction in mean power frequency and root mean square EMG amplitude during sustained MVCs. The intramuscular spike amplitude-frequency histograms showed that the gastrocnemius muscle had a progressive reduction in the motor unit discharge frequency, particularly those with a relatively high amplitude, whereas the soleus muscle hardly showed a reduction in motor unit activity. Reduction in motor unit activity was also found to be more pronounced in gastrocnemius muscles with higher proportions of type II fibers. Brief maximal tetanic stimulations initially matching the MVC failed to increase the contraction force. Similarly, the evoked compound mass action potentials showed little change in the amplitude in subjects with different muscle fiber compositions. Results of this study suggest that during sustained MVCs, force fatigue could not be attributed to a failure of muscle membrane electrical propagation; a progressive reduction in motor unit activation does not result in a functional disadvantage, but may optimize excitation-contraction coupling by avoiding a muscle electrical conduction failure; and the extent of the reduction in motor unit activation seems to be muscle-fiber-type-dependent which may account for the reduction in amplitude and frequency of the surface EMG.     

Motor unit recruitment and bursts of activity in the surface electromyogram during a sustained contraction

Bursts of activity in the surface electromyogram (EMG) during a sustained contraction have been interpreted as corresponding to the transient recruitment of motor units, but this association has never been confirmed. The current study compared the timing of trains of action potentials discharged by single motor units during a sustained contraction with the bursts of activity detected in the surface EMG signal. The 20 motor units from 6 subjects [recruitment threshold, 35.3 +/- 11.3% maximal voluntary contraction (MVC) force] that were detected with fine wire electrodes discharged 2-9 trains of action potentials (7.2 +/- 5.6 s in duration) when recruited during a contraction that was sustained at a force below its recruitment threshold (target force, 25.4 +/- 10.6% MVC force). High-pass filtering the bipolar surface EMG signal improved its correlation with the single motor unit signal. An algorithm applied to the surface EMG was able to detect 75% of the trains of motor unit action potentials. The results indicate that bursts of activity in the surface EMG during a constant-force contraction correspond to the transient recruitment of higher-threshold motor units in healthy individuals, and these results could assist in the diagnosis and design of treatment in individuals who demonstrate deficits in motor unit activation.     

Comparison of the recruitment and discharge properties of motor units in human brachial biceps and adductor pollicis during isometric contractions

Experiments were designed to assess the relative contribution of rate coding and motor unit recruitment to force production in two muscles of different fiber composition and function. Single motor unit action potentials were recorded during steady isometric contraction in biceps brachii, a large proximal limb muscle of mixed fiber composition, and adductor pollicis, a small hand muscle comprised mainly of type I muscle fibers. Action potential spike trains were obtained over the entire force range in each muscle. The results suggest that these two muscles are controlled in different ways. In biceps brachii, recruitment was observed from 0 to 88% maximum voluntary contraction (MVC). In adductor pollicis, no motor unit was observed to be recruited at forces greater than 50% MVC, with the majority of recruitment occuring below 30% MVC. On the average, motor units in adductor pollicis discharged at higher rates, with less regularity, and with a greater frequency of occurrence of short interspike intervals (intervals ≤ 20 msec) than those in biceps brachii. Such findings suggest that rate coding plays a more prominent role in force modulation in adductor pollicis, while recruitment plays a more important role throughout the contractile force range in biceps brachii.     

The recruitment order of electrically activated motor neurons investigated with a novel collision technique.

OBJECTIVE: The development of a novel collision technique for assessment of the activation order of electrically activated nerve fibers, which is an important question in functional electrical therapy or for interpretation of results of motor unit number estimates. METHODS: Compound muscle action potentials were recorded with the belly-tendon configuration from the abductor digiti minimi. A novel modified Hopf's collision technique was applied on ten healthy male subjects to determine the distributions of conduction velocities (DCV) of all ulnar nerve fibers and of the fibers activated by electrical stimuli eliciting 20%, 50%, and 80% of the maximal muscle response. RESULTS: The maximum nerve conduction velocity was (means+/-SE) 64.1+/-0.85m/s. The median conduction velocity of estimated DCV was 58.9+/-0.97m/s (stimulus at 20%), 58.0+/-0.98m/s (50%), 57.2+/-0.91m/s (80%), and 56.5+/-0.84m/s (whole nerve) (all different between each other, P<0.001). CONCLUSIONS: The proposed collision technique allows the assessment of nerve conduction velocity distributions at maximal and sub-maximal stimulation levels and provided evidence for an inverse activation order of nerve fibers with electrical stimulation. SIGNIFICANCE: The excessive fatigue seen with nerve electrical stimulation can be explained by a preferential activation of large diameter nerve fibers. The motor units first activated with electrical stimulation are likely not representative of the motor unit pool in the muscle, which poses limitations in the reliability of some of the proposed methods for motor unit counting.     

Tracking motor unit action potentials in the tibialis anterior during fatigue

New surface electromyogram (SEMG) techniques offer the potential to advance knowledge of healthy and diseased motor units. Conduction velocity (CV) estimates, obtained from indwelling electrodes, may provide diagnostic information, but the standard method of CV estimation from SEMG may be of only limited value. We developed a motor unit (MU) tracking algorithm to extract motor unit conduction velocity (MUCV) and motor unit action potential (MUAP) amplitude estimates from SEMG. The technique is designed to provide a noninvasive means of accessing fatigue and recruitment behavior of individual MUs. We have applied this MU tracking algorithm to SEMG data recorded during isometric fatiguing contractions of the tibialis anterior (TA) muscle in nine healthy subjects, at 30%-40% maximum voluntary contraction (MVC). The results reveal that MUCVs and MUAP amplitudes of individual MUs can be estimated and tracked across time. Time-related changes in the MU population may also be monitored. Thus, the SEMG technique employed provides insight into the behavior of the underlying muscle at the MU level by noninvasive means.     

Muscle-fiber conduction velocity estimated from surface EMG signals during explosive dynamic contractions

Muscle-fiber conduction velocity (CV) was estimated from surface electromyographic (EMG) signals during isometric contractions and during short (150-200 ms), explosive, dynamic exercises. Surface EMG signals were recorded with four linear adhesive arrays from the vastus lateralis and medialis muscles of 12 healthy subjects. Isometric contractions were at linearly increasing force from 0% to 100% of the maximum. The dynamic contractions consisted of explosive efforts of the lower limb on a sledge ergometer. For the explosive contractions, muscle-fiber CV was estimated in seven time-windows located along the ascending time interval of the force. There was a significant correlation between CV values during the isometric ramp and explosive contractions (R = 0.75). Moreover, CV estimates increased significantly from (mean +/- SD) 4.32 +/- 0.46 m/s to 4.97 +/- 0.45 m/s during the increasing-force explosive task. It was concluded that CV can be estimated reliably during dynamic tasks involving fast limb movements and that, in these contractions, it may provide important information on motor-unit control properties.     

Variation of amount of muscle discharges during ballistic isometric voluntary contraction in man

The effect of force velocity on the relation between voluntary force exertion and amount of muscle discharge was investigated. Surface e.m.g. from the adductor pollicis muscle and voluntary force curve were recorded simultaneously. Examined forces were selected from 500 to 3500 g at the peak force (about 30% of MVC) with time to peak of force curve between 60 ms and 500 ms. The amount of discharge during slow ramp contraction increased with the force increment. In ballistic contractions there was a wide variation in both the amount and rate of discharge. It is suggested that the modes of motor unit activities are different between force exertion with time to peak of less than 150 ms and force exertion with time to peak of over 150 ms.