Bilateral experimental muscle pain changes electromyographic activity of human jaw-closing muscles during mastication

 The effects of bilateral experimental muscle pain on human masticatory patterns were studied. Jaw movements and electromyographic (EMG) recordings of the jaw-closing muscles were divided into multiple single masticatory cycles and analyzed on a cycle-by-cycle basis. In ten men simultaneous bilateral injections of hypertonic saline (5%) into the masseter muscles caused strong pain (mean±SE: 7.5±0.4 on a 0–10 scale), significantly reduced EMG activity of jaw-closing muscles in the agonist phase, and significantly increased EMG activity in the antagonist phase. Nine of the subjects reported a sensation of less intense mastication during pain. Injections of isotonic saline (0.9%) did not cause pain or significant changes in masticatory patterns. The influence of higher brain centers on conscious human mastication can not be discarded but the observed phase-dependent modulation could be controlled by local neural circuits and/or a central pattern generator in the brain stem which are capable of integrating bilateral nociceptive afferent activity. Received: 19 February 1997 / Accepted: 14 April 1997     

Human motor unit activity during the onset of muscle fatigue in submaximal isometric isotonic contraction

Summary The onset of fatigue has been studied by relating motor unit activity and surface myoelectric activity during constant force isometric contraction in man.The surface (global) EMG of the biceps brachii was recorded using bipolar electrodes. The global EMGs of the other elbow flexors were also recorded. Motor unit activity was recorded simultaneously at three points of the biceps brachii by using wire electrodes.The time course of the integrated surface EMG showed that fatigue occurred right at the beginning of the contraction. The increase of the integrated EMG was especially important when the value of the force maintenance was high. The time course of this increase was close to that of the output of the spikes recorded by the wire electrodes.No matter what the value of the force maintenance, MU recruitment occurred throughout the contraction. The existence of an increase in the MU firing frequency depended on the value of this force.Contractile element fatigue is believed to provide the explanation of these results, while neuromuscular junction fatigue may perhaps be more important near the time limit.     

The scaling of motor noise with muscle strength and motor unit number in humans

Understanding the origin of noise, or variability, in the motor system is an important step towards understanding how accurate movements are performed. Variability of joint torque during voluntary activation is affected by many factors such as the precision of the descending motor commands, the number of muscles that cross the joint, their size and the number of motor units in each. To investigate the relationship between the peripheral factors and motor noise, the maximum voluntary torque produced at a joint and the coefficient of variation of joint torque were recorded from six adult human subjects for four muscle/joint groups in the arm. It was found that the coefficient of variation of torque decreases systematically as the maximum voluntary torque increases. This decreasing coefficient of variation means that a given torque or force can be more accurately generated by a stronger muscle than a weaker muscle. Simulations demonstrated that muscles with different strengths and different numbers of motor units could account for the experimental data. In the simulations, the magnitude of the coefficient of variation of muscle force depended primarily on the number of motor units innervating the muscle, which relates positively to muscle strength. This result can be generalised to the situation where more than one muscle is available to perform a task, and a muscle activation pattern must be selected. The optimal muscle activation pattern required to generate a target torque using a group of muscles, while minimizing the consequences of signal dependent noise, is derived.     

The influence of muscle pain and fatigue on the activity of synergistic muscles of the leg

The purpose of this study was to investigate the effect of experimentally induced muscle pain on the motor-control strategies of synergistic muscles during submaximal fatiguing isometric contractions. The root mean square (RMS) and median frequency (MF) of the surface electromyographic (EMG) signal from synergistic plantarflexors and dorsiflexors were assessed to exhaustion. Ten subjects performed sustained dorsiflexions and plantarflexions at two contraction levels, 50% and 80% of maximum voluntary contraction, with or without muscle pain, induced by injection of 6% hypertonic saline in one synergist. In the painful contractions, the RMS of the EMG signal was decreased compared to the control condition in the initial phase of the contraction, in the muscles where pain was induced as well as in the nonpainful synergists. Moreover, the EMG signal MF decreased faster during muscle pain than in the control condition. The endurance time was shorter during muscle pain, and some of the nonpainful synergists showed increased compensatory activity at the end of the contractions to maintain the target force. The decreased EMG activation during pain was coupled with significantly decreased torque levels during the painful condition that would partly explain the results. However, the ratio between force and EMG amplitude was decreased for both the painful and nonpainful synergists, so other mechanisms might explain the present findings. This study shows that localized muscle pain can reorganize the EMG activity of synergists where no pain is present. These findings may have implications for the understanding of manifestations seen in relation to painful musculoskeletal disorders.     

The influence of experimentally induced pain on shoulder muscle activity

Muscle function is altered in painful shoulder conditions. However, the influence of shoulder pain on muscle coordination of the shoulder has not been fully clarified. The aim of the present study was to examine the effect of experimentally induced shoulder pain on shoulder muscle function. Eleven healthy men (range 22–27 years), with no history of shoulder or cervical problems, were included in the study. Pain was induced by 5% hypertonic saline injections into the supraspinatus muscle or subacromially. Seated in a shoulder machine, subjects performed standardized concentric abduction (0°–105°) at a speed of approximately 120°/s, controlled by a metronome. During abduction, electromyographic (EMG) activity was recorded by intramuscular wire electrodes inserted in two deeply located shoulder muscles and by surface-electrodes over six superficially located shoulder muscles. EMG was recorded before pain, during pain and after pain had subsided and pain intensity was continuously scored on a visual analog scale (VAS). During abduction, experimentally induced pain in the supraspinatus muscle caused a significant decrease in activity of the anterior deltoid, upper trapezius and the infraspinatus and an increase in activity of lower trapezius and latissimus dorsi muscles. Following subacromial injection a significantly increased muscle activity was seen in the lower trapezius, the serratus anterior and the latissimus dorsi muscles. In conclusion, this study shows that acute pain both subacromially and in the supraspinatus muscle modulates coordination of the shoulder muscles during voluntary movements. During painful conditions, an increased activity was detected in the antagonist (latissimus), which support the idea that localized pain affects muscle activation in a way that protects the painful structure. Further, the changes in muscle activity following subacromial pain induction tend to expand the subacromial space and thereby decrease the load on the painful structures.     

Effects of muscle fatigue induced by low-level clenching on experimental muscle pain and resting jaw muscle activity: gender differences

The purpose of this study was to investigate the effects of jaw-muscle fatigue evoked by low-level tooth-clenching followed by the induction of experimental muscle pain by injection of glutamate on the perception of fatigue and pain and on the resting electromyographic (EMG) activity. In addition, the role of gender on these interactions was studied. The EMG activities of bilateral masseter (MAL, MAR) and temporalis (TAL, TAR) muscles in 11 healthy young women and 12 men were measured before (Baseline) and after tooth-clenching for 30 min at 10% of maximal force (Post1), after subsequent glutamate (Glu) or isotonic saline (Iso) injection into the MAL following the tooth-clenching (Post2) and 60 min after tooth-clenching (Post3). The intensities of fatigue, fatigue-related muscle pain and headache-like symptoms were scored on 0–10 cm visual analog scales (VAS). The glutamate-evoked pain was continuously scored on an electronic VAS. Sustained low-level tooth-clenching consistently produced fatigue sensation, fatigue-related muscle pain and headache-like symptoms in both genders with significantly higher fatigue VAS scores in men than in women, while the accompanying increase in the resting EMG activity appears higher in women than in men in the masseter muscles. In this study no gender differences were found for the perceived amount of experimental pain induced by glutamate injection. Additional increases of the resting EMG activity after injections occurred only in men in the injected masseter muscle and non-injected temporalis muscles. The present findings provide new information on the complex influence of gender on sensory-motor integration in the trigeminal system which may contribute to differences in susceptibility to develop musculoskeletal pain problems.     

Surface electromyogram spectral characterization and motor unit activity during voluntary ramp contraction in men

Summary The relationships were investigated between the surface electromyographic (SEMG) power spectrum analysed by the 20 order autoregressive model (AR spectrum) and underlying motor unit (MU) activity during isometric contractions increasing linearly from 0% to 80% maximal voluntary contraction. Intramuscular spikes and SEMG signals were recorded simultaneously from biceps brachii muscle; the former were analysed by a computer-aided intramuscular MU spike amplitude-frequency (ISAF) histogram and the latter subjected to AR spectral analysis. Results indicated that there was a positive correlation between the force output and the mean amplitude of the ISAF histogram but not with the mean frequency. These changes were accompanied by changes in relative power of the high frequency (100–200 Hz) peak (HL) in the AR spectrum. It was also found that there was a positive correlation between the mean amplitude of the ISAF histogram and the HL value. These data suggested that the power of the high frequency peak in the AR spectrum of the SEMG signal preferentially reflected the progressive recruitment of underlying MU according to their size. Differences between the AR spectrum and the spectrum estimated by fast Fourier transform algorithm have also been discussed.     

Experimental muscle pain changes motor control strategies in dynamic contractions

This study investigated the effect of muscle pain on muscle activation strategies during dynamic exercises. Ten healthy volunteers performed cyclic elbow flexion/extension movements at maximum speed for 2 min after injection of (1) hypertonic (painful) saline in the biceps brachii, (2) hypertonic saline in both biceps brachii and triceps brachii, and (3) isotonic (nonpainful) saline in the biceps brachii muscle. Surface electromyographic (EMG) signals were collected from the upper trapezius, biceps brachii, triceps brachii, and brachioradialis muscles (to estimate EMG amplitude) and with an electrode arrays from biceps brachii (to estimate muscle fiber conduction velocity [CV]). In all conditions, the acceleration of the movement decreased throughout the exercise, and kinematic parameters were not altered by pain. With respect to the control condition, pain induced a decrease of the biceps brachii (mean ± SE, –23±4%) and brachioradialis (–10±0.4%) integrated EMG (IEMG) in the beginning of the exercise, and an increase (45±3.5%) of the upper trapezius IEMG at all time points during the exercise. The biceps brachii IEMG decreased over time during the nonpainful exercises (–11±0.6%) while it remained constant in the painful condition. Biceps brachii CV decreased during painful conditions (–12.8±2.2%) while it remained constant during the nonpainful condition. In conclusion, muscle pain changes the motor control strategy to sustain the required dynamic task both in the relative contribution between synergistic muscles and in the motor unit activation within the painful muscle. Such a changed motor strategy may be highly relevant in models of occupational musculoskeletal pain conditions.     

Modulation of stretch-evoked reflexes in single motor units in human masseter muscle by experimental pain

The interaction between muscle pain and motor function of the jaw has been examined in recent years, but the nature of the modulation of the short-latency stretch reflex by pain is not fully understood. In this study, the reflex responses to stretch were measured in single low-threshold motor units that were kept discharging at a constant frequency, before, during and after the induction of experimental pain in one masseter muscle by controlled infusion of hypertonic saline. The probability of evoking a reflex response in individual motor units in the painful muscle at near-monosynaptic latency was reduced by a mean of about 20%. However, the overall reflex response in the surface electromyogram of both the ipsi- and contralateral masseter muscles was greater during pain. This was apparently a secondary response to the pain-induced increase in pre-stimulus activity in the motoneurone pools of both muscles, because increased motoneurone excitability may facilitate stretch reflexes. It is concluded that the most likely explanation for the reduced reflex response of low-threshold masseter motor units during experimental pain is a tonic reduction in the fusimotor drive to the masseter spindles.     

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.     

The influence of recruitment order and temperature on muscle contraction with special reference to motor unit fatigue

Summary Although recruitment in man often proceeds from the slowest to fastest motor units, a variety of stimuli can alter this order. To study the effect of recruitment order on isometric performance, the tetanic tension of individual fast and slow twitch motor units was measured during fatiguing isometric contractions of the medial gastrocnemius muscle of the cat with recruitment proceeding from either the slowest to fastest or fastest to slowest motor units throughout the contractions. The muscles were stimulated electrically through the ventral roots of the spinal cord. Fatiguing isometric tensions were examined at 10, 20, 40, 70, or 100% of the initial strength of the muscles at 28 and 38 C. The results of these experiments showed that for contractions at low isometric tensions (20 and 40% of the muscles' strength), especially at the lower temperature, the endurance was longer when recruitment proceeded from the slowest to fastest units. The reason for this appeared to be linked to the more rapid rate of fall of tension over time in fast as opposed to slow twitch motor units.Supported by the NIH grant number 7ROINS16003-01     

Resistance to glycogen depletion of motor units in the cat rectus lateralis muscle

Summary In nembutal anesthetized adult cats, intracellular stimulation of single abducens motoneurones was used to elicit glycogen depletion of their muscle units. Stimulation by short trains (13 pulses at 40 Hz) delivered once a second, was applied for 20 to 110 min. The activation of the motor unit was monitored by intracellular recording of motoneurone action potentials and by EMG. After the end of stimulation, the muscle was excised and frozen to be cut in serial sections that were processed for demonstration of either glycogen, ATPases or SDH. In two experiments, a motor unit could be histochemically identified because 10–15 fibres showed zones of complete glycogen depletion measuring about 5 mm in length. All the depleted fibres had the same histochemical profile: ATPases reactions gave dark staining with alkaline preincubation and light staining with acid preincubation whereas SDH activity was low. In other experiments, prolonged stimulation produced either no depletion at all or very limited zones of partial depletion in a few muscle fibres.Supported by CNRS ATP no. 126 and by Fondation pour la Recherche Médicalewith the technical assistance of N. Seyfritz, INSERM     

Opioid-insensitive hypoalgesia to mechanical stimuli at sites ipsilateral and contralateral to experimental muscle pain in human volunteers

Musculoskeletal pains are often characterised by referred pain and hyperalgesia. The aim of the present study was to examine the sensitivity to pressure and pinprick at sites ipsi- and contralateral to capsaicin-induced pain in the tibialis anterior (TA) muscle. Visual analogue scale (VAS) scores of the sensation to sub- and supra-pain threshold stimuli by pressure and pinprick were recorded before, during and after experimental muscle pain. It was found that pressure stimulation (120% of baseline pain threshold) delivered over the ipsilateral deep peroneal nerve between the 1st and 2nd metatarsal bones showed a significant increase in VAS scores during muscle pain. The referred pain did not overlap this hyperalgesic site. Ipsilateral test sites at the TA muscle, great toe and between the 3rd and 4th metatarsal bones did not show any changes in response to pressure stimulation during pain. In contrast, test sites at the ipsilateral ankle showed hypoalgesia to pressure during muscle pain. In the contralateral leg hypoalgesia to pressure was found at all sites during pain. The decreased sensitivity to pressure was confirmed with both sub- and supra-pressure pain-threshold stimuli. VAS scores to pinprick were either decreased or unchanged during pain compared to before pain. Naloxone administrated in a placebo-controlled manner had no effect on hypoalgesia to pressure or pinprick during muscle pain. Thus, the generalised decreased sensitivity may reflect activation of non-opioid endogenous pain inhibitory systems. The lack of change in sensitivity at some sites could indicate a competitive balance between excitatory and inhibitory mechanisms. The deep peroneal nerve specifically innervates both the TA muscle and the only site of hyperalgesia indicating spatial summation of afferent activity from these structures.     

Interactions between motor units in modulating discharge patterns of primary muscle spindle endings

Summary Discharge patterns of group Ia afferents of muscle spindles in the (isometric) cat semitendinosus muscle were recorded when subjected to the influence of contractions of three motor units elicited by stimulation of three -efferents with different regular or stochastic stimulus patterns. In order to study conditioning interactions between motor unit contractions, defined time constellations of stimuli to different motor units were isolated from the stimulus trains by electronic means. This technique was also applied to discharge patterns of two Ia fibres to isolate correlated discharges. The effects of defined time constellations of stimuli upon discharge patterns of single Ia afferents or correlated discharges of pairs of Ia afferents were assessed by poststimulus time histograms (PSTHs). It turned out that the influence exerted by one motor unit on spindle discharges was more or less strongly modulated by actions of the other motor units, dependent on the relative timing of their contractions. These effects could in part be explained by the relative locations of motor units and spindles within the muscle. These results are discussed with respect to possible mechanisms of low-amplitude physiological tremor.Supported by a grant from the Deutsche Forschungsgemeinschaft, SFB 33 (Nervensystem und biologische Information), Göttingen     

Experimental muscle pain results in reorganization of coordination among trapezius muscle subdivisions during repetitive shoulder flexion

The aim of the study was to examine the effect of experimental unilateral upper trapezius muscle pain on the relative activation of trapezius muscle subdivisions bilaterally during repetitive movement of the upper limb. Surface EMG signals were detected from nine healthy subjects from the upper, middle and lower divisions of trapezius during a repetitive bilateral shoulder flexion task. Measurements were performed before and after injection of 0.5 ml hypertonic (pain condition) and isotonic (control) saline into the upper division of the right trapezius muscle in two experimental sessions. On the painful side, upper trapezius showed decreased EMG amplitude (average rectified value, ARV) and lower trapezius increased ARV throughout the entire task following the injection of hypertonic saline (40.0 ± 22.2 vs. 26.0 ± 17.4 μV, and 12.5 ± 7.6 vs. 25.6 ± 14.8 μV, respectively, at the beginning of the contraction). On the side contralateral to pain, greater estimates of ARV were identified for the upper division of trapezius as the task progressed (37.4 ± 20.2 vs. 52.7 ± 28.4 μV, at the end of the contraction). Muscle fiber conduction velocity did not change with pain in all three divisions of the right trapezius muscle. The results suggest that local elicitation of nociceptive afferents in the upper division of the trapezius induces reorganization in the coordinated activity of the three subdivisions of the trapezius in repetitive dynamic tasks.     

Motor unit action potential rate and motor unit action potential shape properties in subjects with work-related chronic pain

The objective of this study was to investigate differences in motor control of the trapezius muscle in cases with work-related chronic pain, compared to healthy controls. Ten cases with chronic pain and 13 controls participated in the study. Electromyographic (EMG) signals were recorded from the upper trapezius during five computer work-related tasks. Motor control was assessed using global root-mean-square value (RMS_G), motor unit action potential (MUAP) rate (number of MUAPs per second, MR) and two MUAP shape parameters, i.e. root-mean-square (RMS_MUAP) and median frequency (FMED_MUAP). MR and FMED_MUAP were higher for the cases than for the controls (P<0.05). RMS_MUAP showed a trend for higher values in the chronic pain group (P<0.13), whereas RMS_G did not show a significant difference between the groups. The higher MR, FMED_MUAP and the trend for higher RMS_MUAP suggest that more high-threshold MUs contribute to low-level computer work-related tasks in chronic pain cases. Additionally, the results suggest that the input of the central nervous system to the muscle is higher in the cases with chronic pain.     

Rotation of synergistic activity during isometric jaw closing muscle contraction in man

5 healthy subjects were studied during 10–15 min of isometric jaw elevator contraction above fatigue threshold level. Bite force was measured between upper and lower front teeth and electromyographic (EMG) activity recorded from the right temporal and masseter muscles. Of the two muscles only the masseter was active at the start of the test and usually during the whole test. When the test was repeated, however, great relief from the pain in the fatigued masseter was sometimes experienced and the temporalis took over the load. All subjects experienced this “switch” phenomenon after a varying number of tests, one of them already during his first test. The mechanism seemed to be completely out of voluntary control and showed facilitation at repeated tests.     

Experimental muscle pain decreases the frequency threshold of electrically elicited muscle cramps

This study in humans tested the hypothesis that nociceptive muscle afferent input facilitates the occurrence of muscle cramps. In 13 healthy adults, muscle cramps were experimentally induced in the foot by stimulating the tibialis posterior nerve at the ankle with 2-s bursts of stimuli separated by 30 s, with stimulation frequency increasing by 2-Hz increments from 10 Hz until the cramp appeared. The minimum stimulation frequency that induced the cramp was defined “cramp frequency threshold”. In 2 days, elicitation of the cramp was performed in the two-feet with and without (baseline condition) injection of hypertonic (painful condition) or isotonic (control condition) saline into the deep midportion of the flexor hallucis brevis muscle, from where surface EMG signals were recorded. The cramp frequency threshold was lower for the painful condition with respect to its baseline (mean ± SE, hypertonic saline: 25.7 ± 2.1 Hz, corresponding baseline: 31.2 ± 2.8 Hz; P < 0.01) while there was no difference between the threshold with isotonic injection with respect to baseline. EMG average rectified value and power spectral frequency were higher during the cramp than immediately before the stimulation that elicited the cramp (pre-cramp: 13.9 ± 1.6 μV and 75.4 ± 3.8 Hz, respectively; post-cramp: 19.9 ± 3.2 μV and 101.6 ± 6.0 Hz; P < 0.05). The results suggest that nociceptive muscle afferent activity induced by injection of hypertonic saline facilitates the generation of electrically elicited muscle cramps.     

Motor unit conduction velocity during sustained contraction of the vastus medialis muscle

The aim of the study was to analyze motor unit conduction velocity at varying force of the vastus medialis muscle during sustained contraction. Surface (8-electrode array) and intramuscular (two wire electrodes) EMG signals were recorded from the distal part of the dominant vastus medialis muscle of ten healthy male subjects. The subjects sat on a chair with the knee 90° flexed and performed seven 180-s long contractions at forces in the range 2.5–30% of the maximal voluntary contraction force. For each force level, the discharge patterns of the newly recruited motor units with respect to the previous force level were identified from the intramuscular recordings and used as trigger for averaging the surface EMG signals. Motor unit conduction velocity was estimated from the averaged surface EMG. Average discharge rate at which motor units were analyzed was the same for each force level (mean ± SD, 8.3 ± 0.8 pulses per second). Motor unit conduction velocity at the beginning of the contraction and its rate of change over time increased with force (P < 0.05). Conduction velocity at the beginning of the contraction estimated from the interference surface EMG (4.44 ± 0.66 m/s) and from single motor units (4.75 ± 0.56 m/s) were positively correlated (R ² = 0.46; P < 0.0001) but significantly different (P < 0.05). The results indicate that single motor unit conduction velocity and its rate of change during sustained contraction, assessed at a fixed discharge rate, depend on force level.     

The “size principle” and synaptic effectiveness of muscle afferent projections to human extensor carpi radialis motoneurones during wrist extension

The question of whether muscle spindle afferents might control human motoneurone activity on the basis of the “size principle” during voluntary contraction was investigated by recording the discharge of single motor units (n=196) in wrist extensor muscles while stimulating the homonymous muscle spindles by means of tendon taps. The mechanical stimuli were delivered with a constant post-spike delay of 80 ms so that the resulting afferent volleys could be expected to reach the motoneurones towards the end of the inter-spike interval (mean±SD duration: 124.7±11.9 ms). In the six subjects tested, the response probability was found to be significantly correlated with the motor units' functional parameters. Differences in twitch rise times, twitch amplitudes, recruitment thresholds and macro-potential areas were found to account for 18%, 9%, 6% and 2% of the differences in the response probability observed within the whole population of motor units tested. These differences could not be due to differences in firing rate for two reasons: first, the motor units were found to discharge with a similar range of inter-spike intervals whatever their functional characteristics; secondly, the weak positive correlation observed between the response probability and the motor unit firing rate showed parallel regression lines between the late-recruited fast-contracting motor units and the first-recruited slowly contracting motor units, but they-intercept was significantly higher in the latter case. This confirmed that the responses of the first-recruited slowly contracting motor units tended to be larger whatever the firing rates. In most of the pairs tested in the same experiment, the motor units which had the lowest recruitment thresholds, longest contraction times, smallest contraction forces or smallest motor unit macro-potentials tended to produce the largest responses, which also had the longest latencies. Taking the response latency to be an index of a motoneurone's conduction velocity and therefore of its size, the data obtained with this index — and with other functional indices such as the twitch rise times and amplitudes, the macro-potential areas and the recruitment thresholds — can be said to be fully consistent with the “size principle”, as previously found in anaesthetized animals. It can be inferred that the presynaptic inhibition which is liable to take action during voluntary contraction does not seem to alter the graded distribution of the muscle afferent projections to human wrist extensor motoneurones.