Neuromuscular propagation after fatiguing contractions of the paralyzed soleus muscle in humans

We analyzed the M wave and torque after repetitive activation and recovery of the human soleus muscle in individuals with spinal cord injury. Fifteen individuals with complete paralysis had the tibial nerve activated for 330 ms every second with a 20-Hz train. The M wave and torque were analyzed before fatigue, immediately after fatigue, and during recovery. The torque and three M-wave measurements (amplitude, duration, median frequency) changed significantly after fatigue in the chronic group, but the M-wave area was not changed. The M wave was completely recovered after 5 min of rest, even though the torque remained depressed during recovery. The M-wave changes appeared to contribute minimally to the reduced torque in individuals with chronic paralysis. The disassociation in the M-wave–torque relationship during fatigue and recovery suggests, that electrical stimulation under electromyography control is not an ideal method to optimize torque in paralyzed muscle. © 1998 John Wiley & Sons, Inc. Muscle Nerve 21:776–787, 1998.     

Fatigue modulates synchronous but not asynchronous soleus activation during stimulation of paralyzed muscle

ObjectiveElectrical stimulation over a motor nerve yields muscle force via a combination of direct and reflex-mediated activation. We determined the influence of fatigue on reflex-mediated responses induced during supra-maximal electrical stimulation in humans with complete paralysis.MethodsWe analyzed soleus electromyographic (EMG) activity during repetitive stimulation (15 Hz, 125 contractions) in 22 individuals with complete paralysis. The bout of stimulation caused significant soleus muscle fatigue (53.1% torque decline).ResultsBefore fatigue, EMG at all latencies after the M-wave was less than 1% of the maximal M-wave amplitude (% MaxM). After fatigue there was a fourfold (p < 0.05) increase in EMG at the H-reflex latency; however, the overall magnitude remained low (<2% change in % MaxM). There was no increase in “asynchronous” EMG ～ 1 s after the stimulus train.ConclusionsFatigue enhanced the activation to the paralyzed soleus muscle, but primarily at the H-reflex latency. The overall influence of this reflex modulation was small. Soleus EMG was not elevated during fatigue at latencies consistent with asynchronous activation.SignificanceThese findings support synchronous reflex responses increase while random asynchronous reflex activation does not change during repetitive supra-maximal stimulation, offering a clinical strategy to consistently dose stress to paralyzed tissues.     

EFFECT OF NEOSTIGMINE, d-TUBOCURARINE AND CLINICAL CONDITION ON EVOKED ELECTROMYOGRAM FROM ORBICULARIS OCULI IN MYASTHENIA GRAVIS

In our previous report, evoked electromyograms of the orbicularis oculi muscle with repetitive stimulation given at frequencies of 5, 10, 20, 50 and 100 c/s were examined in myasthenia gravis. The amplitude of M-waves showed several specific changes against the stimulation frequencies employed. The patterns of the amplitude of M-waves appearing with each frequency could be classified into 3 types, Type I, Type II and Type III according to relation between the frequency of stimulation and decrease and/ or increase of M-wave amplitude. In the present study, the effect of neostigmine, d-tubocurarine and clinical condition on the various pattern of M-wave amplitude curve classified into above mentioned three types was examined.     

Repeatability of electrically evoked EMG signals in the human vastus medialis muscle

The repeatability of spectral and amplitude parameters and conduction velocity estimates of M-waves was tested on the vastus medialis muscle of 9 normal subjects. Isometric contractions sustained for 30 s were elicited by stimulation of the main muscle motor point and repeated on 5 different days. The initial value and two indicators of myoelectric manifestations of muscle fatigue were computed for each variable. The test—retest Pearson correlation coefficient, the paired Wilcoxon test, and the intraclass correlation coefficient (ICC) showed that parameters of spectral variables are more repeatable than those of amplitude variables and conduction velocity. The ICC ranged from 86.4% for the initial value of median frequency to 21.6% for the initial value of the average rectified value. Fatigue indices showed ICCs in the range of 20–64%. It is concluded that: (a) initial values and fatigue indices based on spectral variables are more repeatable than those based on amplitude variables; (b) the repeatability of conduction velocity estimates is not yet sufficient for clinical application; (c) M-wave shape, rather than amplitude or width, is a characteristic of individual muscles; and (d) electrode location is critical. © 1998 John Wiley & Sons, Inc. Muscle Nerve 21: 184–193, 1998.     

M-wave changes after high- and low-frequency electrically induced fatigue in different muscles

The mechanisms of fatigue-induced changes in evoked compound muscle action potential (M-waves) are not well documented. In rats, isolated fast-glycolytic (tibialis anterior, or TA) and slow-oxidative muscles (soleus, or SOL) were stimulated repetitively at a low (10-Hz) or high (80-Hz) rate. Decreased amplitude and prolonged duration of M-waves were only significant after high-frequency fatigue in TA and SOL muscles; that is, in the conditions in which an influx of calcium was measured. On the other hand, maximal force failure and maximal lactic acid increase in the bath medium occurred in TA muscle after high- and low-frequency fatigue trials. Postfatigue increase in potassium concentration occurred in all circumstances. Thus, M-wave alterations depend mainly on the stimulation paradigm and not on the muscle type, and cannot be used as a marker of changes in intracellular potassium or lactate ions. This amplifies understanding of the significance of M-wave changes in human exercise protocols.     

Fatigue-related changes in neuromuscular excitability of rat hindlimb muscles

Brief repetitive trains of supramaximal nerve stimulation produce intermittent muscle activation and, in time, a progressive decline in force (i.e., neuromuscular fatigue) and depression of the electromyogram (EMG). These changes may include within-train reductions in EMG due to a failure of neuromuscular propagation. The aim of the present study was to investigate changes in EMG during a 360-second stimulus regimen designed to fatigue soleus and extensor digitorum longus muscles of anesthetized rats by activating the muscle with repetitive trains of 40 Hz stimuli. Measurements included peak force for each tetanus, variation of the within-train EMG (coefficient of variation for area), and magnitude of the first EMG waveform (area) of each train. Fatigue was characterized as the relative decline in force over the course of the test. The responses of the test muscles were categorized, based on an absolute scale of fatigability, into five groups: potentiated, nonfatigable, low fatigability, intermediate fatigability, and high fatigability. Fatigable muscles (low, intermediate, and high fatigability groups) demonstrated a decreased EMG magnitude and an increased EMG-area variation with repetitive activation. This increased variation, however, was nonmonotonically related to fatigability such that the least and most fatigable muscles had the smallest within-train EMG variation. We suggest that these data can be explained by considering the EMG (compound muscle action potential) as a stochastic process that represents a composite of single-fiber events (axonal to sarcolemmal transmission) with variable probabilities.     

Depression and recovery of reflex amplitude during electrical stimulation after spinal cord injury

ObjectiveThe aim of this study was to quantify, for the first time, H-reflexes evoked during prolonged trains of wide-pulse neuromuscular electrical stimulation (WP-NMES) in individuals with chronic spinal cord injury (SCI). We hypothesised that after the first H-reflex, reflex amplitudes would be depressed (due to post-activation depression), but would recover and this recovery would be enhanced after a “burst” of 100 Hz WP-NMES.MethodsSoleus M-waves and H-reflexes evoked during WP-NMES (1 ms pulse width) of the tibial nerve were quantified in nine individuals with SCI. WP-NMES was delivered in two patterns: “constant-frequency” (15 or 20 Hz for 12 s) and “burst-like” (15-100-15 Hz or 20-100-20 Hz; 4 s each phase) at an intensity that evoked an M-wave between 10% and 15% of the maximal M-wave (M_max).ResultsDuring constant frequency stimulation, after the initial depression from the first to the second H-reflex (1st: 57% M_max; 2nd: 25% M_max), H-reflexes did not recover significantly and were 37% M_max at the end of the stimulus train. During the burst-like pattern, after the initial depression (1st: 62% M_max; 2nd: 30%), reflexes recovered completely by the end of the stimulation (to 55% M_max) as they were not significantly different from the first H-reflex. M-waves were initially depressed (1st: 12% M_max; 2nd: 7% M_max) then did not change throughout the stimulation and were not significantly different between stimulation patterns. An analysis of covariance indicated that the depression in M-wave amplitude did not account for the depression in H-reflex amplitude.ConclusionsRelatively large H-reflexes were recorded during both patterns of NMES. The brief burst of 100 Hz stimulation restored H-reflexes to their initial amplitudes, effectively reversing the effects of post-activation depression.SignificanceFor individuals with chronic SCI, generating contractions through central pathways may help reduce muscle atrophy and produce contractions that are more fatigue-resistant for rehabilitation, exercise programs, or to perform activities of daily living.     

Effect of random interpulse interval modulation on neuromuscular fatigue

Neuromuscular endurance during electrical stimulation may be enhanced if naturally occurring motor unit firing patterns are used. Variability in the interpulse interval (IPI) distribution may enable brief periods of rest and optimization of force output. Nine individuals participated in three 3-minute fatigue protocols of the thenar muscles elicited by supramaximal stimulation of the median nerve. All protocols consisted of a mean IPI of 33.3 ms and differed only in the type of IPI modulation, which was constant (0%), random (+/-20%), or ramped from 0% to +/-20%. M-wave amplitude declined following all protocols and the reduction was smallest following the ramp protocol. There was no significant difference among the starting or final forces or between the overall force-time integrals for the three protocols. Thus, IPI variability did not improve endurance time during electrical stimulation and the M-wave amplitude was not a reliable indicator of muscle force output.     

Switching stimulation patterns improves performance of paralyzed human quadriceps muscle

The clinical efficacy of functional electrical stimulation (FES) is limited by the rapid onset of fatigue. Functional electrical stimulation applications typically stimulate skeletal muscles with constant-frequency trains (CFTs). Our laboratory has identified trains that we call doublet-frequency trains (DFTs) and that produce greater forces than CFTs, but more fatigue during repetitive activation than comparable CFTs. The purpose of this study was to see whether a series of CFTs followed by DFTs would reach a targeted isometric peak force more times than either train type alone during repetitive isometric activation of the paralyzed quadriceps muscles of subjects with spinal cord injuries (SCI). The combination of CFTs followed by DFTs reached the targeted isometric force 14% more often than the CFTs alone and 18% more often than the DFTs alone. These findings confirm that switching train types may be a useful strategy to offset the rapid fatigue of the functionally important quadriceps muscle that persons with SCI experience when using FES.     

AN ANALYSIS OF EVOKED ELECTROMYOGRAM FROM ORBICULARIS OCULI IN PATIENTS WITH MYASTHENIA GRAVIS

Evoked electromyograms of the orbicularis oculi muscle with repeated stimulation given at frequencies of 5, 10, 20, 50 and 100 c/s were examined in myasthenia gravis; and the following results were obtained. 1. In the normal subject, the amplitude of M-waves showed almost no change by stimulation at frequencies of 5 and 10 c/s, and a mild gradual increase by stimulation at a frequency of 20 c/s. On stimulation with 50 and 100 c/s, the amplitude of M-waves showed a marked gradual increase and maintained nearly the peak value after a maximum had been reached. 2. In a total of 23 patients with myasthenia gravis, the amplitude of M-waves showed several specific changes against the stimulation frequencies employed. The patterns of the amplitude of M-waves appearing with each frequency were classified into 3 types: Type I, which showed an initial gradual decrease in amplitude with all the stimulation frequencies employed, was observed in 13 patients (56.5%). Type II, which showed an initial gradual decrease at frequencies of 5 c/s and 10 c/s, but a gradual increase followed by gradual decrease at frequencies of 50 and 100 c/s, was observed in 8 patients (34.8%). Type III, which showed no obvious difference from the pattern of the normal curve with stimulation given at not more than 50 c/s but a gradual increase followed by gradual decrease at a frequency of 100c/s, was observed in 2 patients (8.7%). 3. No distinct differences were noted in other neuromuscular diseases taken as control, as compared with the normal.     

Muscle fatigue during concentric and eccentric contractions

We compared the contribution of central and peripheral processes to muscle fatigue induced in the ankle dorsiflexor muscles by tests performed during concentric (CON) and eccentric (ECC) conditions. Each fatigue test consisted of five sets of 30 maximum voluntary contractions at a constant speed of 50 degrees /s for a 30 degrees range of motion of the ankle joint. The torque produced by the dorsiflexors and the surface electromyogram (EMG) of the tibialis anterior muscle were recorded during the fatigue tests. Before, during, and after the tests, the compound muscle action potential (M wave) and the contractile properties in response to single and paired electrical stimuli, as well as the interpolated-twitch method and postactivation potentiation (PAP), were recorded during isometric conditions. Compared with ECC contractions, the CON ones resulted in a greater (P < 0.05) loss of force (-31.6% vs. -23.8%) and a decrease in EMG activity (-26.4% vs. -17.5%). This difference was most pronounced during the first four sets of contractions, but was reduced during the last set. Activation was not altered by the tests because neither the interpolated-twitch response nor the ratio of the voluntary EMG to the amplitude of the M wave was changed in the two fatigue tests. Although there was no significant difference in M-wave amplitude between the two tests, changes in the twitch parameters and in the PAP were found to be greater in the CON than ECC contractions. It is concluded that the greater alterations in the contractile properties observed during the CON contractions indicate that intracellular Ca(2+)-controlled excitation-contraction (E-C) coupling processes, possibly associated with a higher energy requirement, are affected to a much greater degree than during ECC contractions.     

Muscle excitation in elderly adults: the effects of training.

Muscle membrane excitability is thought to decline with aging; the extent of this decline may be noninvasively assessed by measurement of the electrically evoked compound muscle action potential (M-wave). The intent of this study was two-fold: (1) to compare the M-wave in the brachioradialis (BR), tibialis anterior (TA), and thenar (TH) muscles of elderly (mean age = 66.3 +/- 3.7 years) and young (mean age = 31.2 +/- 4.9 years) adults, and (2) to determine the effects of 12 weeks of resistance training on M-wave characteristics in elderly adults. Prior to training, the elderly subjects had significantly smaller (P less than 0.05) resting M-waves than the young adults in the BR (4.8 mV vs. 8.7 mV), TA (8.8 mV vs. 11.0 mV), and TH (5.2 mV vs. 10.2 mV) muscles. During a 2-minute voluntary fatigue paradigm (3 seconds MVC per 2 seconds rest for 2 minutes), there was no evidence of excitability failure in either group. Following training, there was a significant increase (P less than 0.05) in the size of the M-wave of the TH (pretraining: 5.2 mV; posttraining: 8.96 mV) and BR (pretraining: 4.8 mV; posttraining: 6.1 mV), and a nonsignificant increase in the M-wave of the TA, but there was no change in the relative behavior of the M-wave during the 2-minute voluntary fatigue paradigm. It is suggested that the decline in muscle membrane excitation with aging may be due, at least in part, to the effects of a decreased membrane potential on the muscle fiber action potential.(ABSTRACT TRUNCATED AT 250 WORDS)     

Increased blood pressure can reduce fatigue of thenar muscles paralyzed after spinal cord injury

The aim of this study was to evaluate whether increases in blood pressure, and presumably muscle perfusion pressure, improve the endurance of thenar muscles paralyzed chronically by cervical spinal cord injury (SCI). Resting mean arterial pressure (MAP) was low in all eight subjects (64 +/- 2 mmHg). Muscle fatigue (force decline) was produced on 2 days by intermittent supramaximal electrical stimulation of the median nerve at 20 Hz for 2 min. During one of the fatigue tests, a concurrent sustained voluntary contraction of the contralateral elbow flexors was used to increase resting MAP (by 22%, on average). Although this change in blood pressure resulted in no significant change in mean fatigue for the group, changes in MAP with exercise (median nerve stimulation with and without voluntary contraction) correlated with changes in thenar muscle fatigue in seven subjects. For every 10% increase in MAP, fatigue was reduced by approximately 3%. The data suggest that low blood pressure after chronic cervical SCI and poor blood pressure control during exercise exacerbate the fatigability of paralyzed muscles.     

Quadriceps fatigue caused by catchlike-inducing trains is not altered in old age

The relative loss of peak force from electrical stimulation protocols has provided inconsistent results when used to compare muscle fatigability between young and old adults. In addition to the effect of task on these comparisons, age-related alterations in the development and relaxation of force are possible factors that have not been considered. The purposes of this study were to compare the fatigability of the quadriceps of young (26.7 +/- 1.0 years) and old men (78.3 +/- 1.3 years), as assessed by changes in peak force, force time integral (FTI), and half-relaxation time (HRT), during intermittent electrical stimulation protocols, and to determine whether manipulation of the activation frequency affected the comparisons. Fatigue was caused by constant-frequency (CF), and catchlike-inducing (CI) train protocols, both of which consisted of intermittent trains (6 pulses on: 650 ms off) of stimulation. After each protocol, the force-generating capacity of the fatigued muscle was assessed with three trains of stimuli: a CF train, a CI train and a 1-s 50-HZ train. There was no effect of age on the loss of peak force or the development of low-frequency fatigue induced by either protocol. Conversely, irrespective of the protocol, the FTI was better maintained by approximately 9% in the old than young men. Because peak force did not differ between groups during fatigue, it is likely that the FTI was preserved by the exacerbated slowing of HRT in the quadriceps of the old men. The results confirm an apparent paradox between muscle fatigue and stimulation with CI trains: a single CI train produces greater force than a CF train in a fatigued muscle, but there is greater fatigue induced by repetitive CI than CF train stimulation. Old age did not affect this fatigue paradox.     

Effects of fatiguing exercise on high-energy phosphates, force, and EMG: evidence for three phases of recovery

Experiments were designed to evaluate the relative contribution of impulse propagation failure, high-energy phosphate depletion, lowered pH, and impaired excitation-contraction coupling to human muscle fatigue and recovery. 31P nuclear magnetic resonance spectroscopy measurements were made on adductor pollicis muscle, together with simultaneous measurements of M-wave, force, and rectified integrated EMG (RIEMG). During fatigue, maximum voluntary contraction force (MVC) fell by 90%, pH fell from 7.1 to 6.4, and phosphocreatine was almost totally depleted. Neuromuscular efficiency (NME = force/RIEMG) was reduced to 40% of control at the end of the fatiguing contraction, and the M wave was reduced in amplitude and prolonged in duration. Following exercise, the M wave returned to normal within 4 minutes. pH, high-energy phosphates, and MVC recovered within 20 minutes. By contrast, neuromuscular efficiency did not recover within 60 minutes. These findings indicate three different components of fatigue. The first is reflected by the altered M wave and indicates impaired muscle membrane excitation and impulse propagation. The second, associated with reduced MVC, correlates with the metabolic state of the muscle (PCr and pH). The third, indicated by reduced NME, is independent of changes in high-energy phosphates and pH and is probably due to impaired excitation-contraction coupling.     

Fatigue-related changes in motor unit action potentials of adult cats.

The purpose of this study was to quantify the changes in motor-unit action potentials (MUAP) and force during a standard motor-unit fatigue test. MUAP waveforms were characterized by the measurement of amplitude, duration, area, and shape (as reflected in a coefficient of proportionality). Fatigue-resistant motor units exhibited small, but statistically significant, changes in MUAP amplitude and area during the fatigue test, whereas fatigable motor units displayed variable changes in MUAP amplitude, duration, and area. For all motor-unit types, the coefficient of proportionality did not change, and hence the change in MUAP area was proportional to the combined changes in amplitude and duration. The between- and within-train changes in MUAP were also distinct for the fatigue-resistant and fatigable motor units. Although several mechanisms could be responsible for the changes in the MUAP as the fatigue test proceeded, the dissociation of the time courses for MUAP and force indicated that these MUAP changes were not the principal reason for the decline in force under these conditions.     

Evaluation of central and peripheral factors in muscular fatigue

Muscular fatigue was investigated in 13 healthy people by employing a simple device which comprises a computer on line with a conventional EMG equipment able to automatically measure the frequency and duration of free-run EMG recording. The procedure was carried out in the extensor digitorum brevis muscle by using surface electrodes throughout 10 minutes of voluntary maximal effort. The maximal M wave as well as the muscle response to repetitive nerve maximal stimulation was also explored at the beginning and at the end of the experiment. It was observed a decrease of the potentials frequency discharge and an increase of their duration without major changes in the M wave amplitude neither in the muscle response to the repetitive nerve discharge. The findings pointed out to the central factors as the mean responsible for the development of muscular fatigue.     

Predictive model of muscle fatigue after spinal cord injury in humans

The fatigability of paralyzed muscle limits its ability to deliver physiological loads to paralyzed extremities during repetitive electrical stimulation. The purposes of this study were to determine the reliability of measuring paralyzed muscle fatigue and to develop a model to predict the temporal changes in muscle fatigue that occur after spinal cord injury (SCI). Thirty-four subjects underwent soleus fatigue testing with a modified Burke electrical stimulation fatigue protocol. The between-day reliability of this protocol was high (intraclass correlation, 0.96). We fit the fatigue index (FI) data to a quadratic-linear segmental polynomial model. FI declined rapidly (0.3854 per year) for the first 1.7 years, and more slowly (0.01 per year) thereafter. The rapid decline of FI immediately after SCI implies that a "window of opportunity" exists for the clinician if the goal is to prevent these changes. Understanding the timing of change in muscle endurance properties (and, therefore, load-generating capacity) after SCI may assist clinicians when developing therapeutic interventions to maintain musculoskeletal integrity.     

Impact of varying pulse frequency and duration on muscle torque production and fatigue

Neuromuscular electrical stimulation (NMES) involves the use of electrical current to facilitate contraction of skeletal muscle. However, little is known concerning the effects of varying stimulation parameters on muscle function in humans. The purpose of this study was to determine the extent to which varying pulse duration and frequency altered torque production and fatigability of human skeletal muscle in vivo. Ten subjects underwent NMES-elicited contractions of varying pulse frequencies and durations as well as fatigue tests using stimulation trains of equal total charge, yet differing parametric settings at a constant voltage. Total charge was a strong predictor of torque production, and pulse trains with equal total charge elicited identical torque output. Despite similar torque output, higher- frequency trains caused greater fatigue. These data demonstrate the ability to predictably control torque output by simultaneously controlling pulse frequency and duration and suggest the need to minimize stimulation frequency to control fatigue.     

Electrophysiologic changes during exercise testing in patients with chronic obstructive pulmonary disease

To determine whether skeletal muscle is involved in the exercise limitation of chronic obstructive pulmonary disease (COPD), we investigated electrical adaptations in muscle during incremental cycling exercise testing. Changes in quadriceps activity were compared using surface electromyography (SEMG) and motor point stimulation in ten COPD patients and ten healthy subjects. Patients showed significantly lower exercise capacity, and M-wave duration was increased from exercise onset (P < 0.05) with a parallel decrease in amplitude (P < 0.05). The SEMG power spectrum median frequency was always higher (P < 0.04) in patients and its decline was earlier (P < 0.01). The ratio of the root mean square of the SEMG to oxygen uptake was decreased (P < 0.001) during exercise in patients, although it remained constant in controls. Electromyographic parameters were significantly more involved in the exercise limitation than ventilatory factors. Thus, modified electrical activity in muscle appeared in COPD patients from exercise onset, indicating that skeletal muscle function is clearly implicated in the exercise intolerance of these patients.