Jacques Duchateau

Muscle fatigue: what, why and how it influences muscle function

Much is known about the physiological impairments that can cause muscle fatigue. It is known that fatigue can be caused by many different mechanisms, ranging from the accumulation of metabolites within muscle fibres to the generation of an inadequate motor command in the motor cortex, and that there is no global mechanism responsible for muscle fatigue. Rather, the mechanisms that cause fatigue are specific to the task being performed. The development of muscle fatigue is typically quantified as a decline in the maximal force or power capacity of muscle, which means that submaximal contractions can be sustained after the onset of muscle fatigue. There is even evidence that the duration of some sustained tasks is not limited by fatigue of the principal muscles. Here we review experimental approaches that focus on identifying the mechanisms that limit task failure rather than those that cause muscle fatigue. Selected comparisons of tasks, groups of individuals and interventions with the task‐failure approach can provide insight into the rate‐limiting adjustments that constrain muscle function during fatiguing contractions.

Changes in single motor unit behaviour contribute to the increase in contraction speed after dynamic training in humans

1 The adaptations of the ankle dorsiflexor muscles and the behaviour of single motor units in the tibialis anterior in response to 12 weeks of dynamic training were studied in five human subjects. In each training session ten series of ten fast dorsiflexions were performed 5 days a week, against a load of 30–40 % of the maximal muscle strength. 2 Training led to an enhancement of maximal voluntary muscle contraction (MVC) and the speed of voluntary ballistic contraction. This last enhancement was mainly related to neural adaptations since the time course of the muscle twitch induced by electrical stimulation remained unaffected. 3 The motor unit torque, recorded by the spike‐triggered averaging method, increased without any change in its time to peak. The orderly motor unit recruitment (size principle) was preserved during slow ramp contraction after training but the units were activated earlier and had a greater maximal firing frequency during voluntary ballistic contractions. In addition, the high frequency firing rate observed at the onset of the contractions was maintained during the subsequent spikes after training. 4 Dynamic training induced brief (2–5 ms) motor unit interspike intervals, or ‘doublets’. These doublets appeared to be different from the closely spaced (±10 ms) discharges usually observed at the onset of the ballistic contractions. Motor units with different recruitment thresholds showed doublet discharges and the percentage of the sample of units firing doublets was increased by training from 5.2 to 32.7 %. The presence of these discharges was observed not only at the onset of the series of spikes but also later in the electromyographic (EMG) burst. 5 It is likely that earlier motor unit activation, extra doublets and enhanced maximal firing rate contribute to the increase in the speed of voluntary muscle contraction after dynamic training.

Motor unit behaviour and contractile changes during fatigue in the human first dorsal interosseus

1 In 67 single motor units, the mechanical properties, the recruitment and derecruitment thresholds, and the discharge rates were recorded concurrently in the first dorsal interosseus (FDI) of human subjects during intermittent fatiguing contractions. The task consisted of isometric ramp‐and‐hold contractions performed at 50% of the maximal voluntary contraction (MVC). The purpose of this study was to examine the influence of fatigue on the behaviour of motor units with a wide range of activation thresholds. 2 For low‐threshold (< 25% MVC) motor units, the mean twitch force increased with fatigue and the recruitment threshold either did not change or increased. In contrast, the twitch force and the activation threshold decreased for the high‐threshold (> 25% MVC) units. The observation that in low‐threshold motor units a quick stretch of the muscle at the end of the test reset the unit force and recruitment threshold to the prefatigue value suggests a significant role for fatigue‐related changes in muscle stiffness but not twitch potentiation or motor unit synchronization. 3 Although the central drive intensified during the fatigue test, as indicated by an increase in surface electromyogram (EMG), the discharge rate of the motor units during the hold phase of each contraction decreased progressively over the course of the task for motor units that were recruited at the beginning of the test, especially the low‐threshold units. In contrast, the discharge rates of newly activated units first increased and then decreased. 4 Such divergent behaviour of low‐ and high‐threshold motor units could not be individually controlled by the central drive to the motoneurone pool. Rather, the different behaviours must be the consequence of variable contributions from motoneurone adaptation and afferent feedback from the muscle during the fatiguing contraction.

Some aspects of the acute phase response after a marathon race, and the effects of glutamine supplementation

Abstract Strenuous exercise may be associated with immune suppression. However, the underlying mechanism is not known. A decrease in the plasma level of glutamine, which is utilised at a high rate by cells of the immune system, and an increase in the plasma level of some cytokines may impair immune functions such as lymphocyte proliferation after prolonged, exhaustive exercise. In two separate studies of the Brussels marathon, using similar protocols, the time course of the changes in the plasma concentrations of some amino acids (glutamine, glutamate, alanine, tryptophan and branched chain amino acids), acute phase proteins and cytokines (interleukins IL-1α, IL-2, IL-6, tumour necrosis factor type a) was measured in male athletes. The numbers of circulating leucocytes and lymphocytes were also measured. Amino acid and cytokine concentrations have not previously been measured concomitantly in marathon runners; the measurement of some of these parameters the morning after the marathon (16 h) is novel. Another novel feature is the provision of glutamine versus placebo to marathon runners participating in the second study. In both studies the plasma concentrations of glutamine, alanine and branched chain amino acids were decreased immediately after and 1 h after the marathon. Plasma concentrations of all amino acids returned to pre-exercise levels by 16 h after exercise. The plasma concentration of the complement anaphylotoxin C5a increased to abnormal levels after the marathon, presumably due to tissue damage activating the complement system. There was also an increase in plasma C-reactive protein 16 h after the marathon. The plasma levels of IL-1α were unaffected by the exercise, while that of IL-2 was increased 16 h after exercise. Plasma IL-6 was increased markedly (≈ 45-fold) immediately after and at 1 h after exercise. Neopterine, a macrophage activation marker, was significantly increased post-exercise. There was a marked leucocytosis immediately after the marathon, which returned to normal 16 h later. At the same time there was a decrease in the number of T-lymphocytes, which was further reduced within 1 h to below pre-exercise levels. Glutamine supplementation, as administered in the second study, did not appear to have an effect upon lymphocyte distribution.

Age-related decline in rate of torque development is accompanied by lower maximal motor unit discharge frequency during fast contractions

The aim of this study was to investigate the association between the rate of torque development and maximal motor unit discharge frequency in young and elderly adults as they performed rapid submaximal contractions with the ankle dorsiflexors. Recordings were obtained of the torque exerted by the dorsiflexors during the isometric contractions and the surface and intramuscular electromyograms (EMGs) from the tibialis anterior. The maximal rate of torque development and integrated EMG (percentage of total EMG burst) at peak rate of torque development during fast contractions were lower in elderly than young adults by 48% (P < 0.05) and 16.5% (P < 0.05), respectively. The young adults, but not the elderly adults, exhibited a positive association (r2 = 0.33; P < 0.01) between the integrated EMG computed up to the peak rate of torque development and the maximal rate of torque development achieved during the fast contractions. These age-related changes during fast voluntary contractions were accompanied by a decline (P < 0.001) in motor unit discharge frequency (19, 28, and 34% for first 3 interspike intervals, respectively) and in the percentage of units (45%; P < 0.05) that exhibited double discharges (doublets) at brief intervals (<5 ms). Because aging decreased the maximal rate of torque development of fast voluntary contractions to a greater extent ( approximately 10%) than that of an electrically evoked twitch, collectively the results indicate that the age-related decline in maximal motor unit discharge frequency likely limit, in addition to the slowing of muscle contractile properties, the performance of fast voluntary contractions.

Effect of static stretch training on neural and mechanical properties of the human plantar flexor muscles

To determine the contributions of neural and mechanical mechanisms to the limits in the range of motion (ROM) about a joint, we studied the effects of 30 sessions of static stretch training on the characteristics of the plantar‐flexor muscles in 12 subjects. Changes in the maximal ankle dorsiflexion and the torque produced during passive stretching at various ankle angles, as well as maximal voluntary contraction (MVC) and electrically induced contractions, were recorded after 10, 20, and 30 sessions, and 1 month after the end of the training program. Reflex activities were tested by recording the Hoffmann reflex (H reflex) and tendon reflex (T reflex) in the soleus muscle. Training caused a 30.8% (P < 0.01) increase in the maximal ankle dorsiflexion. This improved flexibility was associated (r2 = 0.88; P < 0.001) with a decrease in muscle passive stiffness and, after the first 10 sessions only, with a small increase in passive torque at maximal dorsiflexion. Furthermore, both the H‐ and T‐reflex amplitudes were reduced after training, especially the latter (−36% vs. −14%; P < 0.05). The MVC torque and the maximal rate of torque development were not affected by training. Although the changes in flexibility and passive stiffness were partially maintained 1 month after the end of the training program, reflex activities had already returned to control levels. It is concluded that the increased flexibility results mainly from reduced passive stiffness of the muscle–tendon unit and tonic reflex activity. The underlying neural and mechanical adaptation mechanisms, however, showed different time courses. Muscle Nerve 29: 248–255, 2004

Motor unit recruitment order during voluntary and electrically induced contractions in the tibialis anterior

Abstract The recruitment order of motor units (MU) was compared during voluntary and electrically induced contractions. With the use of spike-triggered averaging, a total of 302 MUs with recruitment thresholds ranging from 1% to 88% of maximal voluntary contraction were recorded in the human tibialis anterior muscle in five subjects. The mean (±SD) MU force was 98.3±93.3 mN (mean torque 16.8±15.9 mNm) and the mean contraction time (CT) 46.2±12.7 ms. The correlation coefficients (r) between MU twitch force and CT versus the recruitment threshold in voluntary contractions were +0.68 and –0.38 (P<0.001), respectively. In voluntary contractions, MUs were recruited in order of increasing size except for only 6% of the cases; whereas, during transcutaneous electrical stimulation (ES) at the muscle motor point, MU pairs showed a reversal of recruitment order in 28% and 35% of the observations, respectively, when the pulse durations were 1.0 ms or 0.1 ms. This recruitment reversal during ES was not related to the magnitude of the difference in voluntary recruitment thresholds between MUs. It is concluded that if the reversal of MU recruitment observed during ES is biophysically controlled by differences in their nerve axon input impedance, in percutaneous stimulation at the motor point, other factors such as the size and the morphological organisation of the axonal branches can also influence the order of activation.

Behaviour of short and long latency reflexes in fatigued human muscles.

1. The human abductor pollicis brevis (APB) and first dorsal interosseus (FDI) were fatigued by sustained maximal voluntary contractions and, in the case of the APB also by electrically induced (30 Hz) contractions, until the loss of force reached 50% of control. The short latency or Hoffmann reflex (H reflex) and the long latency reflex (LLR) were evoked during weak voluntary contractions by the electrical stimulation of the median nerve at the wrist in control, during and after the fatigue experiments. 2. As compared to control, the normalized H reflex amplitude in the two fatigue modalities was found to have decreased by 30% without any significant change in the LLR. This finding and the observation that the LLR was enhanced by 46% in simultaneous recordings, in which the APB remained at rest during FDI fatigue, could be explained by a stronger descending fatigue‐induced central drive which spreads to neighbouring non‐fatigued muscles. 3. A comparison of the H reflex and the LLR behaviour during fatigue indicates that motoneurone activation threshold is not affected but that changes in peripheral drive are present, which possibly induce presynaptic inhibition of Ia afferents and/or inhibition of interneurones in the oligosynaptic pathways. Our observation of a rather slow time course for the H reflex decrease during fatigue supports the point of view that these inhibitions are activated by metabolic and/or chemical changes in the fatigued muscle. 4. It is concluded from the results of this study that muscle fatigue induces an enhanced descending supraspinal drive which compensates for a loss of excitation from the peripheral afferents on motoneurones.

Neuromuscular Electrical Stimulation and Voluntary Exercise

SummaryNeuromuscular electrical stimulation (NMES) has been in practice since the eighteenth century for the treatment of paralysed patients and the prevention and/or restoration of muscle function after injuries, before patients are capable of voluntary exercise training. More recently NMES has been used as a modality of strengthening in healthy subjects and highly trained athletes, but it is not clear whether NMES is a substitute for, or a complement to, voluntary exercise training. Moreover the discussion of the mechanisms which underly the specific effects of NMES appears rather complex at least in part because of the disparity in training protocols, electrical stimulation regimens and testing procedures that are used in the various studies.It appears from this review of the literature that in physical therapy, NMES effectively retards muscle wasting during denervation or immobilisation and optimises recovery of muscle strength during rehabilitation. It is also effective in athletes with injured, painful limbs, since NMES contributes to a shortened rehabilitation time and aids a safe return to competition. In healthy muscles, NMES appears to be a complement to voluntary training because it specifically induces the activity of large motor units which are more difficult to activate during voluntary contraction. However, there is a consensus that the force increases induced by NMES are similar to, but not greater than, those induced by voluntary training. The rationale for the complementarity between NMES and voluntary exercise is that in voluntary contractions motor units are recruited in order, from smaller fatigue resistant (type I) units to larger quickly fatiguable (type II) units, whereas in NMES the sequence appears to be reversed.As a training modality NMES is, in nonextreme situations such as muscle denervation, not a substitute for, but a complement of, voluntary exercise of disused and healthy muscles.

Muscle fatigue and the mechanisms of task failure.

HUNTER, S. K., J. DUCHATEAU, and R. M. ENOKA. Muscle fatigue and the mechanisms of task failure. Exerc. Sport Sci. Rev., Vol. 32, No. 2, pp. 44–49, 2004. An alternative approach in the study of muscle fatigue is to address the question, “What causes task failure during a fatiguing contraction?” This approach is described by considering how variation in the type of load supported and contraction intensity influence both the time to task failure and the centrally mediated adjustments in reflex activity and motor unit behavior.