Roger M. Enoka

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.

Mechanisms that contribute to differences in motor performance between young and old adults

This paper examines the physiological mechanisms responsible for differences in the amplitude of force fluctuations between young and old adults. Because muscle force is a consequence of motor unit activity, the potential mechanisms include both motor unit properties and the behavior of motor unit populations. The force fluctuations, however, depend not only on the age of the individual but also on the muscle group performing the task, the type and intensity of the muscle contraction, and the physical activity status of the individual. Computer simulations and experimental findings performed on tasks that involved single agonist and antagonist muscles suggest that differences in force fluctuations are not attributable to motor unit twitch force, motor unit number, or nonuniform activation of the agonist muscle, but that they are influenced by the variability and common modulation of motor unit discharge in both the agonist and antagonist muscles. Because the amplitude of the force fluctuations does not vary linearly with muscle activation, these results suggest that multiple mechanisms contribute to the differences in force fluctuations between young and old adults, although the boundary conditions for each mechanism remain to be determined.

Steadiness is reduced and motor unit discharge is more variable in old adults

The purpose of this study was to compare the steadiness and discharge rate of motor units during submaximal contractions performed by young and old adults. Subjects performed isometric and slow shortening and lengthening contractions with the first dorsal interosseous muscle. The steadiness of the isometric and slow anisometric contractions was less for the old subjects compared with young subjects, especially at the lower target forces and with the lightest loads. Furthermore, the steadiness of the lengthening contractions was less compared with the shortening contractions for the old subjects. Although the mean discharge rates of motor units were not different for the two groups of subjects, the variability of the discharge rates was greater for the old subjects during the isometric and anisometric contractions. We conclude that a more variable discharge by single motor units probably contributes to the reduced ability of old adults to perform steady muscle contractions.

Impairment of neuromuscular propagation during human fatiguing contractions at submaximal forces.

1. The purpose of the study was to examine the dependence of neuromuscular propagation impairment on the level of isometric force sustained to the endurance limit. The task involved human volunteers sustaining a submaximal abduction force with the index finger by activating the first dorsal interosseous muscle as long as possible. 2. The submaximal force was sustained at one of three levels (20, 35 or 65% of maximum) by increasing motor unit activity, as indicated by the electromyogram (EMG), during the fatiguing contraction. Although the EMG increased during the fatiguing contraction, the EMG was significantly less than maximum at the endurance limit for all subjects (deficit of 19‐55% of maximum). This deficit was inversely related to the level of the sustained submaximal force. 3. The maximum voluntary contraction and twitch forces were significantly reduced following the fatiguing contraction. As with the EMG, the degree of force reduction was greatest for the subjects who sustained the low target forces. 4. The fatiguing contraction caused a 12‐23% decline in M wave amplitude, a 33‐51% increase in M wave duration, and no change in M wave area. The decline in M wave amplitude, which is an index of neuromuscular propagation impairment, was greatest among the subjects who sustained the low target forces. 5. The mean power frequency of the EMG decreased by a similar amount (50‐57%) during the fatiguing contraction for all three groups of subjects. 6. A model representing the interaction of processes that enhance and impair force was developed to explain the recovery of twitch force following the sustained contractions at different target forces. 7. We conclude that the fatigue experienced by a subject when force is sustained at a submaximal value does involve an impairment of neuromuscular propagation. This impairment is one factor that limits muscle excitation during a submaximal, fatiguing contraction and contributes to the diminished force capability by the end of the fatigue task.

Neural adaptations with chronic physical activity.

Chronic activity patterns, such as strength training, limb immobilization, and aging, produce marked adaptations in both the muscular and nervous systems. In this brief review, some of the involved mechanisms are examined as they are revealed through studies on the maximality, specificity, and pattern of the neural drive to muscle. The studies on maximality indicate that it is difficult to activate maximally a muscle by voluntary command, the capacity varies across muscles, tasks, and training, and the maximum discharge rates of motor neurons decreases with immobilization and increases with strength training. The data on specificity demonstrate that: strength can be increased by training with imagined contractions; the velocity specificity of isokinetic training is evident with intended contractions; the strength training influences the untrained homologous muscle in the contralateral limb; the bilatral deficit can become a bilateral facilitation with appropriate training; and that eccentric contractions appear to involve a different activation scheme compared to isometric and concentric contractions. Finally, the literature on the pattern of the neural drive suggests that: coactivation varies with training and often decreases as skill level increases; measures of motor-unit synchronization reveal changes in neuronal connectivity with physical training; the reflex potentiation varies across muscles, individuals, and activity patterns; the modulation of the H-reflex amplitude with training involves changes in the motor neuron; and the motor neurons exhibit a bistable, excitability property that may be influenced by exercise. Despite the breadth of this evidence, there remain substantial gaps in our knowledge, particularly regarding the symmetry of adaptations with increased and decreased chronic physical activity.

Muscle strength and its development. New perspectives

SummarySkeletal muscle undergoes substantial adaptation when it is subjected to a strength training regimen. At one extreme, these effects are manifested as profound morphological changes, such as those exemplified by bodybuilders. However, it is possible to increase strength without any change in muscle size. This dissociation underscores the notion that strength is not solely a property of muscle but rather it is a property of the motor system. The nervous system seems to be of paramount importance for the expression and development of strength. Indeed, it is probable that increases in strength can be achieved without morphological changes in muscle but not without neural adaptations. This review focuses on the role of the nervous system in the development of strength. In the strength literature, 3 topics exemplify the importance of the nervous system in strength development. These 3 topics are considered in detail in the review: electromyostimulation, cross-training effects, and EMG-force relationships. Evidence is presented from several different paradigms emphasising the significant contribution of neural mechanisms to the gains in strength with short term training. Although little is known about the specific neural mechanisms associated with strength training adaptations, the literature emphasises that the measure of human performance known as strength can be influenced by a variety of neurophysiological processes.

MOTOR UNIT PHYSIOLOGY: SOME UNRESOLVED ISSUES

The purpose of this review was to examine three issues that limit our understanding of motor unit physiology: (1) the range and distribution of the innervation ratios in a muscle; (2) the association between discharge rate and force; and (3) the variation in motor unit activity across contractions that differ in speed and type. We suggest that if more data were available on these issues, the understanding of neuromuscular function would be enhanced substantially, especially with regard to plasticity in the motor neuron pool, adequacy of the neural drive to muscle, and flexibility of activation patterns across various types of contractions. Current data are limited and these limitations influence our ability to interpret adaptations in muscle function in health and disease.

Estimating the strength of common input to human motoneurons from the cross‐correlogram.

1. The relationship between the motor unit discharge pattern (rate and variability) and synchronization of motor unit pairs was studied in the first dorsal interosseus muscle of human subjects. In separate trials of up to 4 min duration, subjects voluntarily controlled the mean discharge rate of an identified motor unit at one of several prescribed rates (range 7.5‐17.5 Hz). 2. The effect of discharge rate on the synchronous peak in the cross‐correlogram was examined in eighty motor unit pairs from six subjects. Five commonly used synchronization indices were used to quantify synchrony in the cross‐correlograms constructed from different discharge‐rate trials. For each synchronization index, the apparent magnitude of synchrony increased at lower motor unit discharge rates. The synchronization indices were not equally sensitive to discharge rate; increases in the different indices ranged from 72 to 494% between the highest and lowest discharge rates. 3. A model of the membrane potential trajectory underlying rhythmic motoneuron discharge was used to explain the observed increase in the magnitude of the synchronization indices at lower discharge rates. The essential feature of this model is that the probability of a common‐input EPSP causing a synchronous discharge in two motoneurons is independent of discharge rate. This means that the number of synchronous action potentials in excess of chance in any trial depends on the properties of the common‐input EPSPs and the duration of the trial, but is not related to motor unit discharge rates. The model also demonstrated that when the excess synchronous counts are normalized to motor unit discharge rate, or baseline counts in the histogram (as in the conventional synchronization indices), the magnitude of the index increases when the motor unit discharge rates are low. 4. The strength of common input to motoneurons could be misinterpreted if conventional synchronization indices are used because of discharge‐rate effects. The model was used to derive an index of the strength of common input to motoneurons (CIS) that was independent of motor unit discharge rate. CIS is the frequency of synchronous action potentials in the motor unit pair in excess of those expected due to chance (calculated during periods of tonic discharge in both units). The mean CIS in first dorsal interosseus motor unit pairs ranged from 0.052 to 1.005 extra synchronous action potentials per second across subjects. 5. Discharge variability was correlated with each of the synchronization indices and the CIS.(ABSTRACT TRUNCATED AT 400 WORDS)

Fatigue and fatigability in neurologic illnesses: proposal for a unified taxonomy.

Fatigue is commonly reported in many neurologic illnesses, including multiple sclerosis, Parkinson disease, myasthenia gravis, traumatic brain injury, and stroke. Fatigue contributes substantially to decrements in quality of life and disability in these illnesses. Despite the clear impact of fatigue as a disabling symptom, our understanding of fatigue pathophysiology is limited and current treatment options rarely lead to meaningful improvements in fatigue. Progress continues to be hampered by issues related to terminology and assessment. In this article, we propose a unified taxonomy and a novel assessment approach to addressing distinct aspects of fatigue and fatigability in clinical and research settings. This taxonomy is based on our current knowledge of the pathophysiology and phenomenology of fatigue and fatigability. Application of our approach indicates that the assessment and reporting of fatigue can be clarified and improved by utilizing this taxonomy and creating measures to address distinct aspects of fatigue and fatigability. We review the strengths and weaknesses of several common measures of fatigue and suggest, based on our model, that many research questions may be better addressed by using multiple measures. We also provide examples of how to apply and validate the taxonomy and suggest directions for future research.

Relative activation of two human elbow flexors under isometric conditions: a cautionary note concerning flexor equivalence

SummaryWe examined the electromyographic (EMG) activity of two human elbow-flexor muscles, biceps brachii and brachioradialis, during isometric contractions. The task required subjects to match the EMG level of one of the muscles (the control muscle) to one of four target levels (5, 10, 15, or 20% of maximum) at various elbow angles. A new technique was developed for the target-matching task. The activity of the other muscle (the test muscle) was simultaneously recorded during the task. For the notion of flexor equivalence to be supported, the EMG levels for the two muscles should have covaried. This was not the case. The results revealed three features: (1) while the control-muscle EMG remained constant across joint angles, the test-muscle EMG varied with joint angle, and the trend of this variation differed among subjects; (2) in nine out of ten subjects the trend of test-muscle EMG variation with joint angle was reversed when the other muscle served as the test muscle; and (3) the testmuscle EMG associated with the four target levels was subject-, muscle-, and angle-dependent. These results caution against the generalization of the flexor equivalent concept to isometric conditions. In particular, the activity of one muscle is not a reliable indicator of the activity of other muscles subserving the same joint action.