Thorsten Rudroff

Unraveling the neurophysiology of muscle fatigue

Despite 100years of research since the seminal work of Angelo Mosso (1846-1910), our understanding of the interactions between the nervous system and muscle during the performance of fatiguing contractions remains rather rudimentary. Although the nervous system simply needs to provide an activation signal that will elicit the net muscle torque required for a prescribed action, changes in the number and diversity of synaptic inputs that must be integrated by the spinal motor neurons to accommodate the changes in the force-producing capabilities of the muscle fibers complicate the process of generating the requisite activation signal. This brief review examines two ways in which the activation signal can be compromised during sustained contractions and thereby contribute to the rate at which the muscles fatigue. These examples provide insight on the types of adjustments that occur in the nervous system during fatiguing contractions, but emphasize that much remains to be learned about the physiological processes that contribute to the phenomenon known as muscle fatigue.

NET EXCITATION OF THE MOTOR UNIT POOL VARIES WITH LOAD TYPE DURING FATIGUING CONTRACTIONS

To identify the underlying physiological mechanisms for the difference in the time to failure for two types of fatiguing contractions, 20 subjects performed force and position tasks with the elbow flexor muscles at a comparable net muscle torque for a similar duration. Prior to terminating each task, blood flow was occluded to estimate the relative amount of feedback transmitted by small‐diameter afferents to the spinal cord. Mean arterial pressure at the conclusion of the fatiguing contraction increased similarly for the two tasks (force: 119% ± 14%; position: 114% ± 15%). However, the final values for the electromyographic activity for the elbow flexor muscles (26% ± 14% and 21% ± 11%, respectively; P < 0.05), and the increase in the fluctuations in acceleration and force (225% ± 152% and 154% ± 53%, respectively; P < 0.05) in the sagittal plane, were significantly greater during the position task compared with the force task. These results suggest a different balance in the excitatory and inhibitory inputs to the spinal motor neurons for the two tasks, which has implications for the design of work tasks and exercise prescription in rehabilitation. Muscle Nerve, 2005

Load type influences motor unit recruitment in biceps brachii during a sustained contraction

Twenty subjects participated in four experiments designed to compare time to task failure and motor-unit recruitment threshold during contractions sustained at 15% of maximum as the elbow flexor muscles either supported an inertial load (position task) or exerted an equivalent constant torque against a rigid restraint (force task). Subcutaneous branched bipolar electrodes were used to record single motor unit activity from the biceps brachii muscle during ramp contractions performed before and at 50 and 90% of the time to failure for the position task during both fatiguing contractions. The time to task failure was briefer for the position task than for the force task (P=0.0002). Thirty and 29 motor units were isolated during the force and position tasks, respectively. The recruitment threshold declined by 48 and 30% (P=0.0001) during the position task for motor units with an initial recruitment threshold below and above the target force, respectively, whereas no significant change in recruitment threshold was observed during the force task. Changes in recruitment threshold were associated with a decrease in the mean discharge rate (-16%), an increase in discharge rate variability (+40%), and a prolongation of the first two interspike intervals (+29 and +13%). These data indicate that there were faster changes in motor unit recruitment and rate coding during the position task than the force task despite a similar net muscle torque during both tasks. Moreover, the results suggest that the differential synaptic input observed during the position task influences most of the motor unit pool.

Electromyographic measures of muscle activation and changes in muscle architecture of human elbow flexors during fatiguing contractions

The study compared changes in intramuscular and surface recordings of EMG amplitude with ultrasound measures of muscle architecture of the elbow flexors during a submaximal isometric contraction. Ten subjects performed a fatiguing contraction to task failure at 20% of maximal voluntary contraction force. EMG activity was recorded in biceps brachii, brachialis, and brachioradialis muscles using intramuscular and surface electrodes. The rates of increase in the amplitude of the surface EMG for the long and short heads of biceps brachii and brachioradialis were greater than those for the intramuscular recordings measured at different depths. The amplitude of the intramuscular recordings from three muscles increased at a similar rate (P = 0.13), as did the amplitude of the three surface recordings from two muscles (P = 0.83). The increases in brachialis thickness (27.7 +/- 5.7 to 30.9 +/- 3.5 mm; P < 0.05) and pennation angle (10.9 +/- 3.5 to 16.5 +/- 4.8 degrees ; P = 0.003) were not associated with the increase in intramuscular EMG amplitude (P > 0.58). The increase in brachioradialis thickness (22.8 +/- 4.8 to 25.5 +/- 3.4 mm; P = 0.0075) was associated with the increase in the amplitude for one of two intramuscular EMG signals (P = 0.007, r = 0.79). The time to failure was more strongly associated with the rate of increase in the amplitude of the surface EMG than that for the intramuscular EMG, which suggests that the surface measurement provides a more appropriate measure of the change in muscle activation during a fatiguing contraction.

Muscle activity and time to task failure differ with load compliance and target force for elbow flexor muscles

The primary purpose of this study was to determine the influence of load compliance on time to failure during sustained isometric contractions performed with the elbow flexor muscles at four submaximal target forces. Subjects pulled against a rigid restraint during the force task and maintained a constant elbow angle, while supporting an equivalent inertial load during the position task. Each task was sustained for as long as possible. Twenty-one healthy adults (23 ± 6 yr; 11 men) participated in the study. The maximal voluntary contraction (MVC) force was similar (P = 0.95) before the subjects performed the force and position tasks at each of the four target forces: 20, 30, 45, and 60% of MVC force. The time to task failure was longer for the force tasks (576 ± 80 and 325 ± 70 s) than for the position tasks (299 ± 77 and 168 ± 35 s) at target forces of 20 and 30% (P < 0.001), but was similar for the force tasks (178 ± 35 and 86 ± 14 s) and the position tasks (132 ± 29 and 87 ± 14 s) at target forces of 45 and 60% (P > 0.19). The briefer times to failure for the position task at the lower forces were accompanied by greater rates of increase in elbow flexor muscle activity, mean arterial pressure, heart rate, and rating of perceived exertion. There was no difference in the estimates of external mechanical work at any target force. The dominant mechanisms limiting time to failure of sustained isometric contractions with the elbow flexor muscles appear to change at target forces between 30 and 45% MVC, with load compliance being a significant factor at lower forces only.

Time to failure of a sustained contraction is predicted by target torque and initial electromyographic bursts in elbow flexor muscles

The purpose of the study was to identify factors that could predict differences among individuals in the time to failure of a submaximal contraction. Twenty subjects (10 men, 25 ± 6 years) supported an inertial load equivalent to 20% of the maximal voluntary contraction (MVC) force with the elbow flexor muscles for as long as possible. The time to failure was predicted by the frequency of electromyographic bursts in the long head of biceps brachii during the first 20% of the contraction, the amplitude of bursts in the brachioradialis during the first 20% of the contraction, and the target torque. Subjects who could sustain the task longer exhibited greater initial (first 20% of contraction) electromyographic burst frequency in the long head of biceps brachii, lower initial burst amplitudes in the brachioradialis muscle, and lower target torque. Knowing the main predictors of a submaximal fatiguing contraction with the elbow flexor muscles may assist clinicians in personalizing therapeutic interventions. Muscle Nerve, 2007

PET/CT imaging of age- and task-associated differences in muscle activity during fatiguing contractions.

The study compared positron emission tomography/computed tomography (PET/CT) of [(18)F]-2-fluoro-2-deoxy-D-glucose ([(18)F]-FDG) uptake by skeletal muscles and the amount of muscle activity as indicated by surface electromyographic (EMG) recordings when young and old men performed fatiguing isometric contractions that required either force or position control. EMG signals were recorded from thigh muscles of six young men (26 ± 6 yr) and six old men (77 ± 6 yr) during fatiguing contractions with the knee extensors. PET/CT scans were performed immediately after task failure. Glucose uptake in 24 leg muscles, quantified as standardized uptake values, was greater for the old men after the force task and differed across tasks for the young men (force, 0.64 ± 0.3 g/ml; position, 0.73 ± 0.3 g/ml), but not the old men (force, 0.84 ± 0.3 g/ml; position, 0.79 ± 0.26 g/ml) (age × task interaction; P < 0.001). In contrast, the rate of increase in EMG amplitude for the agonist muscles was greater for the young men during the two contractions and there was no difference for either group of subjects in the rate of increase in EMG amplitude across the two tasks. The imaging estimates of glucose uptake indicated age- and task-dependent differences in the spatial distribution of [(18)F]-FDG uptake by skeletal muscles during fatiguing contractions. The findings demonstrate that PET/CT imaging of [(18)F]-FDG uptake, but not surface EMG recordings, detected the modulation of muscle activity across the fatiguing tasks by the young men but not the old men.

Positron emission tomography detects greater blood flow and less blood flow heterogeneity in the exercising skeletal muscles of old compared with young men during fatiguing contractions

The results of previous studies that attempted to demonstrate the effects of ageing on skeletal muscle blood flow are controversial because these studies used indirect assessments of skeletal muscle blood flow obtained via whole limb blood flow measurements that provide no information on the distribution of blood flow within particular muscles. We used positron emission tomography to measure blood flow per gram of muscle in old and young men with similar levels of physical activity. Resting muscle blood flow was similar in both groups and exercising muscle blood flow was greater and less heterogeneous in the older men. Old and young men achieved similar maximal voluntary contraction forces and endurance times during two types of fatiguing isometric task. These findings indicate that physically active old men have intact neural drive to the muscle and achieve adequate exercise hyperaemia despite the age‐induced decrease in their muscle volume.

Core muscle characteristics during walking of patients with multiple sclerosis.

The purpose of this study was to investigate core muscle characteristics during walking in patients with multiple sclerosis (MS). Eight patients (4 men) with relapsing-remitting MS (aged 44.9 +/- 8.6 yr) and sex-matched controls (37.9 +/- 8.4 yr) walked on a treadmill for 15 min at a self-selected speed. Positron emission tomography/computed tomography imaging was used to measure core muscle activity immediately after walking based on glucose uptake. Activity was not different between the MS and control group for any of the identified muscles (p > 0.28). Within the MS group, side differences in activity were identified in the lateral flexor group, the external and internal obliques, and the rectus abdominis (p < 0.05), with the less-affected side being activated more. Furthermore, greater muscle volume was found on the more-affected side of the transversus abdominis, quadratus lumborum, and the low-back extensor group (p < 0.03). These muscle characteristics suggest patients with MS utilize compensatory mechanisms during walking to maintain balance and posture. These strategies likely result in increased muscle energy cost and early fatigability.

Pronation-supination torque and associated electromyographic activity varies during a sustained elbow flexor contraction but does not influence the time to task failure

In this study we measured the pronation–supination torque, flexion force, and electromyographic activity in elbow flexor muscles during an isometric contraction in which a submaximal elbow flexion force was kept constant for as long as possible. Ten subjects performed the contraction at 20% of maximal voluntary contraction (MVC) torque until failure. Electromyographic (EMG) activity of the long and short heads of biceps brachii, brachialis, brachioradialis, and triceps brachii was recorded with surface and intramuscular electrodes. The mean time to failure was 8.2 ± 6.2 min. The fluctuations in flexion force and pronation–supination torque were correlated (r range = 0.68–0.92), and subjects exhibited a range of pronation–torque profiles that were not associated with the time to failure. Knowing the influence of concurrent actions about the pronation–supination axis during a submaximal fatiguing contraction with the elbow flexor muscles has implications for the design of workstations in ergonomic settings and in the prescription of activities for rehabilitation programs. Muscle Nerve 40: 231–239, 2009