Andrew J. Fuglevand

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.

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)

Re-evaluation of muscle wisdom in the human adductor pollicis using physiological rates of stimulation

Motor unit discharge rates decline by about 50 % over 60 s of a sustained maximum voluntary contraction (MVC). It has been suggested that this decline in discharge rate serves to maintain force by protecting against conduction failure and by optimizing the input to motor units as their contractile properties change. This hypothesis, known as muscle wisdom, is based in part on studies in which muscle force was shown to decline more rapidly when stimulation was maintained at a high rate than when stimulus rate was reduced over time. The stimulus rates used in those studies, however, were higher than those normally encountered during MVCs. The purpose of this study was to compare force loss under constant and declining stimulus rate conditions using rates similar to those that occur during voluntary effort. Isometric force and surface EMG signals were recorded from human adductor pollicis muscles in response to supramaximal stimuli delivered to the ulnar nerve at the elbow. Three fatigue protocols, each 60 s in duration, were carried out on separate days on each of 10 subjects: (1) continuous stimulation at 30 Hz, (2) stimulation at progressively decreasing rates from 30 to 15 Hz and (3) sustained MVC. The relative force–time integral (endurance index) was significantly smaller for the sustained MVC (0.75 ± 0.08) and decreasing stimulus rate conditions (0.76 ± 0.16) compared to the condition in which stimulus rate was maintained at 30 Hz (0.90 ± 0.13). These findings suggest that decreases in discharge rate may contribute to force decline during a sustained MVC.

Cessation of human motor unit discharge during sustained maximal voluntary contraction

The purpose of this study was to determine whether cessation of motor unit discharge contributes to fatigue in human subjects. Multiple fine-wire and tungsten microelectrodes were inserted into the extensor digitorum or extensor indicis muscles of the forearm in an attempt to record the activity of the same motor unit from different locations within either muscle while subjects maintained a maximal voluntary contraction of the finger extensors until force dropped by approximately 50%. The activities of 13 motor units were followed for extended periods during the fatigue task. Of these, six appeared to cease discharging prior to the end of the task, which could not be attributed to electrode movement. These findings suggest that some motor neurons may not be able to discharge continuously in the presence of sustained volitional synaptic drive or that excitatory drive may diminish during maximal voluntary effort.

Discharge behaviour of single motor units during maximal voluntary contractions of a human toe extensor

1 While it is known that the average firing rate of a population of motoneurones declines with time during a maximal voluntary contraction, at least for many muscles, it is not known how the firing patterns of individual motoneurones adapt with fatigue. To address this issue we used tungsten microelectrodes to record spike trains (mean ±s.e.m., 183 ± 27 spikes per train; range, 100–782 spikes) from 26 single motor units in extensor hallucis longus during sustained (60–180 s) maximal dorsiflexions of the big toe in seven human subjects. 2 Long spike trains were recorded from 13 units during the first 30 s of a maximal voluntary contraction (mean train duration, 9.6 ± 1.2 s; range, 3.6–21.9 s) and from 13 units after 30 s (mean train duration, 16.6 ± 3.7 s; range, 7.1–58.1 s). Maximal isometric force generated by the big toe declined to 78.3 ± 6.3 % of its control level by 60–90 s and to 39.5 ± 1.4 % of control by 120–150 s. Despite this substantial fatigue, mean firing rates did not change significantly over time, declining only slightly from 15.8 ± 0.7 Hz in the first 30 s to 14.0 ± 0.5 Hz by 60–90 s and 13.6 ± 0.3 Hz by 120–150 s. 3 To assess fatigue‐related adaptation in discharge frequency and variability of individual motor units, each spike train was divided into 2–15 equal segments containing at least 50 interspike intervals. Discharge variability was measured from the coefficient of variation (s.d./mean) in the interspike intervals, with the s.d. being calculated using a floating mean of 19 consecutive intervals. Adaptation was computed as the average change in firing rate or variability that would occur for each 1 s of activity. There were no systematic changes in either firing rate or variability with time. 4 We conclude that single motoneurones supplying the extensor hallucis longus, a muscle comprised primarily of slow twitch muscle units, show little adaptation in firing with fatigue, suggesting that a progressive reduction in firing rate is not an invariable consequence of the fatigue associated with sustained maximal voluntary contractions.

Role of intertendinous connections in distribution of force in the human extensor digitorum muscle

The human extensor digitorum (ED) muscle gives rise distally to multiple tendons that insert onto and extend digits 2–5. It has been shown previously that the spike‐triggered average forces of motor units in ED are broadly distributed across many tendons. Such force dispersion may result from linkages between the distal tendons of ED and may limit the ability to move the fingers independently. The purpose of this study, therefore, was to determine the extent to which the connections between tendons of ED distribute force across the fingers. Stimulation of ED muscle fibers was performed at 107 different sites in four subjects. The isometric force exerted on digits 2–5 resulting from the stimulation was measured separately. Stimulus‐triggered averaging of each of the four force channels yielded the force contribution to each of the digits due to the stimulation at each site. A selectivity index from 0 (a site that distributes force equally across the fingers) to 1.0 (a site that produces force on a single finger) was computed to describe the distribution of force across the four fingers. The selectivity index resulting from electrical stimulation of ED averaged 0.70 ± 0.21. These selectivity index values were significantly greater (P < 0.001) than those obtained for single motor units using spike‐triggered averaging. These findings suggest that linkages between the distal tendons of ED probably play only a minor role in distributing force across the fingers and, therefore, other factors must be primarily responsible for the inability to move the fingers independently. Muscle Nerve 28: 614–622, 2003

Intramuscular Electrical Stimulation of Facial Muscles in Humans and Chimpanzees: Duchenne Revisited and Extended

The pioneering work of Duchenne (1862/1990) was replicated in humans using intramuscular electrical stimulation and extended to another species (Pan troglodytes: chimpanzees) to facilitate comparative facial expression research. Intramuscular electrical stimulation, in contrast to the original surface stimulation, offers the opportunity to activate individual muscles as opposed to groups of muscles. In humans, stimulation resulted in appearance changes in line with Facial Action Coding System (FACS) action units (AUs), and chimpanzee facial musculature displayed functional similarity to human facial musculature. The present results provide objective identification of the muscle substrate of human and chimpanzee facial expressions- data that will be useful in providing a common language to compare the units of human and chimpanzee facial expression.

Common Input across Motor Nuclei Mediating Precision Grip in Humans

Short-term synchrony was measured for pairs of motor units located within and across muscles activated during a task that mimicked precision grip in the dominant and nondominant hands of human subjects. Surprisingly, synchrony for pairs of motor units residing in separate muscles (flexor pollicis longus, a thumb muscle, and flexor digitorum profundus, an index-finger muscle) was just as large as that for pairs of units both within the thumb muscle. Furthermore, the high level of synchrony seen across muscles in the dominant hand was absent in the nondominant hand. These results suggest that descending pathways diverge to provide extensive common input across motor nuclei involved in the precision grip and that such divergence might contribute to the preferred use of one hand over the other.

Limitations of the surface electromyography technique for estimating motor unit synchronization

Motor unit synchronization was estimated from the surface electromyograms (EMG) of the first dorsal interosseus muscle of human volunteers by a simplified surface-EMG technique (Milner-Brown et al. 1973, 1975). Single motor units were identified from intramuscular recordings and were used to obtain a spike-triggered average of the surface-EMG. The discharge rate of a reference motor unit was controlled at two levels (high and low), and the effect of motor unit activity on the surface-EMG estimate of synchronization was studied in 56 motor units. The surface-EMG estimate of motor unit synchronization was significantly higher when the reference motor unit discharged at the high rate than when it discharged at the low rate. A regression analysis indicated that the synchronization ratio calculated from the surface EMG was significantly correlated with the level of EMG activity in the muscle. Motor unit synchronization was also estimated from surface-EMG measurements that were derived by computer simulation. The simulation permitted manipulation of motor unit activity (discharge rate and recruitment) with a complete absence of synchrony among the units in the pool. The stimulated surface-EMG index was influenced by an artifact associated with signal rectification, and this effect changed non-monotonically with motor unit activity. Furthermore, the increase in the motor unit activity reduced the signal-to-noise ratio of the spike-triggered surface EMG average, and consequently decreased the sensitivity of the surface-EMG index as an estimate of motor unit synchronization. We conclude that the simplified surface-EMG method (Milner-Brown et al. 1973, 1975) does not provide a useful index of motor unit synchronization due to its inability to accurately distinguish the synchronization from methodological effects related to a rectification artifact and variation in the signal-to-noise ratio.