scholarly journals The compensatory interaction between motor unit firing behavior and muscle force during fatigue

2016 ◽  
Vol 116 (4) ◽  
pp. 1579-1585 ◽  
Author(s):  
Paola Contessa ◽  
Carlo J. De Luca ◽  
Joshua C. Kline

Throughout the literature, different observations of motor unit firing behavior during muscle fatigue have been reported and explained with varieties of conjectures. The disagreement amongst previous studies has resulted, in part, from the limited number of available motor units and from the misleading practice of grouping motor unit data across different subjects, contractions, and force levels. To establish a more clear understanding of motor unit control during fatigue, we investigated the firing behavior of motor units from the vastus lateralis muscle of individual subjects during a fatigue protocol of repeated voluntary constant force isometric contractions. Surface electromyographic decomposition technology provided the firings of 1,890 motor unit firing trains. These data revealed that to sustain the contraction force as the muscle fatigued, the following occurred: 1) motor unit firing rates increased; 2) new motor units were recruited; and 3) motor unit recruitment thresholds decreased. Although the degree of these adaptations was subject specific, the behavior was consistent in all subjects. When we compared our empirical observations with those obtained from simulation, we found that the fatigue-induced changes in motor unit firing behavior can be explained by increasing excitation to the motoneuron pool that compensates for the fatigue-induced decrease in muscle force twitch reported in empirical studies. Yet, the fundamental motor unit control scheme remains invariant throughout the development of fatigue. These findings indicate that the central nervous system regulates motor unit firing behavior by adjusting the operating point of the excitation to the motoneuron pool to sustain the contraction force as the muscle fatigues.

1998 ◽  
Vol 23 (1) ◽  
pp. 87-94 ◽  
Author(s):  
Christopher Rich ◽  
George L. O′Brien ◽  
Enzo Cafarelli

Motor unit firing rates in human muscle can be determined from recordings made with small-diameter microelectrodes inserted directly into the muscle during voluntary contraction. Frequently, these counts are pooled to give an average motor unit firing rate under a given set of conditions. Since the fibers of one motor unit are dispersed among the cells of several others, it is conceivable that discharge rates can be measured in more than one cell from the same unit. If this occurred frequently, the distribution of firing rates could be influenced by those from units counted more than once. Based on literature values, we made the following assumptions: vastus lateralis contains approximately 300 motor units, with an average innervation ratio of 1500. Muscle cell diameter is about 50 to 100 μm and cells are randomly distributed over a motor unit territory of 10 μm diameter. The recording range of a microelectrode is about 600 μm. Given the distribution of cells normally found in whole human muscle, the probability of recording from two or more cells of the same motor unit at 50% MVC follows a Poisson distribution with a mean of 0.44. This model suggests that although there is a low probability of some duplication in this technique, the extent to which it influences the distribution of average motor unit firing rates is minimal over the entire range of forces produced by vastus lateralis. Key words: probability, motor unit, single unit recording, human muscle, rate coding


2004 ◽  
Vol 92 (5) ◽  
pp. 2878-2886 ◽  
Author(s):  
Ping Zhou ◽  
William Zev Rymer

The dependence of the form of the EMG-force relation on key motoneuron and muscle properties was explored using a simulation approach. Surface EMG signals and isometric forces were simulated using existing motoneuron pool, muscle force, and surface EMG models, based primarily on reported properties of the first dorsal interosseous (FDI) muscle in humans. Our simulation results indicate that the relation between electrical and mechanical properties of the individual motor unit level plays the dominant role in determining the overall EMG amplitude-force relation of the muscle, while the underlying motor unit firing rate strategy appears to be a less important factor. However, different motor unit firing rate strategies result in substantially different relations between counts of the numbers of motoneuron discharges and the isometric force. Our simulation results also show that EMG amplitude (estimated as the average rectified value) increases as a result of synchronous discharges of different motor units within the pool, but the magnitude of this increase is determined primarily by the action potential duration of the synchronized motor units. Furthermore, when the EMG effects are normalized to their maximum levels, motor unit synchrony does not exert significant effects on the form of the EMG-force relation, provided that the synchrony level is held similar at different excitation levels.


2013 ◽  
Vol 109 (6) ◽  
pp. 1548-1570 ◽  
Author(s):  
Paola Contessa ◽  
Carlo J. De Luca

We developed a model to investigate the influence of the muscle force twitch on the simulated firing behavior of motoneurons and muscle force production during voluntary isometric contractions. The input consists of an excitatory signal common to all the motor units in the pool of a muscle, consistent with the “common drive” property. Motor units respond with a hierarchically structured firing behavior wherein at any time and force, firing rates are inversely proportional to recruitment threshold, as described by the “onion skin” property. Time- and force-dependent changes in muscle force production are introduced by varying the motor unit force twitches as a function of time or by varying the number of active motor units. A force feedback adjusts the input excitation, maintaining the simulated force at a target level. The simulations replicate motor unit behavior characteristics similar to those reported in previous empirical studies of sustained contractions: 1) the initial decrease and subsequent increase of firing rates, 2) the derecruitment and recruitment of motor units throughout sustained contractions, and 3) the continual increase in the force fluctuation caused by the progressive recruitment of larger motor units. The model cautions the use of motor unit behavior at recruitment and derecruitment without consideration of changes in the muscle force generation capacity. It describes an alternative mechanism for the reserve capacity of motor units to generate extraordinary force. It supports the hypothesis that the control of motoneurons remains invariant during force-varying and sustained isometric contractions.


2003 ◽  
Vol 90 (5) ◽  
pp. 2919-2927 ◽  
Author(s):  
Alexander Adam ◽  
Carlo J. De Luca

Motor-unit firing patterns were studied in the vastus lateralis muscle of five healthy young men [21.4 ± 0.9 (SD) yr] during a series of isometric knee extensions performed to exhaustion. Each contraction was held at a constant torque level, set to 20% of the maximal voluntary contraction at the beginning of the experiment. Electromyographic signals, recorded via a quadrifilar fine wire electrode, were processed with the precision decomposition technique to identify the firing times of individual motor units. In repeat experiments, whole-muscle mechanical properties were measured during the fatigue protocol using electrical stimulation. The main findings were a monotonic decrease in the recruitment threshold of all motor units and the progressive recruitment of new units, all without a change of the recruitment order. Motor units from the same subject showed a similar time course of threshold decline, but this decline varied among subjects (mean threshold decrease ranged from 23 to 73%). The mean threshold decline was linearly correlated ( R2 ≥ 0.96) with a decline in the elicited peak tetanic torque. In summary, the maintenance of recruitment order during fatigue strongly supports the notion that the observed common recruitment adaptations were a direct consequence of an increased excitatory drive to the motor unit pool. It is suggested that the increased central drive was necessary to compensate for the loss in force output from motor units whose muscle fibers were actively contracting. We therefore conclude that the control scheme of motor-unit recruitment remains invariant during fatigue at least in relatively large muscles performing submaximal isometric contractions.


AGE ◽  
2016 ◽  
Vol 38 (3) ◽  
Author(s):  
Kohei Watanabe ◽  
Aleš Holobar ◽  
Motoki Kouzaki ◽  
Madoka Ogawa ◽  
Hiroshi Akima ◽  
...  

2000 ◽  
Vol 111 (12) ◽  
pp. 2196-2199 ◽  
Author(s):  
Yoshihisa Masakado ◽  
Kazuto Akaboshi ◽  
Akio Kimura ◽  
Naoichi Chino

2013 ◽  
Vol 48 (5) ◽  
pp. 806-813 ◽  
Author(s):  
Kohei Watanabe ◽  
Marco Gazzoni ◽  
Ales Holobar ◽  
Toshiaki Miyamoto ◽  
Kazuhito Fukuda ◽  
...  

2018 ◽  
Vol 119 (6) ◽  
pp. 2186-2193 ◽  
Author(s):  
Paola Contessa ◽  
John Letizi ◽  
Gianluca De Luca ◽  
Joshua C. Kline

The control of motor unit firing behavior during fatigue is still debated in the literature. Most studies agree that the central nervous system increases the excitation to the motoneuron pool to compensate for decreased force contributions of individual motor units and sustain muscle force output during fatigue. However, some studies claim that motor units may decrease their firing rates despite increased excitation, contradicting the direct relationship between firing rates and excitation that governs the voluntary control of motor units. To investigate whether the control of motor units in fact changes with fatigue, we measured motor unit firing behavior during repeated contractions of the first dorsal interosseous (FDI) muscle while concurrently monitoring the activation of surrounding muscles, including the flexor carpi radialis, extensor carpi radialis, and pronator teres. Across all subjects, we observed an overall increase in FDI activation and motor unit firing rates by the end of the fatigue task. However, in some subjects we observed increases in FDI activation and motor unit firing rates only during the initial phase of the fatigue task, followed by subsequent decreases during the late phase of the fatigue task while the coactivation of surrounding muscles increased. These findings indicate that the strategy for sustaining force output may occasionally change, leading to increases in the relative activation of surrounding muscles while the excitation to the fatiguing muscle decreases. Importantly, irrespective of changes in the strategy for sustaining force output, the control properties regulating motor unit firing behavior remain unchanged during fatigue. NEW & NOTEWORTHY This work addresses sources of debate surrounding the manner in which motor unit firing behavior is controlled during fatigue. We found that decreases in the motor unit firing rates of the fatiguing muscle may occasionally be observed when the contribution of coactive muscles increases. Despite changes in the strategy employed to sustain the force output, the underlying control properties regulating motor unit firing behavior remain unchanged during muscle fatigue.


2019 ◽  
Vol 122 (3) ◽  
pp. 1147-1162 ◽  
Author(s):  
Lara McManus ◽  
Matthew W. Flood ◽  
Madeleine M. Lowery

Motor unit firing times are weakly coupled across a range of frequencies during voluntary contractions. Coherent activity within the beta-band (15–35 Hz) has been linked to oscillatory cortical processes, providing evidence of functional connectivity between the motoneuron pool and motor cortex. The aim of this study was to investigate whether beta-band motor unit coherence is altered with increasing abduction force in the first dorsal interosseous muscle. Coherence between motor unit firing times, extracted from decomposed surface electromyography (EMG) signals, was investigated in 17 subjects at 10, 20, 30, and 40% of maximum voluntary contraction. Corresponding changes in nonlinear surface EMG features (specifically sample entropy and determinism, which are sensitive to motor unit synchronization) were also examined. A reduction in beta-band and alpha-band coherence was observed as force increased [ F(3, 151) = 32, P < 0.001 and F(3, 151) = 27, P < 0.001, respectively], accompanied by corresponding changes in nonlinear surface EMG features. A significant relationship between the nonlinear features and motor unit coherence was also detected ( r = −0.43 ± 0.1 and r = 0.45 ± 0.1 for sample entropy and determinism, respectively; both P < 0.001). The reduction in beta-band coherence suggests a change in the relative contribution of correlated and uncorrelated presynaptic inputs to the motoneuron pool, and/or a decrease in the responsiveness of the motoneuron pool to synchronous inputs at higher forces. The study highlights the importance of considering muscle activation when investigating changes in motor unit coherence or nonlinear EMG features and examines other factors that can influence coherence estimation. NEW & NOTEWORTHY Intramuscular alpha- and beta-band coherence decreased as muscle contraction force increased. Beta-band coherence was higher in groups of high-threshold motor units than in simultaneously active lower threshold units. Alterations in motor unit coherence with increases or decreases in force and with the onset of fatigue were accompanied by corresponding changes in surface electromyography sample entropy and determinism. Mixed-model analysis indicated mean firing rate and number of motor units also influenced the coherence estimate.


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