For the past five decades there has been wide acceptance of a relationship between the firing rate of motor units and the afterhyperpolarization of motoneurons. It has been promulgated that the higher-threshold, larger-soma, motoneurons fire faster than the lower-threshold, smaller-soma, motor units. This relationship was based on studies on anesthetized cats with electrically stimulated motoneurons. We questioned its applicability to motor unit control during voluntary contractions in humans. We found that during linearly force-increasing contractions, firing rates increased as exponential functions. At any time and force level, including at recruitment, the firing rate values were inversely related to the recruitment threshold of the motor unit. The time constants of the exponential functions were directly related to the recruitment threshold. From the Henneman size principle it follows that the characteristics of the firing rates are also related to the size of the soma. The "firing rate spectrum" presents a beautifully simple control scheme in which, at any given time or force, the firing rate value of earlier-recruited motor units is greater than that of later-recruited motor units. This hierarchical control scheme describes a mechanism that provides an effective economy of force generation for the earlier-recruited lower force-twitch motor units, and reduces the fatigue of later-recruited higher force-twitch motor units-both characteristics being well suited for generating and sustaining force during the fight-or-flight response.

During isometric contractions, the fluctuation of the force output of muscles increases as the muscle fatigues, and the contraction is sustained to exhaustion. We analyzed motor unit firing data from the vastus lateralis muscle to investigate which motor unit control parameters were associated with the increased force fluctuation. Subjects performed a sequence of isometric constant-force contractions sustained at 20% maximal force, each spaced by a 6-s rest period. The contractions were performed until the mean value of the force output could not be maintained at the desired level. Intramuscular EMG signals were detected with a quadrifilar fine-wire sensor. The EMG signals were decomposed to identify all of the firings of several motor units by using an artificial intelligence-based set of algorithms. We were able to follow the behavior of the same motor units as the endurance time progressed. The force output of the muscle was filtered to remove contributions from the tracking task. The coefficient of variation of the force was found to increase with endurance time (P < 0.001, R(2) = 0.51). We calculated the coefficient of variation of the firing rates, the synchronization of pairs of motor unit firings, the cross-correlation value of the firing rates of pairs of motor units, the cross-correlation of the firing rates of motor units and the force, and the number of motor units recruited during the contractions. Of these parameters, only the cross-correlation of the firing rates (P < 0.01, R(2) = 0.10) and the number of recruited motor units (P = 0.042, R(2) = 0.22) increased significantly with endurance time for grouped subjects. A significant increase (P < 0.001, R(2) = 0.16) in the cross-correlation of the firing rates and force was also observed. It is suggested that the increase in the cross-correlation of the firing rates is likely due to a decrease in the sensitivity of the proprioceptive feedback from the spindles.

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.

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.