Properties of human motor units after prolonged activity at a constant firing rate

Abstract

The primary purpose of this study was to examine if there are changes in the intrinsic properties of spinal motoneurons after prolonged submaximal contractions. To do this, we assessed whether or not the synaptic drive to motoneurons needs to increase in order to maintain a constant firing rate of a motor unit. Recruitment of new units and an increase in total electromyographic (EMG) activity of the muscle of interest were taken as estimates of an increase in synaptic drive. Subjects were asked to maintain a constant firing rate of a clearly identifiable (targeted) motor unit from the first dorsal interosseous muscle for approximately 10 min, while surface EMG and force were recorded simultaneously. For the 60 units studied, the duration of the constant-firing-rate period ranged from 73 to 1,140 s (448 +/- 227 s; mean +/- SD). There was a significant increase ( t-test, p<0.001) in the magnitude of mean surface EMG, and DC force while the targeted motoneuron maintained a constant rate suggesting an increase in the net excitatory input to the motoneuron pool. Changes occurring simultaneously in other parameters, namely, variability in interspike interval, magnitude of force fluctuations, the duration of motor unit action potentials, and the median power frequency of surface EMG were also computed. The firing rates of 16 concurrently firing motoneurons, not controlled by the subject, remained constant. The key finding of this study is that after prolonged activity, a motoneuron requires a stronger excitatory input to maintain its firing rate. Additional results are indicative of significant changes in the characteristics of the synaptic inputs, changes at the neuromuscular junction (both pre- and postsynaptic regions) and the sarcolemma.

Motor Unit Rotation in a Variety of Human Muscles

“…The inability to observe substitution or rotation is suggested to result from their experimental protocols. For example, in the paper by Smith (1934), an effort to discharge the target motor unit was increased continuously, which maintained the activity of that unit, and recruited additional units, similar to the results reported in a recent study by Johnson et al (2004). Later studies that have claimed substitution and rotation to occur (Basmajian 1973;Fallentin et al 1993;Person 1974;Thomas et al 1978) have actually observed switching between motor units within a complex muscle when the subject switched tasks (Loeb 1985;Riek and Bawa 1992).…”

“…These observations suggest changes in the intrinsic properties of higher-threshold motoneurons that render them incapable of further discharge. It has also been shown that a motoneuron requires stronger synaptic input to maintain a constant firing rate (Johnson et al 2004). If synaptic input is not increased, the firing rate of a motoneuron first decreases (Enoka et al 1989) and then the motoneuron ceases to fire.…”

Fatigue-Sensitive Afferents Inhibit Extensor but Not Flexor Motoneurons in Humans

“…In animals, when motoneurons are repetitively stimulated by sustained intracellular currents, many cells either reduce their discharge or stop firing (Kernell and Monster, 1982a,b;Spielmann et al, 1993;Sawczuk et al, 1997). Similarly, in humans, the synaptic drive necessary to maintain repetitive firing of single motor units increases during weak contractions (Johnson et al, 2004). Therefore, several mechanisms probably contribute to changes in motoneuron excitability observed during fatiguing contractions, and different mechanisms are likely to be more prominent at different times during a sustained contraction (Gandevia, 2001).…”

Serotonin spillover onto the axon initial segment of motoneurons induces central fatigue by inhibiting action potential initiation

“…It is often studied during maximal voluntary contractions (5, 6, 9). Nevertheless, it is also present during weak physical contraction (1,2,8,(10)(11)(12). Central fatigue secures rotation of motor units (13) and prevents hyperactivity of muscles (6).…”

“…The force produced by muscles decreases in part because of the lack of glycogen (3) in the muscle and/or failures at the neuromuscular junctions (4). In addition to this well-described muscle fatigue, motor fatigue also involves an element originating in the CNS (5)(6)(7)(8). This "central fatigue" is characterized by a decreased ability to contract the muscle fibers adequately during a motor activity and is observed independently of the muscle fatigue (6).…”