Motor unit recruitment strategies and muscle properties determine the influence of synaptic noise on force steadiness

Abstract

Motoneurons receive synaptic inputs from tens of thousands of connections that cause membrane potential to fluctuate continuously (synaptic noise), which introduces variability in discharge times of action potentials. We hypothesized that the influence of synaptic noise on force steadiness during voluntary contractions is limited to low muscle forces. The hypothesis was examined with an analytical description of transduction of motor unit spike trains into muscle force, a computational model of motor unit recruitment and rate coding, and experimental analysis of interspike interval variability during steady contractions with the abductor digiti minimi muscle. Simulations varied contraction force, level of synaptic noise, size of motor unit population, recruitment range, twitch contraction times, and level of motor unit short-term synchronization. Consistent with the analytical derivations, simulations and experimental data showed that force variability at target forces above a threshold was primarily due to low-frequency oscillations in neural drive, whereas the influence of synaptic noise was almost completely attenuated by two low-pass filters, one related to convolution of motoneuron spike trains with motor unit twitches (temporal summation) and the other attributable to summation of single motor unit forces (spatial summation). The threshold force above which synaptic noise ceased to influence force steadiness depended on recruitment range, size of motor unit population, and muscle contractile properties. This threshold was low (<10% of maximal force) for typical values of these parameters. Results indicate that motor unit recruitment and muscle properties of a typical muscle are tuned to limit the influence of synaptic noise on force steadiness to low forces and that the inability to produce a constant force during stronger contractions is mainly attributable to the common low-frequency oscillations in motoneuron discharge rates.

A dominant role for mechanical resonance in physiological finger tremor revealed by selective minimization of voluntary drive and movement

“…We do not think that our study shows tremor under isometric conditions. We think it is a small component of force fluctuation due to poorly fused motor unit activity at firing frequency (Dideriksen et al 2012). However, we cannot say categorically that a central oscillator never operates in isometric conditions.…”

The optimal neural strategy for a stable motor task requires a compromise between level of muscle cocontraction and synaptic gain of afferent feedback

“…However, only the component of this variability that is common among a sufficiently large proportion of the active motor units is reflected in the force (Dideriksen et al 2012;Farina et al 2014;Negro et al 2009). The common input to the motor neurons is classically quantified as the common drive and has been demonstrated across several muscles (e.g., De Luca et al 1982;Mochizuki et al 2006;Semmler et al 1997).…”

The extraction of neural strategies from the surface EMG: an update

“…For example, the linear correlation in the frequency domain (coherence) between EEG (or other cortical signals) and concurrently recorded EMG has been extensively used to quantify the strength of corticospinal input to motor neurons (2,9,47,92). The connection is indicated by the value of EEG-EMG coherence in the beta band (15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30). Similarly, the coherence between EMG signals recorded from two muscles has been used to assess the strength and frequency of the common synaptic input received by the motor neurons innervating the two muscles (6, 10, 24).…”