Distinguishing intrinsic from extrinsic factors underlying firing rate saturation in human motor units

Abstract

During voluntary contraction, firing rates of individual motor units (MUs) increase modestly over a narrow force range beyond which little additional increase in firing rate is seen. Such saturation of MU discharge may be a consequence of extrinsic factors that limit net synaptic excitation acting on motor neurons (MNs) or may be due to intrinsic properties of the MNs. Two sets of experiments involving recording of human biceps brachii MUs were carried out to evaluate saturation. In the first set, the extent of saturation was quantified for 136 low-threshold MUs during isometric ramp contractions. Firing rate-force data were best fit by a saturating function for 90% of MUs recorded with a maximum rate of 14.8 ± 2.0 impulses/s. In the second set of experiments, to distinguish extrinsic from intrinsic factors underlying saturation, we artificially augmented descending excitatory drive to biceps MNs by activation of muscle spindle afferents through tendon vibration. We examined the change in firing rate caused by tendon vibration in 96 MUs that were voluntarily activated at rates below and at saturation. Vibration had little effect on the discharge of MUs that were firing at saturation frequencies but strongly increased firing rates of the same units when active at lower frequencies. These results indicate that saturation is likely caused by intrinsic mechanisms that prevent further increases in firing rate in the presence of increasing synaptic excitation. Possible intrinsic cellular mechanisms that limit firing rates of motor units during voluntary effort are discussed.

Inhibition linearizes firing rate responses in human motor units: implications for the role of persistent inward currents

“…This finding is nearly identical to that reported previously for a population of 136 human biceps brachii MUs (Fuglevand et al . ). In contrast, during the ascending phase of contractions involving sural nerve stimulation, the proportion of MUs with firing rate profiles best fitted by exponential functions (11/23) was similar to that designated as linear (9/23) and not significantly different from that expected by chance (Fig.…”

“…Previously, we have shown that force and firing rate data for individual MUs during graded increases in isometric force are typically best fitted as a saturating function in the form of a rising exponential (Fuglevand et al . ). As such, we first fitted each phase of force–firing rate data for each trial with an equation of that form: where R ( F ) represents the rate ( R ) of spiking as a function of muscle force ( F ), R max is the maximum rate of spiking, e is the base of the natural logarithms, F is normalized isometric force, F th is the threshold force at which a unit begins to discharge, and R min is the minimum rate of spiking at recruitment threshold.…”

“…We found, however, that augmenting descending excitatory drive to MNs with peripheral excitation mediated by tendon vibration had little effect on the discharge of MUs whose firing rates had already saturated, but robustly increased firing rates of the same units when active at lower rates (Fuglevand et al . ). Those results suggested that firing rate saturation is probably caused by mechanisms intrinsic to MNs.…”

Onion Skin or Common Drive?

“…Increasing the firing rate above this rate is not compatible with optimal contraction control (Bigland-Ritchie and Woods, 1984). Therefore, the rate saturation observed by many researchers in low-threshold human MUs is not surprising (Bigland and Lippold, 1954; Gydikov and Kosarov, 1974; Monster and Chan, 1977; Bellemare et al, 1983; Moritz et al, 2005; Bailey et al, 2007; Fuglevand et al, 2015). …”

Neural Contributions to Muscle Fatigue

“…Therefore, the working mean firing rate range varies a remarkable 8-10 fold, although muscle seems most responsive to rates between 10 and 40 Hz (30), and these are the more frequently recorded rates from large numbers of MUs.…”