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.

Keywords: firing rate; force; motor neuron; motor unit; saturation.

Fig. 1.

Example recording from biceps motor unit (MU). A: isometric force exerted by biceps muscle (bottom trace), intramuscular electromyography (IEMG) signal recorded in biceps muscle depicting discharge of a single MU (middle trace), and instantaneous (dots) and moving average (1-s window; line) firing rate of recorded unit (top trace). Vertical dashed lines indicate period during which force was increasing yet MU firing rate had leveled off at a firing rate of ∼15 impulses/s (imp/s). B: plot of instantaneous firing rate vs. muscle force for the unit shown in A. Force was normalized to a percentage of the maximum voluntary contraction (% MVC) force. Data were fit with a rising exponential (red line) of the form represented by Eq. 1. Parameters derived from this fit were recruitment threshold force (F_th), firing rate at recruitment threshold (R_min), maximum rate (R_max), and force constant (Φ).

Fig. 2.

Example recording depicting firing rate saturation in 2 MUs. Isometric force (bottom trace), IEMG signal (middle trace), and instantaneous firing rates of the 2 units detected in the IEMG signal (top traces). The firing rates of both units leveled off despite continued increase in muscle force. In addition, unit 2 was recruited at a time when the firing rate of unit 1 had saturated.

Fig. 3.

Firing rate-force relation for 133 biceps MUs. A: each trace indicates the firing rate-force relation for an individual MU. Force is normalized as % MVC. Black traces indicate MUs (n = 123) whose firing rate-force data were significantly better fit by a rising exponential function (Eq. 1) than a linear function. Red traces indicate MUs (n = 10) whose firing rate data were best fit by a linear function. B: for improved clarity, firing rate-force relations shown in A are redrawn for a force range up to 2.5% MVC.

Fig. 4.

Relation between stimulus frequency and isometric force. A: mean (SD) steady-state elbow flexion force exerted during submaximal stimulation of biceps at different pulse frequencies using intramuscular electrodes. Force increased as a sigmoid function of stimulus frequency with maximum force attained at a stimulus frequency of ∼30 imp/s. B: histogram depicting maximum firing rates recorded during ramp contractions in 123 MUs that exhibited saturating firing rate responses (black traces in Fig. 3). Average maximum rate (14.8 imp/s) is depicted as a vertical dashed line projecting to A. Based on the force-stimulus frequency curve in A, MUs discharging at this average maximum rate would likely generate ∼63% of their force capacity.

Fig. 5.

Response of single biceps MU to tendon vibration. Subject voluntarily increased firing of unit to different initial rates (indicated by horizontal dashed lines): ∼10 (A), ∼11 (B), and ∼15 imp/s (C). Vibration was then applied to the biceps tendon (vertical dashed lines). Traces from bottom to top show elbow flexion force, intramuscular EMG signal, discriminated MU spikes, moving average (1-s window) MU firing rate, and noncalibrated acceleration signal indicating application of vibration. There was a marked increase in firing rate with vibration in A and B but no detectable change in rate in C despite clear evidence of vibration-mediated increase in muscle force. D: traces from C are redrawn and extended to show subsequent period of voluntary increase in muscle force. Once the unit reached a discharge rate of ∼15 imp/s, additional increases in firing rate were not observed in response to enhanced excitation mediated by tendon vibration or voluntary drive.

Fig. 6.

Quantification of vibration-mediated changes in firing rate. Example recording of biceps MU responding to tendon vibration illustrates quantification. The initial rate was determined as the average spike rate in a 2-s window (black vertical dashed lines) immediately before vibration. The vibration rate was calculated as the average spike rate in a 2-s window (red vertical dashed lines) 0.5 s after the onset of vibration. The difference in firing rate (Δrate) was calculated as the difference between the vibration rate and initial rate. Traces from bottom to top show elbow flexion force, intramuscular EMG signal, discriminated MU spikes, moving average (0.5-s window) MU firing rate, and noncalibrated acceleration signal indicating application of vibration.

Fig. 7.

Vibration-mediated changes in firing rate as a function of initial rate. A: Δrate induced by tendon vibration for 362 total trials recorded in 96 MUs plotted as a function of the initial (i.e., previbration) firing rate. The firing rate change evoked by tendon vibration decreased as the initial rate on which the vibration was superimposed increased. Line shows linear regression (P < 0.001). B: average change in isometric force (Δforce) caused by tendon vibration for the same 362 trials shown in A. Linear regression was not significant (P = 0.16). Dashed line indicates average magnitude of vibration-induced force.