Motor unit recruitment and proprioceptive feedback decrease the common drive

Abstract

It has been documented that concurrently active motor units fire under the control of a common drive. That is, the firing rates show high correlation with near-zero time lag. This degree of correlation has been found to vary among muscles and among contractions performed at different force levels in the same muscle. This study provides an explanation indicating that motor units recruited during a contraction cause an increase in the variation (SD) and a decrease in the degree (amplitude) of the correlation of the firing rates. The degree of correlation is lower in muscles having greater spindle density. This effect appears to be mediated by the proprioceptive feedback from the spindles and possibly the Golgi tendon organs. Muscle spindles in particular respond to the mechanical excitation of the nonfused muscle fibers and provide a discordant excitation to the homonymous motoneurons, resulting in a decrease in the correlation of the firing rates of motor units. The implication of this work is that the decreased correlation of the firing rates in some muscles is not necessarily an indication of a decreased common drive from the CNS, but rather an inhibitory influence of the proprioceptive feedback from the peripheral nervous system. This explanation is useful for understanding various manifestations of the common drive reported in the literature.

FIG. 1.

The firing rates of 4 motor units (MUs) detected from the first dorsal interosseous (FDI) muscle during an isometric constant-force contraction at the 20% MVC level performed by a 24-yr-old subject. The top trace represents the force of the contraction. The contraction lasted 50 s and the time axis is segmented. The firing rates are smoothed with a low-pass filter having a 2-Hz cutoff frequency. The smoothing was applied to provide a more distinguishable representation of the firing rates. Note that the firing rates fluctuate in unison with no apparent phase lag, indicating the presence of a “common drive.”

FIG. 2.

A: instantaneous cross-correlation function of the firing rates of 2 MUs from the contraction in Fig. 1. Note that the peak of this function for each time instance occurs at or near a time lag of 0 s and that the amplitude of the peak is not constant throughout the contraction. The dark line represents the isometric constant force of the FDI. B: a contour-level representation of the instantaneous cross-correlation function. The location of the peak of the instantaneous cross-correlation function is easily identified as being near 0-s time lag. Note that the amplitude of the function varies throughout the contraction. C: the ensemble of the maxima instantaneous cross-correlation (MIC) functions, representing the time course of the common drive, of all the possible MU pairs in the contraction shown in Fig. 1. Note that they all fluctuate during their time course. The MIC function shown as a blue trace was derived from the instantaneous cross-correlation function shown in the top panel.

FIG. 3.

A: an example of a MIC function containing a significant decrease (P < 0.05) of 0.1 unit (see text for details) in the neighborhood of a MU recruited at t = 12 s. The shaded area indicates the duration (8 s) of the smoothing window used to derive the MIC function. Note that the beginning of the decrease coincides with the beginning of the smoothing window, 4 s prior to the actual recruitment time. This lead effect is caused by the smoothing window applied to the instantaneous cross-correlation function from which the MIC function is derived. B: the firing rate (in pulses per second) of the 2 MUs used to calculate the above-shown MIC function and the firing rate of the newly recruited MU at t = 12 s. It can be seen that prior to the recruitment, the firing rates are fluctuating in unison with no apparent delay. However, soon after recruitment the firing rates begin to lose their well-coordinated phase and amplitude relationship and appear to be discordant. This behavior is highlighted by the shaded elliptical region and is quantified by the MIC function. The duration of the smoothing window is shown above the firing rates. It can be seen that the discordant firing rates take effect on the MIC function as soon as the leading edge of the smoothing window intersects them at the time of recruitment. The MIC function value calculated at this time is placed at the time corresponding to half of the window length, i.e., 4 s. Consequently, this is the earliest an effect can be registered on the MIC function. (However, if the discordant behavior of the firing rates is weak or is slightly delayed and the correlation of the firing rates prior to the recruitment time is progressively increasing, then the effect will be noticed later, i.e., between 4 s prior to recruitment and the time of recruitment.)

FIG. 4.

In this figure the symbol represents the mean value, the box represents the SE, and the bars represent the SD of the MIC amplitude and SD values calculated across subjects and contractions for different muscles, each of which is represented by a different symbol. A: the SD of the MIC function of the firing rates vs. the average number of MUs that are recruited during the contraction. Note that the slope of the linear regression is significantly (P < 0.042) greater than zero and has an R² value of 0.685. The vales for the 2 FDI contractions (filled circle and square) are significantly different (P < 0.005). B: the SD of the MIC function of the firing rates vs. the spindle density in each muscle measured in number of spindles per gram of muscle. The SD values appear to be unrelated to the spindle density. C: the amplitude of the MIC function of the firing rates vs. the average number of MUs that are recruited during the contraction. Note that the regression among the muscles is poor (R² = 0.012) and the slope is not significantly different from zero (P < 0.837). However, within the same muscle (the FDI) the amplitude of the MIC function decreases as the number of recruited MUs increases. The values for the FDI in the ramp-force contractions (filled circle) and the FDI constant-force contractions (filled square) are significantly different (P < 0.001). D: the amplitude of the MIC function of the firing rates vs. the spindle density in each muscle measured in number of spindles per gram of muscle. Note that the amplitude decreases as the spindle density increases. The slope of the linear regression is significantly (P < 0.017) greater than zero and has an R² value of 0.888.