Periodic modulation of motor-unit activity in extrinsic hand muscles during multidigit grasping

Abstract

We recently examined the extent to which motor units of digit flexor muscles receive common input during multidigit grasping. This task elicited moderate to strong motor-unit synchrony (common input strength, CIS) across muscles (flexor digitorum profundus, FDP, and flexor pollicis longus, FPL) and across FDP muscle compartments, although the strength of this common input was not uniform across digit pairs. To further characterize the neural mechanisms underlying the control of multidigit grasping, we analyzed the relationship between firing of single motor units from these hand muscles in the frequency domain by computing coherence. We report three primary findings. First, in contrast to what has been reported in intrinsic hand muscles, motor units belonging to different muscles and muscle compartments of extrinsic digit flexors exhibited significant coherence in the 0- to 5- and 5- to 10-Hz frequency ranges and much weaker coherence in the higher 10-20 Hz range (maximum 0.0025 and 0.0008, respectively, pooled across all FDP compartment pairs). Second, the strength and incidence of coherence differed considerably across digit pairs. Third, contrary to what has been reported in the literature, across-muscle coherence can be stronger and more prevalent than within-muscle coherence, as FPL-FDP2 (thumb-index digit pair) exhibited the strongest and most prevalent coherence in our data (0.010 and 43% at 3 Hz, respectively). The heterogeneous organization of common input to these muscles and muscle compartments is discussed in relation to the functional role of individual digit pairs in the coordination of multiple digit forces in grasping.

FIG. 1

Grip device. The frontal and side views of the device used to measure normal forces and horizontal torques is shown.

FIG. 2

Motor-unit activity during object hold. A: raw electromyographic (EMG) data from the index finger compartment of FDP (FDP2; top) and a thumb flexor (FPL; bottom). B: motor units discriminated from each raw EMG trace and their respective instantaneous firing rates (bottom and top, respectively). C: the action potentials of the discriminated motor units (1347 and 1144 from FDP2 and FPL EMG records, respectively). D: the interspike interval (ISI) distributions of each motor unit. The data shown in A and B are from a smaller recording period than the entire duration of the object hold trial (∼4 min). All traces are from the same subject (subject 3).

FIG. 3

Comparison of time and frequency domain analysis. A--C, middle: the cross-correlograms computed on motor-unit pairs from FPL–FDP3, FPL–FDP2, and FDP4–FDP5 (subjects 5, 3, and 4, respectively). The CIS values are given as well as the peak start and end times (in italics). Top: the cumulative sum (cusum) of the counts in each cross-correlogram used to define the peak region. Vertical dotted lines delineate the peak duration. Bottom: the coherence between the same motor-unit pairs used to compute the cross-correlograms above. The values on the y axis are the magnitude of the motor-unit coherence across the frequency range of interest (x axis; bin width = 0.78 Hz). Horizontal dotted line indicates the 95% confidence limit above which the magnitude of the coherence is defined as statistically significant.

FIG. 4

Incidence and pooled coherence. A and B: the incidence of significant coherence and pooled coherence, respectively, for all motor-unit pairs from across FDP compartment and FPL–FDP compartment combinations (left and right, respectively). ⋯ , the 95% confidence level. C: the difference between the Fisher transformed pooled coherencies of B, left and right (across FDP compartments and across FPL-FDP, respectively). Values falling outside the 95% confidence interval (⋯) indicate a significant difference between the 2 pooled coherencies at that frequency.

FIG. 5

Pooled coherence from individual digit pair combinations. Plots in A and B show pooled coherence computed on motor units from FPL–FDP compartment and from FDP compartment combinations, respectively. ⋯ , the 95% confidence limit.

FIG. 6

Significant differences in pooled coherence for all digit pair comparisons. A–C: the magnitude of the significant differences between digit pairs from within 0–5, 5–10, and 10 –20 Hz, respectively. The magnitudes of significant difference were quantified as the area outside the confidence intervals of the difference plot (e.g., Fig. 4C). White and black indicate no difference and maximum difference, respectively (0 and 0.1 on the grayscale bar). Note that the darker squares indicate that the pooled coherence from the digit pairs on the horizontal axis are greater than those computed from the digit pairs on the vertical axis. Index, middle, ring, little fingers and the thumb are denoted I, M, R, L, and T, respectively.

FIG. 7

Strength of motor unit synchrony and coherence. Each data point represents the average motor unit synchrony (CIS; vertical axis) and pooled coherence averaged within 0–5 Hz (A), 5–10 Hz (B), and 10–20 Hz (C) frequency ranges (horizontal axis) for each of the 10 digit pair combinations. Vertical error bars indicate the SD of the mean CIS values. For graphical clarity, SD of the mean coherence was omitted. Digits labeled as in Fig. 6.