Preferential distribution of nociceptive input to motoneurons with muscle units in the cranial portion of the upper trapezius muscle

Abstract

Pain is associated with changes in the neural drive to muscles. For the upper trapezius muscle, surface electromyography (EMG) recordings have indicated that acute noxious stimulation in either the cranial or the caudal region of the muscle leads to a relative decrease in muscle activity in the cranial region. It is, however, not known if this adaption reflects different recruitment thresholds of the upper trapezius motor units in the cranial and caudal region or a nonuniform nociceptive input to the motor units of both regions. This study investigated these potential mechanisms by direct motor unit identification. Motor unit activity was investigated with high-density surface EMG signals recorded from the upper trapezius muscle of 12 healthy volunteers during baseline, control (intramuscular injection of isotonic saline), and painful (hypertonic saline) conditions. The EMG was decomposed into individual motor unit spike trains. Motor unit discharge rates decreased significantly from control to pain conditions by 4.0 ± 3.6 pulses/s (pps) in the cranial region but not in the caudal region (1.4 ± 2.8 pps; not significant). These changes were compatible with variations in the synaptic input to the motoneurons of the two regions. These adjustments were observed, irrespective of the location of noxious stimulation. These results strongly indicate that the nociceptive synaptic input is distributed in a nonuniform way across regions of the upper trapezius muscle.

Keywords: coherence; experimental pain; high-density EMG; motor units; upper trapezius.

Copyright © 2016 the American Physiological Society.

Figures

Fig. 1.

Schematic representation of the electrode grid positioned over the right upper trapezius with the indication of the location of the injections of isotonic/hypertonic saline into the cranial and caudal regions of the upper trapezius. The rectangle on the right illustrates the spatial distribution of the innervation zone across the electrode grid for all subjects (black: high probability; white: low probability). Here, the white, dashed line represents the most common location for all subjects.

Fig. 2.

Trains of motor unit (MU) action potentials for 2 representative subjects in the control condition (A) and with hypertonic saline (B). Based on the shape and the spatial distribution, the action potential from motor unit #1 (bold, black lines in A and B) and from #4 (bold, gray lines in A and B) was identified as coming from the same motor units across the 2 conditions. The shape and spatial distribution of the action potential of motor unit #1 are shown in C (control condition) and D (pain condition). Similarly, the action potential for motor unit #4 is shown in E (control condition) and F (pain condition). Motor units #2 and #3 were not the same across the 2 conditions. Each line in C–F represents the estimated shape of the action potential from each bipolar recording in intervals of 40 ms (±20 ms with respect to identified discharge time). The correlation coefficient for the action potentials across the 2 conditions was 0.95 for MU #1 and 0.96 for MU #4. The injections were performed on the right (lateral) side at the second row of electrodes (cranial) and at the ninth row of electrodes (caudal).

Fig. 3.

Mean (±SE) pain intensity scores following the injection of isotonic saline and hypertonic saline into the cranial and caudal region of the upper trapezius muscle. No differences in peak pain intensity were observed for the injection of hypertonic saline in the 2 locations.

Fig. 4.

Discharge rate characteristics for motor units identified in all 3 conditions. A and B: average discharge rate for the first 15 s across the 3 conditions (control: white bars; isotonic: gray bars; hypertonic: black bars) for motor units located in the cranial and caudal regions, respectively. *P < 0.05; statistically significant difference across conditions. C: motor unit discharge rates during the first 15 s following the injection of hypertonic saline for motor units located in the cranial and caudal regions, depending on injection location (solid bars: caudal; striped bars: cranial). Each bar includes 10, 11, 11, and 15 motor units (from left to right). For motor units of each region, there was no statistically significant difference between injection location (cranial: P = 0.65; caudal: P = 0.45).

Fig. 5.

Common input to the motoneurons innervating cranial motor units and motoneurons innervating caudal motor units with and without pain (A). The boxplots represent 0.25, 0.5, and 0.75 quartiles (whiskers indicate full range) of the peak coherence in the delta (0–5 Hz), alpha (5–15 Hz), and beta (15–35 Hz). The dashed line indicates the level for significant coherence. B: pain-evoked changes in peak coherence across the delta, alpha, and beta bands for CSTs consisting of spike trains from cranial motor units (dark gray) or from caudal motor units (light gray). n = number of trials included (significant coherence peaks).