The effects of experimental muscle and skin pain on the static stretch sensitivity of human muscle spindles in relaxed leg muscles

Abstract

Animal studies have shown that noxious inputs onto gamma-motoneurons can cause an increase in the activity of muscle spindles, and it has been proposed that this causes a fusimotor-driven increase in muscle stiffness that is believed to underlie many chronic pain syndromes. To test whether experimental pain also acts on the fusimotor system in humans, unitary recordings were made from 19 spindle afferents (12 Ia, 7 II) located in the ankle and toe extensors or peronei muscles of awake human subjects. Muscle pain was induced by bolus intramuscular injection of 0.5 ml 5% hypertonic saline into tibialis anterior (TA); skin pain was induced by 0.2 ml injection into the overlying skin. Changes in fusimotor drive to the muscle spindles were inferred from changes in the mean discharge frequency and discharge variability of spindle endings in relaxed muscle. During muscle pain no afferents increased their discharge activity: seven afferents (5 Ia, 2 II) showed a decrease and six (4 Ia, 2 II) afferents were not affected. During skin pain of 13 afferents discharge rate increased in one (Ia) and decreased in two (1 Ia, 1 II). On average, the overall discharge rate decreased during muscle pain by 6.1% (P < 0.05; Wilcoxon), but remained essentially the same during skin pain. There was no detectable correlation between subjective pain level and the small change in discharge rate of muscle spindles. Irrespective of the type of pain, discharge variability parameters were not influenced (P > 0.05; Wilcoxon). We conclude that, contrary to the 'vicious cycle' hypothesis, acute activation of muscle or skin nociceptors does not cause a reflex increase in fusimotor drive in humans. Rather, our results are more aligned with the pain adaptation model, based on clinical studies predicting pain-induced reductions of agonist muscle activity.

Figure 1. Example of muscle spindle afferent activity recorded from a relaxed leg muscle before, during and after experimentally induced muscle pain

This sensory unit was classified as Ia muscle spindle afferent innervating a peroneus muscle. Regardless of strong pain (rated 6 on a scale 0–10) instantaneous discharge rate was not affected by nociceptive stimulation; however, during a period when pain fully subsided the discharge rate slightly decelerated (3.6%) and the irregularity index increased (22%). For clarity, the figure shows 10 s intervals from respective periods. Note the absence of surface EMG activity. Blood pressure (BP) was monitored throughout the experiment.

Figure 2. Effect of deep muscle pain on muscle spindle afferent discharge rate and variability

A, comparison between discharge rate and irregularity index during control period and during painful stimulation. B, changes in the irregularity index as a function of changes in discharge rate. Control and pain periods indicated by open and filled symbols, respectively. Circles represent primary (Ia) muscle spindle afferents and squares represent secondary (II) muscle spindle afferents. Three muscle spindles recorded from subjects who did not feel any pain from hypertonic saline injection are shaded grey instead of black and encircled by the dashed line in A.

Figure 3. Changes in discharge rate during separate phases of pain

A, deep muscle pain. B, superficial skin pain. Changes in discharge rate relative to control period are shown for peak pain period (‘Peak’), phase of pain recession (‘End’) and phase after pain completely subsided (‘After’). Single afferents are connected by lines. The circles and continuous lines represent primary (Ia) muscle spindle afferents, while squares and dashed lines represent secondary (II) muscle spindle afferents. Only those afferents which were recorded until pain fully subsided are included in the analyses.

Figure 4. Effect of superficial skin pain on muscle spindle afferent discharge rate and variability

A, comparison between discharge rate and irregularity index during control period and during painful stimulation. B, changes in irregularity index as the function of changes in discharge rate. Control and pain periods indicated by open and filled symbols, respectively. Circles represent primary (Ia) muscle spindle afferents and squares represent secondary (II) muscle spindle afferents.