Resting discharge of human muscle spindles is not modulated by increases in sympathetic drive

Abstract

There is evidence in experimental animals that, in addition to receiving fusimotor drive, muscle spindles are subject to modulation by the sympathetic nervous system. We examined the validity of this idea in human subjects by recording from muscle spindles in the relaxed ankle and toe extensor muscles during a strong and sustained physiological activation of muscle sympathetic outflow. Unitary recordings were made from 20 primary and 17 secondary muscle spindle afferents via a tungsten microelectrode inserted percutaneously into the peroneal nerve in 10 awake, healthy subjects seated with the legs supported in the extended position. ECG, blood pressure, respiration and calf circumference were also recorded. The majority of the muscle spindles were spontaneously active at rest; a background discharge was induced in four silent spindles by vibrating the tendon. A sustained increase in muscle vasoconstrictor activity, an increase in calf volume and a fall in pulse pressure were produced by subjects performing a 30-40 s maximal inspiratory breath-hold. Despite this strong increase in muscle sympathetic outflow no significant changes occurred in the discharge of either primary or secondary muscle spindle afferents, measured as a change in mean frequency and variability over sequential 5 s epochs and compared with the preceding period of rest. Strong chemoreceptor-driven sympathetic bursts during sustained expiratory breath-holds also failed to modulate the firing of 14 spindle endings. We conclude that a sustained, physiological increase in muscle sympathetic activity causes no detectable change in muscle spindle firing, lending no support to the concept that the sympathetic nervous system can influence the sensitivity of human muscle spindles directly.

Figure 2. Effects of sympathetic activation on a spindle primary ending

Recording from a spontaneously active primary muscle spindle ending in extensor digitorum longus during passive plantarflexion of the toes, which stretches the spindle (A), and a sustained maximal inspiratory breath-hold, which increases muscle sympathetic drive but does not change the spindle firing (B). Calf volume, calf circumference measured contralaterally.

Figure 1. Effects of sympathetic activation on a spindle secondary ending

Recording from a spontaneously active secondary muscle spindle ending in tibialis anterior during passive dorsiflexion of the ankle, which unloads the spindle (A), and a sustained maximal inspiratory breath-hold, which increases muscle sympathetic drive but does not change the spindle firing (B). Superimposed spikes are shown in the inset of A. The inset of B shows an expanded section and illustrates the far-field muscle sympathetic activity detected from the same microelectrode (RMS-processed nerve signal). BP, blood pressure.

Figure 3. Effects of sympathetic activation on a spindle secondary ending

Recording from a silent secondary muscle spindle ending in extensor digitorum longus. A, the ending was activated by vibrating the tendon at 20 Hz, firing with every second cycle. B, the the unit's entrainment pattern did not change during an end-expiratory apnoea. Multi-unit sympathetic activity was also recorded concurrently from the same microelectrode, illustrated in the RMS-processed nerve signal.

Figure 4. Effects of sympathetic activation on a spindle secondary ending

A, recording from a spontaneously active secondary muscle spindle ending in tibialis anterior (same unit as in Fig. 1) during one series of an end-expiratory apnoea. The box centred over a sympathetic burst illustrates the source of synchronization for the averaging. B, burst-triggered average discharge frequency of the spindle shown in A, calculated from 55 large sympathetic bursts generated during the end-expiratory apnoea.