Mechanical cutaneous stimulation alters Ia presynaptic inhibition in human wrist extensor muscles: a single motor unit study

Abstract

Reflex responses were evoked by radial nerve stimulation in 25 single motor units in the extensor carpi radialis muscles of seven subjects during voluntary isometric wrist extension. The responses consisted of narrow peaks in the post-stimulus time histograms with latencies compatible with monosynaptic activation. When the skin of the palm and finger tips was continuously swept using a soft rotating brush, the purely monosynaptic components of the motor unit responses, as assessed from the contents of the first two 0.25 ms bins of the peak, were found to increase. This increase did not affect the motoneurone net excitatory drive, as assessed by measuring the mean duration of the inter-spike intervals. The cutaneous inputs activated by the brush may have reduced the tonic presynaptic inhibition exerted on the Ia afferents homonymous to the extensor motor units tested. To further investigate whether Ia presynaptic inhibition was involved, the responses of the extensor motor units were conditioned by stimulating the median nerve 20 ms earlier, using a protocol which is known to induce Ia extensor presynaptic inhibition originating from flexor Ia afferents. The median nerve stimulation did not affect the motoneurone excitatory drive, but led to a decrease in the responses of the extensor motor units to the radial nerve stimulation, especially in the purely monosynaptic components. This decrease was consistent with the Ia presynaptic inhibition known to occur under these stimulation conditions. The cutaneous inputs activated by the brush were found to reduce the Ia presynaptic inhibition generated by the median nerve stimulation, without affecting the distribution of the Ia presynaptic inhibition among the various types of motor units tested. The present data suggest that cutaneous inputs from the palm and finger tips may relieve the Ia presynaptic inhibition exerted on the wrist extensor motor nuclei, and thus enhance the proprioceptive assistance to fit the specific requirements of the ongoing motor task.

Figure 2. Typical motor unit response

The subjects were asked to performed wrist extension, keeping their fingers relaxed (A). In order to activate the cutaneous mechanoreceptors, the skin of the palm and fingertips was continuously lightly swept using a soft rotating brush (F). The similarity of the macro-potentials (B and G) and of the twitches (C and H) obtained in both cases confirms that the same motor unit was tested during wrist extension both with and without cutaneous stimulation. In both the recordings in which the radial nerve was being stimulated alone (D) and associated with median nerve stimulation (E,) the response probability of the motor unit was smaller than that measured during wrist extension associated with cutaneous stimulation (I and J).

Figure 1. Motoneurone excitatory drive

A, no consistent differences in the mean integrated EMG activity associated with each motor unit tested with and without median nerve stimulation were observed between the recordings with or without cutaneous stimulation. B, likewise, no consistent differences in the mean duration of the inter-spike intervals observed with each motor unit tested were detected during the various stimulations.

Figure 3. The effects of cutaneous inputs on the Ia presynaptic inhibition induced by median nerve stimulation

The higher the motor unit response probability measured while the radial nerve was being stimulated alone, the stronger its response probability assessed from the whole peak (A) or from the first 0.5 ms (B) was found to be depressed while applying stimulation to the median nerve, both during wrist extension without (▪, dotted line) and with (▵, continuous line) cutaneous stimulation. The higher Y-intercept suggests that the presynaptic inhibition presumed to be evoked by the median nerve stimulation may be relieved by the tonic cutaneous inputs. C and D, mean changes in the response probability in trials during which the median nerve was stimulated and cutaneous stimulation was applied () or not (□). Applying cutaneous stimulation was found to reduce the presumed presynaptic inhibition estimated both from the whole peak (C) and from the monosynaptic components (D).

Figure 4. Ia presynaptic inhibition depended on the functional parameters of the motor units

The strength of the Ia presynaptic inhibition, as assessed from the changes in the purely monosynaptic components of each motor unit response, was significantly correlated with the functional parameters of the unit. The Ia presynaptic inhibition decreased when the recruitment threshold (A) and the macro-potential area (B) increased, and when the twitch contraction time (C) decreased. The similarity of the variances and the slopes suggests that the cutaneous stimulation may not have affected the distribution of Ia presynaptic inhibition among the various types of motor units tested. Note the marked differences between the Y-intercepts of the regression lines computed with and without cutaneous stimulation. ▪, wrist extension; ▵, wrist extension with cutaneous stimulation.

Figure 5. The size of the unconditioned response with cutaneous stimulation did not alter the strength of the Ia presynaptic inhibition

The response probability of a low threshold motor unit tested without cutaneous stimulation was 0.58 impulses per trigger when the radial nerve stimulation was being applied alone (test stimulation 1 at 1.1 MT) and the median nerve stimulation induced a decrease of its response probability of 58 %. The response probability of the same motor unit tested with cutaneous stimulation was 0.75 impulses per trigger when the radial nerve stimulation was being applied alone (A, test stimulation 1). Applying median nerve stimulation decreased its response probability by 41.3 % (B). When the radial nerve stimulation intensity was set at 0.9 MT (test stimulation 2, C), applying median nerve stimulation decreased its response probability by 38.9 % (D). These observations suggest that the cutaneous inputs may relieve the presynaptic inhibition induced by the median nerve stimulation, whatever the intensity of the radial nerve stimulation, i.e. the size of the unconditioned motor unit response.