Distribution of presynaptic inhibition on type-identified motoneurones in the extensor carpi radialis pool in man

Abstract

The question was addressed as to whether the magnitude of Ia presynaptic inhibition might depend on the type of motor unit activated during voluntary contraction in the wrist extensor muscles. For this purpose, we investigated the effects of applying electrical stimulation to the median nerve on the responses of 25 identified motor units to radial nerve stimulation delivered 20 ms after a conditioning stimulation. The reflex responses of the motor units yielded peaks in the post-stimulus time histograms with latencies compatible with monosynaptic activation. Although median nerve stimulation did not affect the motoneurone net excitatory drive assessed from the mean duration of the inter-spike interval, it led to a decrease in the contents of the first two 0.25 ms bins of the peak. This decrease may be consistent with the Ia presynaptic inhibition known to occur under these stimulation conditions. In the trials in which the median nerve was being stimulated, the finding that the response probability of the motor units, even in their monosynaptic components, tended to increase as their force threshold and their macro-potential area increased and as their twitch contraction time decreased suggests that the median nerve stimulation may have altered the efficiency with which the Ia inputs recruited the motoneurones in the pool. These effects were consistently observed in seven pairs of motor units each consisting of one slow and one fast contracting motor unit which were simultaneously tested, which suggests that the magnitude of the Ia presynaptic inhibition may depend on the type of motor unit tested rather than on the motoneurone pool excitatory drive. The present data suggest for the first time that in humans, the Ia presynaptic inhibition may show an upward gradient working from fast to slow contracting motor units which is able to compensate for the downward gradient in monosynaptic reflex excitation from 'slow' to 'fast' motor units. From a functional point of view, a weaker Ia presynaptic inhibition acting on the fast contracting motor units may contribute to improving the proprioceptive assistance to the wrist myotatic unit when the contraction force has to be increased.

Figure 1. Analysis of the motor unit reflex peak using the cumulative sum procedure

The reflex response of a motor unit to the radial nerve stimulation yielded a narrow peak in the post-stimulus time histograms. The characteristics of the peak were automatically determined using the cumulative sum procedure (cusum; Ellaway, 1978). The sharp rising phase in the cusum and its confidence limit were used to determine the first bin count significantly different from the baseline mean. By positioning time limits at the onset and offset of the peak, it was possible to automatically measure the peak duration and latency and the motor unit response probability in the whole peak above the baseline mean and in its purely monosynaptic component (first 0.5 ms).

Figure 2. Paired recording of slow and fast contracting motor units

The activity of a slow contracting motor unit was recorded concurrently with that of a faster contracting motor unit. The subjects were asked to adjust their wrist muscle contraction force to the level necessary to keep the highest force threshold unit firing steadily. In the recording in which the radial nerve was being stimulated alone, the response probability of the motor unit (A, 0.53 impulses per trigger) activated at a low force threshold (0.92 N), i.e. that having a small macro-potential area (C) and a long twitch contraction time (CT; D), was greater than the response probability of the motor unit (E, 0.45 impulses per trigger) activated at a higher force threshold (4.2 N), i.e. that having a larger macro-potential area (G) and a faster twitch contraction time (H). Contrary to this, while concomitantly stimulating the median nerve, the response probability of the fast contracting motor unit (F, 0.33 impulses per trigger; −26.7 %) was greater than that of the slow contracting motor unit (B, 0.26 impulses per trigger; −50.9 %). These data suggest that the magnitude of the presumed Ia presynaptic inhibition may depend on the type of motor unit tested rather than on the motoneurone pool excitatory drive, and that the median nerve stimulation may have altered the strength with which the Ia inputs recruited the motoneurones in the pool. Twitches of the two motor units were extracted during sequences in which the subjects had to maintain each motor unit firing at low frequency discharge, one after the other. The selected inter-spike intervals chosen for the triggering impulses are noted in D and H.

Figure 3. Relationships between the reflex responses in the whole peak (actual data) and the functional parameters of the motor units

While stimulating the radial nerve alone, the response probability of the motor units tended to decrease as their force thresholds (A) and their macro-potential areas (B) increased, and as their twitch contraction times decreased (C), in keeping with the size principle. In the recordings with median nerve stimulation, the response probability of the motor units tended to increase as their force thresholds (D) and their macro-potential areas (E) increased, and as their twitch contraction times decreased (F). In the recordings with median nerve stimulation, there may therefore exist an upward gradient in the proprioceptive Ia monosynaptic assistance to the extensor motor units, working from slow to fast contracting motor units. The median nerve stimulation may have been able to compensate for the downward gradient in monosynaptic reflex excitation from ‘slow’ to ‘fast’ motor units.

Figure 4. Relationships between the changes in the purely monosynaptic components of the responses and the functional parameters of the motor units

In the recordings with median nerve stimulation, the decrease in the first 0.5 ms of the peak responses of the motor units tended to be weaker as their force thresholds (A) and their macro-potential areas (B) increased, and as their twitch contraction times (C) decreased. These data confirm that there may exist an upward gradient in the magnitude of the presynaptic inhibition, working from the fast to the slow contracting motor units.

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

While keeping the intensity of the median nerve constant at 0.8 MT, one low force threshold and one higher force threshold motor unit was tested either while using a constant radial nerve stimulation intensity (stimulation 1) or while adjusting the intensity of the radial nerve stimulation to obtain comparable size of unconditioned response (stimulation 2). In the case of the low threshold motor unit, applying median nerve stimulation decreased to a similar extent its unconditioned response while using stimulation 1 at 1.1 MT (A and B) or stimulation 2 at 0.9 MT (C and D). Likewise in the case of the high threshold motor unit, applying median nerve stimulation decreased to a similar extent its unconditioned response while using stimulation 1 (E and F) or stimulation 2 at 1.2 MT (G and H). These observations confirm that the strength of the Ia presynaptic inhibition may depend on the type of motor unit tested rather than on the size of the unconditioned responses of the motor units.