Facilitation and depression in the responses of spinal Renshaw cells to random stimulation of motor axons.

1. We investigated the responses of cat lumbosacral Renshaw cells to pseudo-Poison stimulus sequences (of three different mean rates) delivered to motor axons in ventral roots or various muscle nerves. The Renshaw cell responses were evaluated by computation of peristimulus time histograms (PSTHs). 2. PSTHs computed with respect to all the stimuli showed, before the reference time, near-constant bin contents corresponding to the mean firing probability (rate), and an initial excitatory component (increase in discharge probability) after the reference time, followed by a small but longer-lasting reduction of firing rate. These two response components were strongly correlated linearly. It is suggested that the postexcitatory rate reduction is predominantly due to afterhyperpolarization. 3. In general, Renshaw cell responses to any stimulus in a stimulus train depended upon the stimulation history. In the averaged record, the response to the second of a pair of stimuli was affected by the first stimulus independently of intervening (random) stimuli. Very often, the second response showed a long-lasting depression (from 25 to greater than 250 ms). In a number of cases a briefer facilitating effect preceded the depression. 4. These conditioning effects were largely homosynaptic, i.e., confined to the particular input channel that was stimulated. This was shown by stimulating two different nerves (or nerve branches) with independent random patterns of similar mean rates and determining the cross-conditioning exerted by one input channel on the excitatory effects of the other. At small intervals between conditioning and test stimuli of some tens of milliseconds, a facilitatory effect could often be seen, which almost certainly reflected spatial summation. However, the subsequent depressant effect was largely accounted for by the postexcitatory rate reduction consequent to the conditioning stimulus in the parallel channel. Autoconditioning was still present. 5. The amount of facilitation and depression as well as their balance depended on the average Renshaw cell response. This in turn depended, at each mean stimulus rate, on the strength of synaptic coupling between an input channel and the cell, and on the mean stimulus rate, declining with an increase in mean rate. That is, the facilitation increased and the depression decreased with decreasing synaptic coupling and increasing mean stimulus rate. 6. Several factors may contribute to facilitation and depression; these are discussed with respect to their relative quantitative significance.(ABSTRACT TRUNCATED AT 400 WORDS)

Time constants of facilitation and depression in Renshaw cell responses to random stimulation of motor axons.

In 9 adult anaesthetized cats, 22 lumbosacral Renshaw cells recorded with NaCl-filled micropipettes were activated by random stimulation of ventral roots or peripheral nerves. The stimulus patterns had mean rates of 9.5-13 or 20-23 or 45 pulses per second and were pseudo-Poisson; short intervals below ca. 5 ms (except in two cases) were excluded. The Renshaw cell responses were evaluated by two kinds of peristimulus-time histograms (PSTHs). "Conventional" PSTHs were calculated by averaging the Renshaw cell discharge with respect to all the stimuli in a train. These PSTHs showed an early excitatory response which was often followed by a longer-lasting slight reduction of the discharge probability. These two response components were positively correlated. "Conditional" PSTHs were determined by averaging the Renshaw cell discharge with respect to the second ("test") stimulus in pairs of stimuli which were separated by varied intervals, delta. The direct effect of the first "conditional" response was subtracted from the excitation following the second ("test") stimulus so as to isolate the effect caused by the second stimulus per se. After such a correction, the effect of the first "conditioning" stimulus showed pure depression, pure facilitation or mixed facilitation/depression. Analysis of such conditioning curves yielded two time constants of facilitation (ranges: ca. 4-35 ms and 93-102 ms) and two of depression (ranges: ca. 7-25 ms and 50-161 ms). It is concluded that these time constants are compatible with processes of short-term synaptic plasticity known from other synapses. Other processes such as afterhyperpolarization and mutual inhibition probably are of less importance.

Frequency response of spinal Renshaw cells activated by stochastic motor axon stimulation.

In anaesthetized or decerebrate cats, motor axons in lumbosacral ventral roots or hindlimb muscle nerves were stimulated with random trains of brief electrical pulses, and Renshaw cell spike sequences were recorded. Spectral analysis was used to determine the range of linear operation of Renshaw cells, via coherence computations, and to calculate their frequency-dependent gains and phases. The analysis showed that the dynamic behaviour of Renshaw cells was different for different strengths of their synaptic input from motor axons and for different mean stimulus rates. In general, the changes in dynamics associated with variation of these two input parameters followed a common trend. This can be related to the average response of Renshaw cells per stimulus, as assessed by peri-stimulus time histograms. For axons having a strong excitatory effect on a Renshaw cell (as judged from the size of early peri-stimulus time histogram peaks), and for low mean stimulus rates (10-23 pulses per second), the linear range of signal transmission (assessed by coherence computation) was usually very broad (from zero sometimes up to over 100 Hz, but mostly up to 50-100 Hz). Following an initial elevation in the range 2-15 Hz, the gain showed first a rapid decrease with frequency, down to a value which at 30-50 Hz could be a tenth of the gain at lower frequencies (2-15 Hz); it then continued to decline slowly. Otherwise the linear range was narrower and/or the coherence was generally lower; the gain was lower and showed little decline with frequency. The phase curves of Renshaw cells generally showed a low-frequency phase lead (up to roughly 10 Hz) and an increasing phase lag thereabove that was generated in part by the conduction delay. The results show that Renshaw cells can follow, particularly sensitively, inputs in a frequency range encompassing the steady firing rates of many alpha-motoneurons. This range of high gain also covers that of a component of physiological tremor (ca. 6-12 Hz), a basic mechanism of which is probably related to unfused contractions of newly recruited motor units firing in this range. It can therefore be expected that recurrent inhibition via Renshaw cells is especially powerful in this physiologically important range of alpha-motoneuron firing.

After-effects of stochastic synaptic Renshaw cell excitation on their discharge probability.

We have studied Renshaw cell (RC) responses to pseudo-Poisson stimulus sequences (small intervals below 5 ms excluded; mean rates between 10 and 45 pulses/s) delivered to motor axons in ventral roots or muscle nerves. Average RC responses to stimuli in a single stimulus channel depended upon the preceding stimulation history. The responses to pairs of stimuli separated by variable intervals (irrespective of intervening stimuli) generally showed a long depressant effect (from 25 to more than 250 ms) of the first ('conditioning') stimulus; in a number of cases a briefer facilitating effect preceded the depressant action. Several possible causes of these conditioning effects are discussed.