1. It is well known that the amplitude of successive monosynaptic reflexes (MSR), elicited by afferent stimuli of constant strength, fluctuate from trial to trial. Previous evidence suggests that such excitability fluctuations within the motor pool can be introduced either pre- and/or postsynaptically. Using unanesthetized decerebrate or decerebrate/spinal cats, we attempted to evaluate the relative importance of pre- and postsynaptic mechanisms to MSR variability and the potential contribution of changes in the identities of responding motoneurons to such variability. 2. Comparisons between the MSR amplitude, measured in a severed ventral root, and the probability of firing of up to three individual motoneurons in fine filaments teased from the same root, confirmed that both correlated and uncorrelated fluctuations of motoneuron excitability are involved in MSR variability. Linear regression analysis from concurrent intracellular recordings from homonymous motoneurons showed that the MSR fluctuations were correlated with the variations in membrane potential baseline, as well as with the fluctuations in the monosynaptic excitatory postsynaptic potential peak amplitude. In all 11 cases tested, the former correlation was stronger than the latter. 3. Stimulation of the caudal cutaneous sural nerve (CCS) was used to alter the postsynaptic potential background on which triceps surae (GS) MSRs were generated. The interval chosen between CCS conditioning and the GS stimulation excluded the involvement of presynaptic inhibition. When conditioned by preceding CCS stimulation, GS population MSRs generally (8/9 cases tested) increased in amplitude without much change in their overall variance. However, the individual motoneurons that contributed to the population responses did show changes in both relative excitability and in the uncorrelated component of their response variance. About half of the concurrently recorded motoneurons (6/13) showed a decrease in relative excitability after CCS conditioning, 5/13 showed an increase, and 2/13 were unchanged. Comparison of unit and population responses indicated that the identities of the motoneurons that responded at any given level of population response were quite different with and without CCS conditioning. 4. High- frequency stimulation of 1a fibers was used to alter the state of presynaptic Group 1a-afferents that produced population MSRs. Post tetanic potentiation following high-frequency stimulation did not greatly alter the variance of population MSRs or ratio of correlated and uncorrelated fluctuations in MSR responses among individual motoneurons within the responding population. However, intratetanic depression and posttetanic potentiation of population MSRs were accompanied by marked shifts in individual motoneuron excitability relative to the population response, again indicated that changes in the identities of responding motoneurons contributes to population response fluctuations. 5. These results, which were similar in decerebrate and spinal preparations, indicate that both pre- and postsynaptic mechanisms produce the fluctuations of excitability in motoneurons during the MSR, with predominance of the latter. Correlated postsynaptic input to motoneurons from common sources appears to explain a large fraction of the variability of MSRs under the conditions studied. Our observations also strongly suggest that the identity of the motoneurons that participate in population MSRs can change under different conditions, presumably because of differences in the organization of synaptic input to different species of motoneurons.
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