Alpha-motoneuron EPSPs exhibit different frequency sensitivities to single Ia-afferent fiber stimulation

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Abstract
A technique for the electrical stimulation of single afferent fibers in cat dorsal roots was developed. This technique was used to study the effect of varying the frequency of Ia-fiber stimulation on the amplitude of the monosynaptic excitatory postsynaptic potential (EPSP) produced in homonymous medial gastrocnemius motoneurons. Cats whose spinal cords were transected at the T[thorax]3 level early in the day of the experiment were used because their Ia-motoneuron EPSP are enlarged. At individual connections the averages of 256 EPSP obtained with spike-triggered averaging and with single-fiber electrical stimulation at closely matched afferent discharge rates (10-60 Hz) were similar in time course. In several cases, the EPSP evoked by both methods were identical in amplitude; in most cases, the EPSP obtained with spike-triggered averaging was slightly smaller than the electrically evoked EPSP. The average of 250 EPSP obtained with electrical stimulation was used to study the effect of frequency of stimulation on EPSP amplitude. Mean amplitude declined as frequency was raised from 50 to 100 Hz at some connections, but at others it failed to decline or even increased. These changes in the mean EPSP amplitude with stimulation frequency were correlated with changes in the amount of depression/facilitation occurring during the trains. Different connections on the same motoneuron showed the same general pattern of frequency sensitivity; a single afferent showed different types of frequency sensitivity on different motoneurons. At some connections a precipitous drop in EPSP amplitude was seen at the onset of a high-frequency train (e.g., 250 Hz), followed by a more gradual decline in amplitude. At these connections, stimulation at lower frequencies (e.g., 30-200 Hz) resulted in only a gradual decline in EPSP amplitude during the stimulus trains. At other connections EPSP either changed little or sometimes even increased during the course of stimulation except at the highest frequencies, where they exhibited only a gradual decline. Maintained synaptic depolarization during the train that might cause nonlinear summation at the synaptic site was shown not to be responsible for the observed depression. Thus, decreases in EPSP amplitude seem to be attributable to changes at the synapse itself. Possible mechanisms such as decreased release from individual boutons, branch blocking and receptor desensitization are discussed. Factors such as the frequency of stimulation, the history of afferent activation and the length of the burst used to obtain the average affect the amplitude of averaged EPSP and, therefore, must be considered when comparing EPSP at different connections.