1. The activation of current-clamped neurons in the chick nucleus magnocellularis (nMAG) by eighth nerve stimulation has been studied in a brain slice preparation using patch electrodes. Single presynaptic stimuli produced rapidly rising, suprathreshold, excitatory postsynaptic potentials (EPSPs) with a synaptic delay of approximately 0.4 ms. Spontaneous, miniature EPSPs (mEPSPs) were evident in control extracellular solution and in the presence of tetrodotoxin (TTX). 2. The EPSP was composed of a large, brief component that was sensitive to antagonists of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors, and a smaller, slowly decaying component that was sensitive to both N-methyl-D-aspartate (NMDA) and AMPA receptor antagonists. 3. Injection of depolarizing current steps revealed a strong outward rectification of the membrane conductance at potentials close to the resting potential. Consequently, neurons could fire only a single, TTX-sensitive action potential during a current step. The conductance responsible for this rectification was sensitive to 1 mM 4-aminopyridine but not to 1 mM tetraethylammonium. 4. Following the termination of depolarizing current pulses, membrane potential decayed with a half-time (t1/2) that decreased as the depolarizing current increased, reaching approximately 0.25 ms for a depolarization from rest of 20 mV. The t1/2 for the decay of EPSPs matched the membrane t1/2, indicating that the underlying synaptic conductance decays more quickly than the membrane t1/2. 5. The slow phase of the EPSP was always longer than the membrane t1/2 and increased in size with hyperpolarization. This result is consistent with the contribution of AMPA receptors to the slow, as well as fast, EPSP. 6. The safety factor for transmission with low-frequency stimuli was large, as indicated by the rise time of the EPSP, the extent to which the EPSP shunted the action potential, and the size of EPSPs after prolongation of the synaptic conductance by cyclothiazide. 7. During repetitive synaptic stimulation, the slow EPSPs summated to produce a plateau depolarization of 10–20 mV. The plateau potential was only partially blocked by NMDA receptor antagonists. 8. During trains of stimuli, the faster EPSPs rode atop the plateau potential and could drive action potentials at rates up to 500 Hz for short periods. Synaptic depression was evident during trains, such that EPSPs often fell below threshold after 5–10 stimuli at rates above 200 Hz. EPSPs could remain suprathreshold for several seconds at 50 Hz.(ABSTRACT TRUNCATED AT 400 WORDS)