In this paper we describe the membrane currents of neurons in the medial nucleus of the trapezoid body (MNTB), which serves as an inverting relay in the binaural auditory pathway. In the following paper (Forsythe & Barnes-Davies (Proc. R. Soc. Lond. B 251, 151 (1993))) we describe the synaptic inputs to the MNTB and discuss the significance of these results for transmission through this nucleus, where the fidelity of information transfer will depend on the integration of synaptic responses with the intrinsic postsynaptic membrane properties. Whole-cell patch clamp recordings were made from MNTB neurons using a thin-slice preparation of the rat brain stem. Resting potentials were -70 mV with a neuronal input resistance of 250 M omega and a membrane time constant of 14 ms. Voltage-clamp studies showed that MNTB neurons possess an inward sodium current, an outward current similar to a delayed rectifier and an inward rectifier. In addition, a novel transient outward current exhibiting rapid kinetics and a sustained current are present, which are both blocked by micromolar concentrations of 4-aminopyridine (4AP). Current-clamp recording showed that MNTB neurons respond to depolarization with a single overshooting action potential (AP); 4AP blocked a fast after-hyperpolarization, increased AP duration, and converted the single AP response on depolarization to a train of action potentials.