1. Parallel fibers of the guinea pig dorsal cochlear nucleus (DCN) were electrically stimulated at the pial surface of the nucleus in a brain-slice preparation. Extracellular field potentials produced by the parallel fibers and postsynaptic cells, and the response of single units were identified and characterized. Responses were compared with those reported for stimulation of parallel fibers in the cerebellum and to those seen with electrical stimulation of the auditory nerve. 2. Stimulation of the DCN parallel fibers generates a consistent set of extracellular field potentials. In layer 1 of the DCN, a short-latency triphasic wave (P1(1)-N1(1)-P2(1)) is followed by a slower negative wave (N2(1)). The onset phase of the N2(1) often exhibits a small positive notch (P2a1). In layer 2, an initial triphasic wave (P1(2)-N1(2)-P2(2)) is followed by a short-latency negative wave (N2(2)) and a slower positive wave (P3(2)). The N1(2) is approximately coincident with the N1(1), whereas the P3(2) is coincident with N2(1). The falling phase of the P3(2) is sometimes interrupted by a brief negative deflection (N3(2)). These field potentials are similar, but not identical to those reported for parallel fiber stimulation in the cerebellum in vivo (15). These responses differ substantially from those produced in the DCN by electrical stimulation of the auditory nerve (50). 3. Low-calcium solutions and pharmacologic manipulations were used to separate pre- and postsynaptic response components in the field potential records. When the slice is bathed in a low-calcium solution the P2a1, N2(1), N2(2), P3(2), and the brief late deflections are abolished. However, the P1(1)-N1(1)-P2(1) and P1(2)-N1(2)-P2(2) remain unaffected. A similar separation of pre- and postsynaptic components can be achieved with 100 microM adenosine or 0.5 mM kynurenic acid. It is concluded that the P1(1)-M1(1)-P2(1) wave is the compound action potential of the unmyelinated parallel fibers, whereas the longer-latency field potential components are generated postsynaptically. 4. The conduction velocity of the parallel fiber volley was measured to be 0.30 m/s at the pial surface, in a line approximately parallel to the strial axis of the nucleus. Mapping experiments reveal that the spread of the P1(1)-N1(1)-P2(1) is greatest along the strial axis, and more limited in the orthogonal direction. 5. Single units were recorded in layer 2. At a distance of 500-700 microns from the stimulating electrode, the latencies of single-unit discharges fall between 2.5 and 4 ms, at the time of the N2(2).(ABSTRACT TRUNCATED AT 400 WORDS)