Previous experiments have shown that the conductances that are thought to underlie the spontaneous oscillations of the membrane potential in inferior olivary (IO) neurons of the mature rat are present at 2 days postnatal (PN). In this study intracellular recordings of transmembrane potentials were made in 209 IO neurons in brainstem slices from rats aged 4-25 days PN. Membrane potential oscillations were not found before 9 days PN but were observed in 41% of neurons examined at 10-15 days PN and in 95% of neurons after 16 days PN. These oscillations exhibited a wide range of frequencies (0.5-9.5 Hz) and amplitudes (2-23 mV). The waveforms of the oscillations in different neurons varied from having 2-3 non-harmonic frequencies of unequal amplitude to being almost sinusoidal. There was a positive relationship between the age of the animal and the frequency (P less than 0.0001) and amplitude (P less than 0.002) of the oscillations. The timecourse of development of the membrane potential oscillations is consistent with ultrastructural data which indicate that neuro-neuronal gap junctions in the rat IO nucleus mature between 10 and 15 days PN. Exposure of the neurons to pharmacological agents that induce oscillations in adult IO neurons failed to induce oscillations in neurons less than 9 days PN. Our findings support the hypothesis that oscillations of the membrane potential in IO neurons depend not only on specific membrane conductances but also on electrotonic coupling between the neurons.