Spontaneous miniature hyperpolarizations were observed in cultured bullfrog neurons. Depolarization increased the frequency and amplitude of the events. Under voltage-clamp, these events were manifested as spontaneous miniature outward currents of SMOCs which were usually less than 2 nA, had a rapid rising phase and a slower voltage-dependent exponential decay. Analysis of inter-event intervals suggested that SMOCs occurred randomly, while analysis of their amplitudes yielded exponential amplitude distributions. Mean SMOC amplitudes and SMOC frequency increased with depolarization, even with 100 microM CdCl2 present. Time constants of SMOC decay resembled time constants obtained from voltage-jump experiments on Ca2+-loaded cells, and together with the sensitivity of SMOCs to tetraethyl ammonium (TEA), suggested that SMOCs are due to activation of fast Ca2+-gated potassium channels. We propose that a SMOC occurs when 10-5000 of these channels are activated by punctate intracellular Ca2+ release.