Spontaneous membrane voltage oscillations were found in 27 of 130 isolated frog saccular hair cells. Voltage oscillations had a mean peak-to-peak amplitude of 23 mV and a mean oscillatory frequency of 4.6 Hz. When compared with non-oscillatory cells, oscillatory cells had significantly greater hyperpolarization-activated and lower depolarization-activated current densities. Two components, the hyperpolarization-activated cation current, I_h, and the K⁺-selective inward-rectifier current, I_K1, contributed to the hyperpolarization-activated current, as assessed by the use of the I_k1-selective inhibitor Ba²⁺ and the I_h-selective inhibitor ZD-7288. Five depolarization-activated currents were present in these cells (transient I_BK, sustained I_BK, I_DRK, I_A, and I_Ca), and all were found to have significantly lower densities in oscillatory cells than in non-oscillatory cells (revealed by using TEA to block I_BK, 4-AP to block I_DRK, and prepulses at different voltages to isolate I_A). Bath application of either Ba²⁺ or ZD-7288 suppressed spontaneous voltage oscillations, indicating that I_h and I_K1 are required for generating this activity. On the contrary, TEA or Cd²⁺ did not inhibit this activity, suggesting that I_BK and I_Ca do not contribute. A mathematical model has been developed to test the interpretation derived from the pharmacological and biophysical data. This model indicates that spontaneous voltage oscillations can be generated when the electrophysiological features of oscillatory cells are used. The oscillatory behaviour is principally driven by the activity of I_K1 and I_h, with I_A playing a modulatory role. In addition, the model indicates that the high densities of depolarization-activated currents expressed by non-oscillatory cells help to stabilize the resting membrane potential, thus preventing the spontaneous oscillations.