Cholinergic neurons in the parabigeminal nucleus of the rat midbrain were studied in an acute slice preparation. Spontaneous, regular action potentials were observed both with cell-attached patch recordings as well as with whole-cell current clamp recordings. The spontaneous activity of PBN neurons was not due to synaptic input, as it persisted in the presence of the pan-ionotropic excitatory neurotransmitter receptor blocker, kynurenic acid, and the cholinergic blockers dihydro-beta-erythroidine (DHE) and atropine. This result suggests the existence of intrinsic currents that enable spontaneous activity. In voltage clamp recordings, I_H and I_A currents were observed in most PBN neurons. I_A had voltage-dependent features that would permit it to contribute to spontaneous firing. In contrast, I_H was activated only at membrane potentials lower than the trough of the spike afterhyperpolarization, suggesting that I_H does not contribute to spontaneous firing of PBN neurons. Consistent with this interpretation, application of 25 MM ZD-7288, which blocked I_H, did not affect the rate of spontaneous firing in PBN neurons. Counterparts to I_A and I_H were observed in current clamp recordings: I_A was reflected as a slow voltage ramp was observed between action potentials and upon release from hyperpolarization, and I_H was reflected as a depolarizing sag often accompanied by rebound spikes in response to hyperpolarizing current injections. In response to depolarizing current injections, PBN neurons fired at high frequencies, with relatively little accommodation. Ultimately, the spontaneous activity in PBN neurons could be used to modulate cholinergic drive in the superior colliculus in either positive or negative directions.