Striatal cholinergic interneurons pause their ongoing firing in response to sensory stimuli that have acquired meaning as a signal for learned behavior. In slices, these cells exhibit both spontaneous activity patterns and spontaneous pauses very similar to those seen in vivo. The mechanisms responsible for ongoing firing and spontaneous pauses were studied in striatal slices using perforated patch recordings. All hyperpolarizations, whether spontaneous or generated by current injection, were amplified and shaped by two hyperpolarization-activated currents. Hyperpolarization onsets were regeneratively amplified by a potassium current (KIR) whose activation promoted further hyperpolarization. The termination of hyperpolarizations was controlled by a time-dependent nonspecific cation current (HCN). The duration and even the sizes of spontaneous and driven hyperpolarizations and pauses in spontaneous activity in cholinergic interneurons are largely autonomous properties of the neuron, rather than reflections of characteristics of the input eliciting the response.