Electrical activity in the gamma frequency range is instrumental for temporal encoding on the millisecond scale in attentive vertebrate brains. Surprisingly, also circadian pacemaker neurons in the cockroach Rhyparobia maderae (Leucophaea maderae) employ fast spontaneous rhythmic activity in the gamma band frequency range (20–70 Hz) together with slow rhythmic activity. The ionic conductances controlling this fast spontaneous activity are still unknown. Here, Ca2+ imaging combined with pharmacology was employed to analyse ion channels underlying spontaneous activity in dispersed circadian pacemakers of the adult accessory medulla, which controls circadian locomotor activity rhythms. Fast spontaneous Ca2+ transients in circadian pacemakers accompany tetrodotoxin (TTX)-blockable spontaneous action potentials. In contrast to vertebrate pacemakers, the spontaneous depolarisations from rest appear to be rarely initiated via TTX-sensitive sustained Na+ channels. Instead, they are predominantly driven by mibefradil-sensitive, low-voltage-activated Ca2+ channels and DK-AH269-sensitive hyperpolarisation-activated, cyclic nucleotide-gated cation channels. Rhythmic depolarisations activate voltage-gated Na+ channels and nifedipine-sensitive high-voltage-activated Ca2+ channels. Together with Ca2+ rises, the depolarisations open repolarising small-conductance but not large-conductance Ca2+-dependent K+ channels. In contrast, we hypothesise that P/Q-type Ca2+ channels coupled to large-conductance Ca2+-dependent K+ channels are involved in input-dependent activity.