We have performed direct electrophysiological recordings from Drosophila peptidergic synaptic boutons in situ, taking advantage of a mutation, ecdysone, which causes an increase in size of these terminals. Using patch-clamp techniques, we have analyzed voltage-dependent potassium currents at the macroscopic and single-channel level. The synaptic membrane contained at least two distinct voltage-activated potassium currents with different kinetics and voltage sensitivity: an I A -like current with fast activation and inactivation kinetics and voltage-dependent steady-state inactivation; a complex delayed current that includes a slowly inactivating component, resembling the I K described in other preparations; and a noninactivating component. The I A -like current in these peptidergic boutons is not encoded by the gene Shaker, because it is not affected by null mutations at this locus. Rather, synaptic I A has properties similar to those of the Shal-encoded I A . Singlechannel recordings revealed the presence in synaptic membranes of three different potassium channel types (A 2 , K D , K L ), with biophysical properties that could account for the macroscopic currents and resemble those of the Shal, Shab, and Shaw channels described in heterologous expression systems and Drosophila neuronal somata. A 2 channels (6 -9 pS) have brief open times, and like the macroscopic I A they exhibited voltage-dependent steady-state inactivation and a rapidly inactivating ensemble average current profile. K D channels (13-16 pS) had longer open times, activate and inactivate with much slower kinetics, and may account for the slowly inactivating component of the macroscopic current. K L (44 -54 pS) channels produced a noninactivating ensemble average and may contribute to the delayed macroscopic current observed.