Although potassium channels play a variety of roles in shaping the electrical properties of neurons, little is known about how these channels are constituted in neurons. To examine the assembly and physiological function of A-type K+ channels in mature differentiated neurons, we have developed a highly efficient gene transfer method for Aplysia neurons that has allowed us to express about 10(7) copies of the cloned Aplysia Shaker (Sh) K+ channel (AK01a) in single identified cells. We find that expression of AK01a phenocopies one of the native transient K+ currents (IAdepol), suggesting that the native channel carrying IAdepol is assembled as a homooligomer of AK01a. Overexpression of AK01a has substantial effect on the action potential, shortening its duration, enhancing its hyperpolarizing afterpotential, and depressing by more than half the amount of transmitter release by the action potential from the terminals. Thus, the AK01a channel not only contributes to the firing properties within a given neuron but also can regulate the signaling between interconnected cells.