1. The dorsal longitudinal flight muscles of Drosophila melanogaster contain three voltage-activated ion currents, two distinct potassium currents and a calcium current. The currents can be isolated from each other by exploiting the developmental properties of the system and genetic tools, as well as conventional pharmacology.2. The fast transient potassium current (I(A)) is the first channel to appear in the developing muscle membrane. It can be studied in isolation between 60 and 70 hr of pupal development. The channels can be observed to carry both outward and inward currents depending on the external potassium concentration. I(A) is blocked by both tetraethylammonium ion (TEA) and 3- or 4-aminopyridine. The inactivation and recovery properties of I(A) are responsible for a facilitating effect on membrane excitability.3. The delayed outward current (I(K)) develops after maturation of the I(A) system. I(K) can be isolated from I(A) by use of a mutation that removes I(A) from the membrane current response and can be studied before the development of Ca(2+) channels. I(K) shows no inactivation. The channels are more sensitive to blockage by TEA than I(A) channels, but are not substantially blocked by 3- or 4-aminopyridine.4. The calcium current (I(Ca)) is the last of the major currents to develop and must be isolated pharmacologically with potassium-blocking agents. I(Ca) shows inactivation when Ca(2+) is present but not when Ba(2+) is the sole current carrier. When Ca(2+) is the current carrier, the addition of Na(+) or Li(+) retards the inactivation of the net inward current. When the membrane voltage is not clamped, Ba(2+) alone, or Ca(2+) with Na(+) (or Li(+)), produces a plateau response of extended duration.5. The synaptic current (I(J)) evoked by motoneurone stimulation is the fastest and largest of the current systems. It has a reversal potential of approximately -5 mV, indicating roughly equal permeabilities of Na(+) and K(+). During a nerve-driven muscle spike, I(J) is the major inward current, causing a very rapid depolarization away from resting potential. An exceptionally large synaptic current is necessary to rapidly discharge the high membrane capacitance (0.03 muF/cell) in these large (0.05 x 0.1 x 0.8 mm) isopotential cells.