The voltage-gated currents in the fly lobula plate tangential cells were examined using the switched electrode voltage clamp technique. In CH cells, two currents were identified (Figs. 1, 2): a slow calcium inward current and a delayed rectifying, noninactivating potassium outward current. HS and VS cells appear to possess similar currents to CH cells, but in addition, exhibit a fast-activating sodium inward current and a sodium-activated potassium outward current (Figs. 3, 4). While the delayed rectifying potassium current in all three cell classes is responsible for the observed outward rectification described previously (Borst and Haag, 1996), the sodium inward current produced the fast and irregular spikelike depolarizations found in HS and VS cells but not in CH cells: When the sodium current is blocked by either. TTX or intracellular QX314, no more action potentials can be elicited in HS cells under current-clamp conditions (Fig. 5). As is demonstrated in HS cells, space clamp conditions are sufficient to suppress synaptically induced action potentials (Fig. 6). The currents described above were incorporated with the appropriate characteristics into compartmental models of the cells (Fig. 7, 8). The anatomical and electrically passive membrane parameters of these cells were determined in a preceding paper (Borst and Haag, 1996). After fitting the current parameters to the voltage-clamp data (Fig. 9), the model cells qualitatively mimicked the fly tangential cells under current clamp conditions in response to current injection (Fig. 10). The simulations demonstrated that the electrical compactness seen in the HS and VS cells, either in passive models or in active models during continuous hyperpolarization, decreased significantly in the active models during continuous depolarization (Fig. 11). Active HS models reproduce the frequency-dependent amplification of current injected into their axon (Fig. 12).