1. Membrane currents of luminosity horizontal cells (L-HCs) and chromatic horizontal cells (C-HCs) isolated from the Xenopus retina were characterized using the whole-cell patch-clamp technique. 2. The current-voltage curve for the L-HC had a characteristic negative slope conductance in the voltage range of -30 to -10 mV that was not evident in the C-HC. 3. A transient outward 4-aminopyridine-sensitive potassium current (A-current) was the most prominent current in C-HCs but was also present in L-HCs. A-current characteristics in the two horizontal cell (HC) classes were closely similar. Its threshold of activation was above -45 mV. The half-voltage of inactivation was close to -70 mV. The decay of the A-current was fit by a single exponential with time constants of 30 and 40 ms at depolarizing voltage steps to -10 and +30 mV, respectively. 4. The voltage for 50% A-current inactivation shifted toward negative potentials shortly after we established the whole-cell configuration. This shift was changed to more positive potentials by internal application of guanosine 5'-triphosphate, resulting in a significant overlap of A-current activation and inactivation functions near -40 mV, which is well within the normal operating range of the HC. 5. Internal application of the G-protein activator GTP gamma S shifted the voltage-dependent inactivation of the A-current toward positive potentials by +15 mV. In contrast, GDP beta S shifted the inactivation curve by about -10 mV, similar to what was observed in untreated cells. 6. GTP and GTP gamma S increased the rate of recovery from inactivation and slowed down the rate of inactivation of the A-current enabled by a depolarizing prepulse. 7. Glutamate superfused in the bath solution significantly accelerated the rate of inactivation of A-current induced by depolarizing prepulses. The rate of A-current recovery from inactivation, however, was not affected by glutamate. 8. Removal of calcium from the bath solution reversibly decreased the amplitude of the A-current without a significant shift in its threshold of activation.