The internal messengers mediating the photocurrent of the molluscan extraocular photoreceptor, A-P-1, were examined. In the dark, pressure-injection of cGMP into the A-P-1, voltage-clamped at resting levels, produced a rapid outward current, associated with an increase in conductance. However, the cGMP-induced current and increase in conductance were suppressed by subsequent photostimulation, suggesting hydrolysis of cGMP by light. The steady-state I/V relation for the cGMP-induced current was non-linear. The I/V relation for the instantaneous cGMP-induced current, measured 50 ms after the beginning of a voltage step, was linear, and reversed at the membrane potential, -67 mV, which corresponded to the K+ equilibrium potential of A-P-1 in 10 mM K+ normal saline. These findings indicate that the internal cGMP induces a voltage- and time-dependent K+ current. Since the photocurrent results from the suppression of a voltage- and time-dependent K+ current similar to above, the photocurrent is considered to be equivalent to the suppression of the cGMP-induced current. Short pressure-injection of GDP-beta-S into A-P-1 reduced the subsequent photocurrent. The photocurrent was also suppressed after an external application of Pertussis toxin. On the other hand, the photocurrent was amplified by prior pressure-injection of inositol 1,4,5-trisphosphate (IP3). However, a short pressure-injection of neomycin into A-P-1 depressed the subsequent photocurrent. These results suggested that the cGMP-induced (dark) current is mediated by cGMP, and that hydrolysis of cGMP by light leads to the photocurrent, then being modified by another messenger, IP3 to be amplified. In addition, the photocurrent seems to originate in an early enzymatic step, T-GTP in the phototransduction.