Kinetic properties of single-ion channels activated by light in Limulus ventral nerve photoreceptors

Previous results on Limulus ventral photoreceptors have suggested that besides inositol trisphosphate, another unknown transmitter may also work in the transduction cascade. This assumption has been supported by the finding of two light-activated channel types. The present report furnishes further evidence of the dual transmitter mechanism in phototransduction by analyzing the kinetic properties and voltage dependency of these cation channels with conductances of 12 pS and 30 pS. Single-channel currents were recorded in Limulus ventral nerve photoreceptors in cell-attached configuration at 14°C. At V_m + 80 mV the open-time histograms of both channels were fit best by the sum of two exponentials; time constants (and weights) were: 0.81 ms (0.62) and 6.20 ms (0.38) for the 12 pS channels and 2.38 ms (0.43) and 19.4 ms (0.57) for the 30 pS channels. At this potential the mean open times were 2.7 ms for the 12 pS and 13.3 ms for the 30 pS channels, about two-times larger than at hyperpolarizing potentials. The deactivation kinetics were also different for the two channels. The time constants of the decay of the channel activity, after switching off the light, were 2.5 s for the 12 pS and 12.9 s for the 30 pS channels. The 12 pS channel exhibits bursting and subconductance states at positive potentials. The subconductances are about 20%, 46% and 72% of the fully open state. Results show that the two types of light-activated channels have different kinetic parameters, voltage dependence and gating mechanisms. The two channels are suggested to be gated by different transmitters or processes. It is proposed that for the 30 pS channel the transmitter could be calcium ion or a calcium-dependent transmitter.