Spontaneous activation of light-sensitive channels in Drosophila photoreceptors

In Drosophila photoreceptors light induces phosphoinositide hydrolysis and activation of Ca²⁺-permeable plasma membrane channels, one class of which is believed to be encoded by the trp gene. We have investigated the properties of the light-sensitive channels under conditions where they are activated independently of the transduction cascade. Whole-cell voltage clamp recordings were made from photoreceptors in a preparation of dissociated Drosophila ommatidia. Within a few minutes of establishing the whole-cell configuration, there is a massive spontaneous activation of cation-permeable channels. When clamped near resting potential, this 'rundown current' (RDC) accelerates over several seconds, peaks, and then relaxes to a steady-state which lasts indefinitely (many minutes). The RDC is invariably associated with a reduction in sensitivity to light by at least 100-fold. The RDC has a similar absolute magnitude, reversal potential, and voltage dependence to the light-induced current, suggesting that it is mediated by the same channels. The RDC is almost completely (≥98%) blocked by La³⁺ (10-20 μM) and is absent, or reduced and altered in the trp mutant (which lacks a La³⁺- sensitive light-dependent Ca²⁺ channel), suggesting that it is largely mediated by the trp-dependent channels. Power spectra of the steady-state noise in the RDC can be fitted by simple Lorentzian functions consistent with random channel openings. The variance/mean ratio of the RDC noise suggests the underlying events (channels) have conductances of ~1.5-4.5 pS in wild- type (WT), but 12-30 pS in trp photoreceptors. Nevertheless, the power spectra of RDC noise in WT and trp are indistinguishable, in both cases being fitted by the sum of two Lorentzians with a major time constant (effective 'mean channel open time') of 1-2 ms and a minor component at higher frequencies (~0.2 ms). This implies that the noise in the WT RDC may actually be dominated by non-trp-dependent channels and that the trp- dependent channels may be of even lower unit conductance.