Jgp_201611737 455..464

In insect photoreceptors, absorption of a photon by a visual pigment molecule triggers a cascade of biochemical reactions culminating in opening of cationic channels belonging to the TRP (transient receptor potential) superfamily (Hardie, 2014). Until recently, these light-activated channels were identified and studied exclusively in the fruit fly Drosophila melanogaster. Its photoreceptors express two channels, TRP and TRPL (TRP-like), characterized by a high degree of similarity with vertebrate TRPC channels (Montell and Rubin, 1989; Hardie and Minke, 1992; Phillips et al., 1992; Niemeyer et al., 1996). Mutant analysis indicated that TRP appears to be the predominant contributor to the total light-induced current (LIC): although the trp knockout phenotype was characterized by a global deterioration of photoreceptor function, trpl knockout gave only relatively small changes (Hardie and Minke, 1992; Niemeyer et al., 1996; Leung et al., 2000). Because TRPL expression increases substantially in chronically light-deprived flies (Bähner et al., 2002), it was suggested that TRPL might specifically facilitate visual information transfer in dim light, whereas TRP would be important for vision in the well-illuminated habitats of the normally day-active fruit fly. However, testing this hypothesis requires identifying the light-activated channel molecules in species with different visual ecologies and behaviors. We recently showed that the properties of native LIC in the nocturnal cockroach Periplaneta americana closely match those in trp knockout Drosophila, including large quantum bumps, and their relatively low dependence on extracellular calcium (Immonen et al., 2014b). Subsequent retinal transcriptome analysis yielded the sequences of two putative light-activated channels highly similar to Drosophila TRP and TRPL (French et al., 2015). Knockdown of P. americana TRP and TRPL channels using RNA interference (RNAi) by injections of long double-stranded RNA (dsRNA) sequences specifically targeting these channels resulted in drastic decreases in their respective mRNA levels and strong changes in electroretinogram (ERG) amplitudes. Importantly, TRP and TRPL mRNA levels were actually increased by about half after the injection of the alternate dsRNA, suggesting the existence of compensatory Electrophysiological studies in Drosophila melanogaster and Periplaneta americana have found that the receptor current in their microvillar photoreceptors is generated by two light-activated cationic channels, TRP (transient receptor potential) and TRPL (TRP-like), each having distinct properties. However, the relative contribution of the two channel types to sensory information coding by photoreceptors remains unclear. We recently showed that, in contrast to the diurnal Drosophila in which TRP is the principal phototransduction channel, photoreceptors of the nocturnal P. americana strongly depend on TRPL. Here, we perform a functional analysis, using patchclamp and intracellular recordings, of P. americana photoreceptors after RNA interference to knock down TRP (TRPkd) and TRPL (TRPLkd). Several functional properties were changed in both knockdown phenotypes: cell membrane capacitance was reduced 1.7-fold, light sensitivity was greatly reduced, and amplitudes of sustained light-induced currents and voltage responses decreased more than twofold over the entire range of light intensities. The information rate (IR) was tested using a Gaussian white-noise modulated light stimulus and was lower in TRPkd photoreceptors (28 ± 21 bits/s) than in controls (52 ± 13 bits/s) because of high levels of bump noise. In contrast, although signal amplitudes were smaller than in controls, the mean IR of TRPLkd photoreceptors was unchanged at 54 ± 29 bits/s because of proportionally lower noise. We conclude that TRPL channels provide high-gain/high-noise transduction, suitable for vision in dim light, whereas transduction by TRP channels is relatively low-gain/low-noise and allows better information transfer in bright light. Distinct roles of light-activated channels TRP and TRPL in photoreceptors of Periplaneta americana