EAG channels expressed in microvillar photoreceptors are unsuited to diurnal vision

Abstract

The principles underlying evolutionary selection of ion channels for expression in sensory neurons are unclear. Among species possessing microvillar photoreceptors the major ionic conductances have only been identified in Drosophila melanogaster. In Drosophila depolarization is provided by light-activated TRP channels with a minor contribution from TRPL channels, while repolarization is mediated by sustained voltage-gated K⁺ (Kv) channels of the Shab family. Bright light stimulates Shab channels, further restricting depolarization and improving membrane bandwidth. Here, data obtained using a combination of electrophysiological, pharmacological, and molecular knockdown techniques, strongly suggest that in photoreceptors of the nocturnal cockroach Periplaneta americana, the major excitatory channel is TRPL, while the predominant delayed rectifier is EAG, a ubiquitous but enigmatic Kv channel. In contrast to the diurnal Drosophila, bright light strongly suppresses EAG conductance in Periplaneta. This light-dependent inhibition (LDI) is caused by calcium entering the cytosol, is amplified following inhibition of calcium extrusion, and can be abolished by chelating intracellular calcium or suppressing eag gene expression by RNA interference. LDI increases membrane resistance, augments gain and reduces signalling bandwidth, impairing information transfer. LDI is also observed in the nocturnal cricket Gryllus integer, whereas in the diurnal water strider Gerris lacustris the delayed rectifier is up-regulated by light. Although LDI is not expected to reduce delayed rectifier current in the normal illumination environment of nocturnal cockroaches and crickets, it makes EAG unsuitable for light response conditioning during the day, and might have caused evolutionary replacement of EAG by other delayed rectifiers in diurnal insects.

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