Simple photoreceptors in some invertebrates: Physiological properties of a new photosensory modality

Abstract

Simple photoreceptors, namely photoresponsive neurons without microvilli and/or cilia have long been known in the central ganglion of crayfish, Aplysia, Onchidium and Helix. Recently, similar simple photoreceptors, ipRGCs were discovered in the mammalian retinas. A characteristic common to all of their photoreceptor potentials shows a slow kinetics and little adaptation, contrasting with the fast and adaptive photoresponses in eye photoreceptors. Furthermore, these simple photoreceptors are not only first-order photosensory cells, but also second-order interneurons. Such characteristics suggested that simple photoreceptors function as a new sensory modality, non-image-forming vision, which is different from the image-forming vision of eye photoreceptors. The Onchidium simple photoreceptors A-P-1 and Es-1 respond to light with a depolarizing receptor potential, caused by closing of light-dependent, cGMP-gated K + channels, as in vertebrate cGMP cascade mediated by Gt-type G-protein. The same simple photoreceptors Ip-2 and Ip-1 are hyperpolarized by light, owing to opening of the same K + channels. This shows the first demonstration of a new type of cGMP cascade, in which Ip-2/Ip-1 are hyperpolarized when light activates guanylate cyclase (GC) through a Go-type G-protein. The ipRGCs, as involved in non-imaging function of ipRGCs, contribute to pupillary light reflex and circadian clocks. However, their function as interneurons has not been ascertained. In Onchidium simple photoreceptors, A-P-1/Es-1 and Ip-2/Ip-1 cells the photoreceptor potentials play a role in LTP-like long-lasting potentiation (LLP) of the non-imaging functions, e.g., excitatory tactile or inhibitory pressure synaptic transmission and the subsequent behavioral responses. It was also shown that this LLP is effective, even if their photoresponse is subthreshold.