Color opponency generated with photoreception by two states of a bistable opsin in the zebrafish pineal organ.

Abstract

In human retina, three kinds of cone opsins, which are sensitive to red, green, and blue, respectively, are expressed in separate cone cells. The difference of their spectral sensitivities generates color opponency in retinal ganglion cells and enables us to percept colors. Similar to retina, the ganglion cells in pineal-related organs from cyclostomes to reptiles are also known to exhibit color opponency, the neural firing inhibition and promotion by UV and visible light irradiation, respectively. We have found parapinopsin, a UV-sensitive pineal opsin, is a common molecule responsible for UV-sensitivity in pineal color opponency. Parapinopsin has bistability, the property of photo-interconvertibility between the UV-sensitive dark state and visible light sensitive photoproduct. This property is never seen in visual opsins, such as cone opsins. To understand a physiological significance of the bistable nature of parapinopsin, we addressed two-photon imaging using transgenic and parapinopsin-deficient zebrafish and found the bistable nature contributes to generating color opponency in the single photoreceptor cell. We further found the photoreceptor cell exhibits color opponency under white light, whose spectral distribution is similar to natural sunlight. These findings provide the new concept that color opponency can be generated with a single kind of bistable opsin without the calculation of outputs from multiple opsins.