Color opponency with a single kind of bistable opsin in the zebrafish pineal organ

Lower vertebrate pineal organs discriminate UV and visible light. Such color discrimination is typically considered to arise from antagonism between two or more spectrally distinct opsins, as, e.g., human cone-based color vision relies on antagonistic relationships between signals produced by red-, green-, and blue-cone opsins. Photosensitive pineal organs contain a bistable opsin (parapinopsin) that forms a signaling-active photoproduct upon UV exposure that may itself be returned to the signaling-inactive “dark” state by longer-wavelength light. Here we show the spectrally distinct parapinopsin states (with antagonistic impacts on signaling) allow this opsin alone to provide the color sensitivity of this organ. By using calcium imaging, we show that single zebrafish pineal photoreceptors held under a background light show responses of opposite signs to UV and visible light. Both such responses are deficient in zebrafish lacking parapinopsin. Expressing a UV-sensitive cone opsin in place of parapinopsin recovers UV responses but not color opponency. Changes in the spectral composition of white light toward enhanced UV or visible wavelengths respectively increased vs. decreased calcium signal in parapinopsin-sufficient but not parapinopsin-deficient photoreceptors. These data reveal color opponency from a single kind of bistable opsin establishing an equilibrium-like mixture of the two states with different signaling abilities whose fractional concentrations are defined by the spectral composition of incident light. As vertebrate visual color opsins evolved from a bistable opsin, these findings suggest that color opponency involving a single kind of bistable opsin might have been a prototype of vertebrate color opponency.

Deep-brain photoreception links luminance detection to motor output in Xenopus frog tadpoles

Nonvisual photoreceptors are widely distributed in the retina and brain, but their roles in animal behavior remain poorly understood. Here we document a previously unidentified form of deep-brain photoreception in Xenopus laevis frog tadpoles. The isolated nervous system retains sensitivity to light even when devoid of input from classical eye and pineal photoreceptors. These preparations produce regular bouts of rhythmic swimming activity in ambient light but fall silent in the dark. This sensitivity is tuned to short-wavelength UV light; illumination at 400 nm initiates motor activity over a broad range of intensities, whereas longer wavelengths do not cause a response. The photosensitive tissue is located in a small region of caudal diencephalon—this region is necessary to retain responses to illumination, whereas its focal illumination is sufficient to drive them. We present evidence for photoreception via the light-sensitive proteins opsin (OPN)5 and/or cryptochrome 1, because populations of OPN5-positive and cryptochrome-positive cells reside within the caudal diencephalon. This discovery represents a hitherto undescribed vertebrate pathway that links luminance detection to motor output. The pathway provides a simple mechanism for light avoidance and/or may reinforce classical circadian systems.

Evolution of photosensory pineal organs in new light: the fate of neuroendocrine photoreceptors

Pineal evolution is envisaged as a gradual transformation of pinealocytes (a gradual regression of pinealocyte sensory capacity within a particular cell line), the so-called sensory cell line of the pineal organ. In most non-mammals the pineal organ is a directly photosensory organ, while the pineal organ of mammals (epiphysis cerebri) is a non-sensory neuroendocrine organ under photoperiod control. The phylogenetic transformation of the pineal organ is reflected in the morphology and physiology of the main parenchymal cell type, the pinealocyte. In anamniotes, pinealocytes with retinal cone photoreceptor-like characteristics predominate, whereas in sauropsids so-called rudimentary photoreceptors predominate. These have well-developed secretory characteristics, and have been interpreted as intermediaries between the anamniote pineal photoreceptors and the mammalian non-sensory pinealocytes. We have re-examined the original studies on which the gradual transformation hypothesis of pineal evolution is based, and found that the evidence for this model of pineal evolution is ambiguous. In the light of recent advances in the understanding of neural development mechanisms, we propose a new hypothesis of pineal evolution, in which the old notion ‘gradual regression within the sensory cell line’ should be replaced with ‘changes in fate restriction within the neural lineage of the pineal field’.

Expression of pineal ultraviolet- and green-like opsins in the pineal organ and retina of teleosts

SUMMARYIn teleostean bony fishes, studies on the adults of various species have shown that pineal photoreceptors are maximally sensitive to short- and middle-wavelength light, possibly utilising both rod-like and pineal-specific opsins. Until recently, however, very little was known about the pineal opsins present in embryonic and larval teleosts and their relationships to opsins expressed by retinal photoreceptors. Our immunocytochemical studies have revealed that, in Atlantic halibut, herring and cod, pineal photoreceptors express principal phototransduction molecules during embryonic life before they appear in retinal photoreceptors. In cDNA from embryonic and adult halibut, we identified two partial opsin gene sequences, HPO1 and HPO4, with highest homology to teleost green and ultraviolet cone opsins (72–83% and 71–83% amino acid identity, respectively). In halibut, these opsins are expressed in the pineal organ of embryos and appear in the retina of larvae. Our recent in situ hybridisation studies with RNA probes for HPO1 and HPO4 demonstrate the presence of green-like opsin mRNAs in the pineal organ and the retina of herring, cod, turbot, haddock, Atlantic salmon, zebrafish and three species of cichlid, and of ultraviolet opsins in the retinas of zebrafish, Atlantic salmon, turbot and the three cichlid species. We conclude that the halibut pineal organ appears to have the potential for both ultraviolet and green photosensitivity from the embryonic stage and that the retina may acquire the same potential during the larval stages. In the other teleosts studied, although both pineal and retinal photoreceptors seem to utilise a green-like opsin from the larval stage, ultraviolet photoreception appears to be restricted to the retina.