Abstract
BackgroundPineal-related organs in cyclostomes, teleosts, amphibians, and reptiles exhibit color opponency, generating antagonistic neural responses to different wavelengths of light and thereby sensory information about its “color”. Our previous studies suggested that in zebrafish and iguana pineal-related organs, a single photoreceptor cell expressing both UV-sensitive parapinopsin and green-sensitive parietopsin generates color opponency in a “one-cell system.” However, it remains unknown to what degree these opsins and the single cell-based mechanism in the pineal color opponency are conserved throughout non-mammalian vertebrates.ResultsWe found that in the lamprey pineal organ, the two opsins are conserved but that, in contrast to the situation in other vertebrate pineal-related organs, they are expressed in separate photoreceptor cells. Intracellular electrophysiological recordings demonstrated that the parietopsin-expressing photoreceptor cells with Go-type G protein evoke a depolarizing response to visible light. Additionally, spectroscopic analyses revealed that parietopsin with 11-cis 3-dehydroretinal has an absorption maximum at ~570 nm, which is in approximate agreement with the wavelength (~560 nm) that produces the maximum rate of neural firing in pineal ganglion cells exposed to visible light. The vesicular glutamate transporter is localized at both the parietopsin- and parapinopsin-expressing photoreceptor terminals, suggesting that both types of photoreceptor cells use glutamate as a transmitter. Retrograde tracing of the pineal ganglion cells revealed that the terminal of the parietopsin-expressing cells is located close enough to form a neural connection with the ganglion cells, which is similar to our previous observation for the parapinopsin-expressing photoreceptor cells and the ganglion cells. In sum, our observations point to a “two-cell system” in which parietopsin and parapinopsin, expressed separately in two different types of photoreceptor cells, contribute to the generation of color opponency in the pineal ganglion cells. ConclusionOur results indicate that the jawless vertebrate, lamprey, employs a system for color opponency that differes from that described previously in jawed vertebrates. From a physiological viewpoint, we propose an evolutionary insight, the emergence of pineal “one-cell system” from the ancestral “multiple (two)-cell system,” showing the opposite evolutionary direction to that of the ocular color opponency.
Highlights
Pineal-related organs in cyclostomes, teleosts, amphibians, and reptiles exhibit color opponency, generating antagonistic neural responses to different wavelengths of light and thereby sensory information about its “color”
Identification of an opsin underlying visible light sensitivity in pineal color opponency First, we investigated whether the river lamprey possesses a parietopsin gene
In the case of the evolution in the pineal color opponency from the ancestral to present-day vertebrates, such an evolutionary direction, from the one-cell to the two-cell system, would be unlikely because it leads the system to decrease the signalto-noise ratio in generating color opponency in the ganglion cells, with high cost to separate the distribution of functional molecules involved in the system. From these points of view, we propose a more plausible scenario as follows (Fig. 4): (i) In the common ancestor of vertebrates, the two-cell system involving photoreceptor cells expressing parapinopsin-like UV-sensitive bistable opsin and those expressing parietopsin-like green-sensitive bleaching opsin cooperatively generated color opponency in the pineal organ. (ii) The two-cell system was maintained in the agnathostome lineage as found in the present-day lamprey. (iii) After the gnathostomeagnathostome split, the one-cell system emerged from the two-cell system by integrating two opsins and two G proteins into a single kind of photoreceptor cell in the gnathostome lineage
Summary
Pineal-related organs in cyclostomes, teleosts, amphibians, and reptiles exhibit color opponency, generating antagonistic neural responses to different wavelengths of light and thereby sensory information about its “color”. Our previous studies suggested that in zebrafish and iguana pineal-related organs, a single photoreceptor cell expressing both UV-sensitive parapinopsin and green-sensitive parietopsin generates color opponency in a “one-cell system.”. In the zebrafish pineal organ, parapinopsin contributes to generating color opponency in the photoreceptor cells by serving as both UV and visible light sensors in a single photoreceptor cell because of its bistable nature, i.e., an interconvertibility between the UV-sensitive dark state and visible light-sensitive photoproduct by UV and visible light absorption, respectively [12]. The generation of color opponency with parapinopsin alone in a single photoreceptor cell requires high-intensity light (i.e., daytime) to form the photoequilibrium-like state between two states of parapinopsin
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