Highlights : with classical non-photosensitive projection neurons (PN). Functionally, however, whereas classical, opn4xa-negative PNs display an achromatic LIGHT OFF response, the novel cell type we describe exhibit a LIGHT ON character that is elicited by green and blue light. Taken together, our data suggest a previously unanticipated heterogeneity in the projection neuron population in the zebrafish pineal organ raising the question of the importance of these differences in pineal function.
The zebrafish pineal organ is a photoreceptive structure containing two main neuronal populations (photoreceptors and projections neurons). Here we describe a new pineal cell type that harbors both characteristics of projection neurons and photoreceptors. Indeed, a subpopulation of projection neurons expresses the melanopsin gene opn4xa suggesting photoreceptive properties. This population of hybrid cell fates, share a similar behaviour regarding dependency for BMP and Notch signalling pathways with classical non-photosensitive projection neurons (PNs) suggesting they are closer to the PN population. We describe two distinct types of activity within PNs: an achromatic LIGHT OFF activity in opn4xa -PNs and a LIGHT ON activity elicited by green and blue light in opn4xa+ PNs. Altogether the discovery and characterization of opn4xa+ PNs suggest a previously unanticipated heterogeneity in the projection neuron population.
The eye is instrumental for controlling circadian rhythms in nocturnal mammals. Here, we address the conservation of this function in the zebrafish, a diurnal vertebrate. Using lakritz (lak) mutant larvae, which lack retinal ganglion cells (RGCs), we show that while a functional eye is required for a phenomenon known as masking, it is largely dispensable for the establishment of circadian rhythms of locomotor activity. Furthermore, the eye is dispensable for the induction of a phase delay following a pulse of white light at CT 16 but contributes to the induction of a phase advance upon a pulse of white light at CT21. Melanopsin photopigments are important mediators of photoentrainment in nocturnal mammals. One of the zebrafish melanopsin genes, opn4xa, is expressed in RGCs but also in photosensitive projection neurons in the pineal gland. To address the role of this photopigment, we generated an opn4xa mutant. Abrogating opn4xa has no effect on masking and circadian rhythms of locomotor activity, or for the induction of phase shifts, but is required for period length control when larvae are subjected to constant light. Finally, analysis of opn4xa;lak double mutant larvae did not reveal redundancy between the function of the eye and Opn4xa in the pineal for photoentrainment or phase shifts after light pulses. Our results challenge the dogma that the eye as the sole mediator of light influences on circadian rhythms and highlight profound differences in the circadian system and photoentrainment between different animal models.Significance statementThe eye in general and melanopsin expressing cells in particular are crucial for circadian rhythms in nocturnal mammals, most notably during photoentrainment, by which circadian rhythms adapt to a changing light environment. In marked contrast to this, we show that in the diurnal zebrafish the eye and photosensitivity dependent on the melanopsin gene opn4xa, which expressed in both the eye and the pineal gland, are largely dispensable for correct circadian rhythms. These results provide the first insight that the light sensors orchestrating circadian rhythms are different between animal models raising the intriguing possibility that vertebrates might employ different molecular/cellular circuits for photoentrainment depending on their phylogeny and/or temporal niche.
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