Abstract
Photoreceptive inputs to the teleost brain are perceived as image of the visual world and as photo-modulation of neuroendocrine and neuronal signals. The retina and pineal organ are major receptive organs with projections to various parts of the brain, but in the past decades deep brain photoreceptors have emerged as candidates for photoreceptive inputs, either independent or in combination with projections from light sensory organs. This study aimed to test the effects of narrow bandwidth light using light-emitting diodes technology on brain neural activity through putative opsin stimulation in Atlantic salmon. The expression of c-fos, a known marker of neural activity, was compared in situ between dark-adapted salmon parr and following light stimulation with different wavelengths. c-fos expression increased with duration of light stimulation and the strongest signal was obtained in fish exposed to light for 120 minutes. Distinct and specific brain regions were activated following dark to light stimulation, such as the habenula, suprachiasmatic nucleus, thalamus, and hypothalamus. The c-fos expression was overlapping with photoreceptors expressing melanopsin and/or vertebrate ancient opsin, suggesting a potential direct activation by light. Interestingly in the habenula, a distinct ring of vertebrate ancient opsin and melanopsin expressing cells is overlapping with c-fos expression after neural activation. Salmon exposed to different spectra had neural activation in similar brain regions. The most apparent difference was melanopsin expression in the lateral cells of the lateral tuberal nuclus in the hypothalamus, which appeared to be specifically activated by red light. Light-stimulated neuronal activity in the deep brain was limited to subpopulations of neurons, mainly in regions with neuronal modulation activity, retinal and pineal innervations and known presence of nonvisual photoreceptors. The overlapping expression patterns of c-fos and nonvisual opsins support direct light stimulation of deep brain photoreceptors and the importance of these systems in light induced brain activity.
Highlights
Light relays important cues for regulating biological processes and rhythms in animals
In the present study we showed robust c-fos expression in distinct cells of the Atlantic salmon brain after light stimulation that were not seen in fish kept in darkness
The cells are located in brain regions with known photoreceptive capacity that have innervations from the retina and pineal, indicating that the neural activation can be a result of direct photoreception by deep brain cells or a combination with the retina and pineal
Summary
Light relays important cues for regulating biological processes and rhythms in animals. Zebrafish (Danio rerio) larvae lacking eyes and pineal were shown to display light seeking behavior following exposure to darkness regulated by melanopsin-expressing cells in the preoptic area [8]. Our previous studies have shown that a transient cluster of dual photoreceptors, expressing vertebrate ancient opsin (VA opsin) and melanopsin, in the hindbrain are permissive to the life history transition of hatching in Atlantic halibut (Hippoglossus hippoglossus) embryo with neuroblastic retina [13]. Zebrafish was shown to have a strong response to changing photic conditions, as light-dark transition, and a 30-minute light pulse at night induced c-fos expression in brain regions co-localised with deep brain photoreceptors. Our studies in Atlantic halibut showed c-fos activation in the dual photoreceptive hindbrain cluster and hatching glands after light induced hatching. The hindbrain cluster was shown to be imbedded in a neuronal network projecting to the narrow belt of hatching glands in the yolk sac, indicating a direct light control of hatching by neuronal activation [13]
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