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Fish are ectotherm, which rely on the external temperature to regulate their internal body temperature, although some may perform partial endothermy. Together with photoperiod, temperature oscillations, contribute to synchronizing the daily and seasonal variations of fish metabolism, physiology and behavior. Recent studies are shedding light on the mechanisms of temperature sensing and behavioral thermoregulation in fish. In particular, the role of some members of the transient receptor potential channels (TRP) is being gradually unraveled. The present study in the migratory Atlantic salmon, Salmo salar, aims at identifying the tissue distribution and abundance in mRNA corresponding to the TRP of the vanilloid subfamilies, TRPV1 and TRPV4, and at characterizing their putative role in the control of the temperature-dependent modulation of melatonin production—the time-keeping hormone—by the pineal gland. In Salmo salar, TRPV1 and TRPV4 mRNA tissue distribution appeared ubiquitous; mRNA abundance varied as a function of the month investigated. In situ hybridization and immunohistochemistry indicated specific labeling located in the photoreceptor cells of the pineal gland and the retina. Additionally, TRPV analogs modulated the production of melatonin by isolated pineal glands in culture. The TRPV1 agonist induced an inhibitory response at high concentrations, while evoking a bell-shaped response (stimulatory at low, and inhibitory at high, concentrations) when added with an antagonist. The TRPV4 agonist was stimulatory at the highest concentration used. Altogether, the present results agree with the known widespread distribution and role of TRPV1 and TRPV4 channels, and with published data on trout (Oncorhynchus mykiss), leading to suggest these channels mediate the effects of temperature on S. salar pineal melatonin production. We discuss their involvement in controlling the timing of daily and seasonal events in this migratory species, in the context of an increasing warming of water temperatures.

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Neurosteroids are involved in the regulation of multiple behavioral and physiological processes and metabolic activities in the vertebrate brain. However, central mechanisms of how neurosteroid synthesis is regulated is far to be understood. Gonadotropin-inhibitory hormone (GNIH) is a hypothalamic neuropeptide that negatively regulates gonadotropin secretion but also inhibits sexual and aggressive behaviors in birds and mammals by modulating aromatase enzyme and neuroestrogen synthesis. In a previous study performed in male sea bass, we reported that Gnih inhibited the reproductive axis by acting at the three levels of the brain-pituitary-gonad axis. Moreover, the presence of Gnih cells and fibers in the telencephalon, mesencephalon and rhombencephalon suggests a role of Gnih in regulating other important brain functions in sea bass, including behavior. In this study, we have analyzed the effects of the intracerebroventricular (icv) injection of sbGnih-2 on the brain and pituitary expression of the main neurosteroids-synthesizing enzymes (stAR, cyp17, 3β-hsd, 17β-hsd, cyp19b, cyp7b), as well as on estrogen and androgen receptors (erα, erβ1, erβ2, ar). A combination of immunohistochemistry and in situ hybridization was also used to identify putative interaction of Gnih- and aromatase-positive cells. We also performed a mirror test study as a proxy to measure aggression levels and agonistic behavior after icv injection of sbGnih-2. Central administration of sbGnih-2 at different doses reduced the transcript levels of 3β-hsd and 17β-hsd, and increased the expression of cyp19b (brain aromatase) in the sea bass brain. Neuroanatomical results suggest that paracrine and neuroendocrine actions could mediate Gnih effects on aromatase expression. Central administration of sbGnih-2 also decreased the pituitary expression of 17β-hsd and estrogen receptors (erβ2). The mirror test analysis showed that sbGnih-2 affected the agonistic/aggressive behavior of sea bass as revealed by the decreased interaction with the mirror, lower time spent in the mirror zone, increased latency to establish contact with the mirror and higher mean distance to the mirror zone. In contrast, locomotor activity parameters measured were not affected by sbGnih-2 injection. Taken together, our results showed for the first time in fish that Gnih inhibits social-aggressive behavior and affects the gene expression of neurosteroid-synthesizing enzymes giving rise to neuroandrogens and neuroestrogens in the sea bass brain.