Brain, Behavior and Evolution

Horne C.a· Helvik J.V.a· Fleming M.S.a· Fjelldal P.G.b· Eilertsen M.a

Author affiliations

aDepartment of Biological Sciences, University of Bergen, Bergen, Norway
bInstitute of Marine Research, Matre Research Station, Matredal, Norway

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Article / Publication Details

First-Page Preview

Received: May 25, 2021
Accepted: July 18, 2022
Published online: August 03, 2022

Number of Print Pages: 12
Number of Figures: 4
Number of Tables: 1

ISSN: 0006-8977 (Print)
eISSN: 1421-9743 (Online)

For additional information: https://www.karger.com/BBE

Abstract

In Atlantic salmon (Salmo salar), seasonal photoperiod is shown to regulate the onset of sexual maturation, yet which brain region(s) is involved, and how light information impacts the neuroendocrine system are still not fully understood in teleosts. Detailed knowledge about the photoperiodic regulation of maturation in fish is still missing. In birds, it is shown that gonadotropin-releasing hormone (Gnrh) is located in the same neurons as vertebrate ancient (VA) opsin, suggesting a direct photoreceptive regulation for the onset of sexual maturity. This study presents a comprehensive topographic mapping of gnrh2, gnrh3, kisspeptin 2 (kiss2), gonadotropin-inhibiting hormone (gnih), and VA opsin using in situ hybridization on mature Atlantic salmon brains. Neurons positive for gnrh3 are expressed in the olfactory bulb and ventral telencephalon, while gnrh2-positive neurons are located dorsally in the midbrain tegmentum. Gonadotropin-inhibiting hormone (Gnih)-expressing cell bodies are present in the ventral thalamus and extend caudally to the hypothalamus with kiss2-expressing cells appearing in a lateral position. VA opsin-positive cells are present in the telencephalon, the rostro-dorsal ring of the left habenula, the ventral thalamus, and the midbrain tegmentum. The results show no similar co-location as found in birds, hypothesizing that the photoreceptive modulation of Gnrh in salmon may interact through neuronal networks. The topography analyses of the essential neuroendocrine cells related to sexual maturation in the Atlantic salmon brain show that diencephalic (thalamus, hypothalamus) and midbrain (tegmentum) regions seem central for controlling sexual maturation.

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References Abbott M, Volkoff H. Thyrotropin releasing hormone (TRH) in goldfish (Carassius auratus): role in the regulation of feeding and locomotor behaviors and interactions with the orexin system and cocaine- and amphetamine regulated transcript (CART). Horm Behav. 2011;59(2):236–45. Abraham E, Palevitch O, Gothilf Y, Zohar Y. Targeted gonadotropin-releasing hormone-3 neuron ablation in zebrafish: effects on neurogenesis, neuronal migration, and reproduction. Endocrinology. 2010;151(1):332–40. Ackerman P, Morgan JD, Iwama G. Anesthetics. Guidelines on the care and use of fish in research, teaching and testing; 2005. Amano M, Moriyama S, Iigo M, Kitamura S, Amiya N, Yamamori K, et al. Novel fish hypothalamic neuropeptides stimulate the release of gonadotrophins and growth hormone from the pituitary of sockeye salmon. J Endocrinol. 2006;188(3):417–23. Amano M, Oka Y, Aida K, Okumoto N, Kawashima S, Hasegawa Y. Immunocytochemical demonstration of salmon GnRH and chicken GnRH-II in the brain of masu salmon, Oncorhynchus masou. J Comp Neurol. 1991;314(3):587–97. Anglade I, Zandbergen T, Kah O. Origin of the pituitary innervation in the goldfish. Cell Tissue Res. 1993;273(2):345–55. Bailhache T, Arazam A, Klungland H, Aleström P, Breton B, Jego P. Localization of salmon gonadotropin-releasing hormone mRNA and peptide in the brain of Atlantic salmon and rainbow trout. J Comp Neurol. 1994;347(3):444–54. Beaudry FEG, Iwanicki TW, Mariluz BRZ, Darnet S, Brinkmann H, Schneider P, et al. The non-visual opsins: eighteen in the ancestor of vertebrates, astonishing increase in ray-finned fish, and loss in amniotes. J Exp Zool B Mol Dev Evol. 2017;328(7):685–96. Biran J, Golan M, Mizrahi N, Ogawa S, Parhar IS, Levavi-Sivan B. LPXRFa, the piscine ortholog of GnIH, and LPXRF receptor positively regulate gonadotropin secretion in Tilapia (Oreochromis niloticus). Endocrinology. 2014;155(11):4391–401. Chatterjee A, Hsieh YL, Yu JYL. Molecular cloning of cDNA encoding thyroid stimulating hormone β subunit of bighead carp aristichthys nobilis and regulation of its gene expression. Mol Cell Endocrinol. 2001;174(1–2):1–9. Chi L, Li X, Liu Q, Liu Y. Photoperiod regulate gonad development via kisspeptin/kissr in hypothalamus and saccus vasculosus of Atlantic salmon (Salmo salar). PLoS One. 2017;12(2):e0169569. Choi JY, Choi CY. Effects of recombinant vertebrate ancient long opsin on reproduction in goldfish, Carassius auratus: profiling green-wavelength light. Fish Physiol Biochem. 2018;44(4):1027–36. Dann SG, Allison WT, Levin DB, Taylor JS, Hawryshyn CW. Salmonid opsin sequences undergo positive selection and indicate an alternate evolutionary relationship in Oncorhynchus. J Mol Evol. 2004;58(4):400–12. Dardente H, Wood S, Ebling F, Sáenz de Miera C. An integrative view of mammalian seasonal neuroendocrinology. J Neuroendocrinol. 2019;31(5):e12729. Davies WL, Hankins MW, Foster RG. Vertebrate ancient opsin and melanopsin: divergent irradiance detectors. Photochem Photobiol Sci. 2010;9(11):1444–57. de Roux N, Genin E, Carel JC, Matsuda F, Chaussain JL, Milgrom E. Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc Natl Acad Sci U S A. 2003;100(19):10972–6. Di Yorio MP, Munoz-Cueto JA, Paullada-Salmeron JA, Somoza GM, Tsutsui K, Vissio PG. The gonadotropin-inhibitory hormone: what we know and what we still have to learn from fish. Front Endocrinol. 2019;10:78. Ekström P, Meissl H. The pineal organ of teleost fishes. Rev Fish Biol Fisher. 1997;7(2):199–284. Falcón J, Guerlotté JF, Voisin P, Collin JP. Rhythmic melatonin biosynthesis in a photoreceptive pineal organ: a study in the pike. Neuroendocrinology. 1987;45(6):479–86. Fernandes AM, Fero K, Driever W, Burgess HA. Enlightening the brain: linking deep brain photoreception with behavior and physiology. Bioessays. 2013;35(9):775–9. Fjelldal PG, Hansen TJ, Wargelius A, Ayllon F, Glover KA, Schulz RW, et al. Development of supermale and all-male Atlantic salmon to research the vgll3 allele: puberty link. BMC Genet. 2020;21(1):123. Galas L, Raoult E, Tonon MC, Okada R, Jenks BG, Castaño JP, et al. TRH acts as a multifunctional hypophysiotropic factor in vertebrates. Gen Comp Endocrinol. 2009;164(1):40–50. García-Fernández JM, Cernuda-Cernuda R, Davies WIL, Rodgers J, Turton M, Peirson SN, et al. The hypothalamic photoreceptors regulating seasonal reproduction in birds: a prime role for VA opsin. Front Neuroendocrinol. 2015;37:13–28. Hang CY, Kitahashi T, Parhar IS. Localization and characterization of val-opsin isoform-expressing cells in the brain of adult zebrafish. J Comp Neurol. 2014;522(17):3847–60. Hang CY, Kitahashi T, Parhar IS. Brain area-specific diurnal and photic regulation of val-opsinA and val-opsinB genes in the zebrafish. J Neurochem. 2015;133(4):501–10. Hanon EA, Lincoln GA, Fustin JM, Dardente H, Masson-Pévet M, Morgan PJ, et al. Ancestral TSH mechanism signals summer in a photoperiodic mammal. Curr Biol. 2008;18(15):1147–52. Hattar S, Liao HW, Takao M, Berson DM, Yau KW. Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science. 2002;295(5557):1065–70. Hazlerigg D, Loudon A. New insights into ancient seasonal life timers. Curr Biol. 2008;18(17):R795–804. Irachi S, Hall DJ, Fleming MS, Maugars G, Björnsson BT, Dufour S, et al. Photoperiodic regulation of pituitary thyroid-stimulating hormone and brain deiodinase in Atlantic salmon. Mol Cell Endocrinol. 2021;519:111056. Kah O, Breton B, Dulka JG, Nunez-Rodriguez J, Peter RE, Corrigan A, et al. A reinvestigation of the Gn-RH (gonadotrophin-releasing hormone) systems in the goldfish brain using antibodies to salmon Gn-RH. Cell Tissue Res. 1986;244(2):327–37. Kah O, Lethimonier C, Somoza G, Guilgur LG, Vaillant C, Lareyre JJ. GnRH and GnRH receptors in metazoa: a historical, comparative, and evolutive perspective. Gen Comp Endocrinol. 2007;153(1–3):346–64. Kitahashi T, Ogawa S, Parhar IS. Cloning and expression of kiss2 in the zebrafish and Medaka. Endocrinology. 2009;150(2):821–31. Klosen P, Sébert ME, Rasri K, Laran-Chich MP, Simonneaux V. TSH restores a summer phenotype in photoinhibited mammals via the RF-amides RFRP3 and kisspeptin. FASEB J. 2013;27(7):2677–86. Kojima D, Mano H, Fukada Y. Vertebrate ancient-long opsin: a green-sensitive photoreceptive molecule present in zebrafish deep brain and retinal horizontal cells. J Neurosci. 2000;20(8):2845–51. Kojima D, Torii M, Fukada Y, Dowling JE. Differential expression of duplicated VAL-opsin genes in the developing zebrafish. J Neurochem. 2008;104(5):1364–71. Lee JH, Miele ME, Hicks DJ, Phillips KK, Trent JM, Weissman BE, et al. KiSS-1, a novel human malignant melanoma metastasis-suppressor gene. J Natl Cancer Inst. 1996;88(23):1731–7. Lien S, Koop BF, Sandve SR, Miller JR, Kent MP, Nome T, et al. The Atlantic salmon genome provides insights into rediploidization. Nature. 2016;533(7602):200–5. Lorgen M, Casadei E, Król E, Douglas A, Birnie MJ, Ebbesson LOE, et al. Functional divergence of type 2 deiodinase paralogs in the Atlantic Salmon. Curr Biol. 2015;25(7):936–41. Migaud H, Davie A, Taylor JF. Current knowledge on the photoneuroendocrine regulation of reproduction in temperate fish species. J Fish Biol. 2010;76(1):27–68. Nakane Y, Ikegami K, Iigo M, Ono H, Takeda K, Takahashi D, et al. The saccus vasculosus of fish is a sensor of seasonal changes in day length. Nat Commun. 2013;4(1):2108. Nakane Y, Yoshimura T. Universality and diversity in the signal transduction pathway that regulates seasonal reproduction in vertebrates. Front Neurosci. 2014;8(115):115. Percie du Sert N, Hurst V, Ahluwalia A, Alam S, Avey MT, Baker M, et al. The ARRIVE guidelines 2.0: updated guidelines for reporting animal research. BMC Veter Res. 2020;16(1):242. Perez JH, Tolla E, Dunn IC, Meddle SL, Stevenson TJ. A comparative perspective on extra-retinal photoreception. Trends Endocrinol Metab. 2019;30(1):39–53. Philp AR, Garcia-Fernandez JM, Soni BG, Lucas RJ, Bellingham J, Foster RG. Vertebrate ancient (VA) opsin and extraretinal photoreception in the Atlantic salmon (Salmo salar). J Exp Biol. 2000;203(Pt 12):1925–36. Revel FG, Saboureau M, Masson-Pévet M, Pévet P, Mikkelsen JD, Simonneaux V Kisspeptin mediates the photoperiodic control of reproduction in hamsters. Curr Biol. 2006;16(17):1730–5. Sandbakken M, Ebbesson L, Stefansson S, Helvik JV. Isolation and characterization of melanopsin photoreceptors of atlantic salmon (Salmo salar). J Comp Neurol. 2012;520(16):3727–44. Sayers EW, Agarwala R, Bolton EE, Brister JR, Canese K, Clark K, et al. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 2019;47(D1):D23–8. Seminara SB, Messager S, Chatzidaki EE, Thresher RR, Acierno JS Jr, Shagoury JK, et al. The GPR54 gene as a regulator of puberty. N Engl J Med. 2003;349(17):1614–27. Shichida Y, Matsuyama T. Evolution of opsins and phototransduction. Philos Trans R Soc Lond B Biol Sci. 2009;364(1531):2881–95. Son YL, Ubuka T, Soga T, Yamamoto K, Bentley GE, Tsutsui K. Inhibitory action of gonadotropin-inhibitory hormone on the signaling pathways induced by kisspeptin and vasoactive intestinal polypeptide in GnRH neuronal cell line, GT1-7. FASEB J. 2016;30(6):2198–210. Soni BG, Foster RG. A novel and ancient vertebrate opsin. FEBS Lett. 1997;406(3):279–83. Spicer OS, Zmora N, Wong TT, Golan M, Levavi-Sivan B, Gothilf Y, et al. The gonadotropin-inhibitory hormone (Lpxrfa) system’s regulation of reproduction in the brain–pituitary axis of the zebrafish (Danio rerio). Biol Rep. 2017;96(5):1031–42. Steven C, Lehnen N, Kight K, Ijiri S, Klenke U, Harris WA, et al. Molecular characterization of the GnRH system in zebrafish (Danio rerio): cloning of chicken GnRH-II, adult brain expression patterns and pituitary content of salmon GnRH and chicken GnRH-II. Gen Comp Endocrinol. 2003;133(1):27–37. Thisse C, Thisse B. High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat Protoc. 2008;3(1):59–69. Tsutsui K. A new key neurohormone controlling reproduction, gonadotropin-inhibitory hormone (GnIH): biosynthesis, mode of action and functional significance. Prog Neurobiol. 2009;88(1):76–88. Tsutsui K, Bentley GE, Bedecarrats G, Osugi T, Ubuka T, Kriegsfeld LJ. Gonadotropin-inhibitory hormone (GnIH) and its control of central and peripheral reproductive function. Front Neuroendocrinol. 2010;31(3):284–95. Tsutsui K, Saigoh E, Ukena K, Teranishi H, Fujisawa Y, Kikuchi M, et al. A novel avian hypothalamic peptide inhibiting gonadotropin release. Biochem Biophys Res Commun. 2000;275(2):661–7. Weltzien FA, Andersson E, Andersen Ø, Shalchian-Tabrizi K, Norberg B. The brain–pituitary–gonad axis in male teleosts, with special emphasis on flatfish (Pleuronectiformes). Comp Biochem Physiol A Mol Integr Physiol. 2004;137(3):447–77. Xia W, Smith O, Zmora N, Xu S, Zohar Y. Comprehensive analysis of GnRH2 neuronal projections in zebrafish. Sci Rep. 2014;4(1):3676. Article / Publication Details

First-Page Preview

Received: May 25, 2021
Accepted: July 18, 2022
Published online: August 03, 2022

Number of Print Pages: 12
Number of Figures: 4
Number of Tables: 1

ISSN: 0006-8977 (Print)
eISSN: 1421-9743 (Online)

For additional information: https://www.karger.com/BBE

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