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Androgen-Dependent Stimulation of Brain Dopaminergic Systems in the Female European Eel (Anguilla anguilla)

Unité Scientifique de Muséum 0401, Unité Mixte de Recherche 5178, Centre National de la Recherche Scientifique/MNHN/UPMC Biologie des Organismes Marins et Ecosystèmes, Département des Milieux et Peuplements Aquatiques, Muséum National d’Histoire Naturelle (F.-A.W., M.-E.S., B.V., N.L.B., S.D.), 75231 Paris, France; Développement, Evolution et Plasticité du Système Nerveux, Unité Propre de Recherche Centre National de la Recherche Scientifique 2197, Institut de Neurobiologie Alfred Fessard, Centre National de la Recherche Scientifique (F.-A.W., C.P., M.-E.S., P.V.), 91198 Gif-sur-Yvette, France; and Endocrinologie Moléculaire de la Reproduction, Unité Mixte de Recherche, Centre National de la Recherche Scientifique 6026, Université de Rennes 1 (O.K.), 35042 Rennes, France

Address all correspondence and requests for reprints to: Dr. Finn-Arne Weltzien, Department of Molecular Biosciences, University of Oslo, PB 1041 Blindern, NO-0316 Oslo, Norway. E-mail: f.a.weltzien{at}imbv.uio.no.

Dopamine (DA), a neurotransmitter present in all vertebrates, is involved in processes such as motor function, learning and behavior, sensory activities, and neuroendocrine control of pituitary hormone release. In the female eel, we analyzed how gonadal steroids regulate brain expression of tyrosine hydroxylase (TH), the rate-limiting enzyme in the biosynthesis of DA. TH mRNA levels were assayed by quantitative real-time RT-PCR. TH-positive nuclei were also localized by in situ hybridization (ISH) and immunohistochemistry, and the location of TH nuclei that project to the pituitary was determined using 1,1'-dioctadecyl-3,3,3',3'-tetramethylindicarbocyanine perchlorate retrograde tracing. Chronic in vivo treatment with testosterone increased TH mRNA specifically in the periglomerular area of the olfactory bulbs and in the nucleus preopticus anteroventralis (NPOav). NPOav was labeled with 1,1'-dioctadecyl-3,3,3',3'-tetramethylindicarbocyanine perchlorate, showing that this nucleus is hypophysiotropic in the eel. The nonaromatizable 5-dihydrotestosterone gave identical results in both areas, whereas 17ß-estradiol had no stimulatory effect, showing that the observed stimulatory effects of testosterone were androgen dependent. In teleosts, DA neurons originating from the NPOav directly inhibit gonadotropic function, and our results indicate an androgen-dependent, positive feedback on this neuroendocrine control in the eel. In mammals, DA interneurons in the olfactory bulbs are involved in the enhancement of olfactory sensitivity and discrimination. Our results in the European eel suggest an androgen-dependent stimulation of olfactory processing, a sensory function believed to be important in eel navigation during its reproductive migration toward the oceanic spawning grounds. To our knowledge, this is the first evidence from any vertebrate of an androgen-dependent effect on DAergic activity in the olfactory bulbs, providing a new basis for understanding the regulation by gonadal steroids of central DAergic systems in vertebrates.

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