Estrogen modifies an electrocommunication signal by altering the electrocyte sodium current in an electric fish, Sternopygus

Abstract

Many species of electric fish emit sexually dimorphic electrical signals that are used in gender recognition. In Sternopygus, mature females produce an electric organ discharge (EOD) that is higher in frequency and shorter in pulse duration than that of mature males. EOD pulse duration is determined by ion currents in the electrocytes, and androgens influence EOD pulse duration by altering the inactivation kinetics of the electrocyte sodium current. We examined whether estrogen modulates the female-specific EOD and, if so, whether it regulates EOD pulse duration by acting on the same androgen- sensitive ion current in the electrocytes. We implanted gonadectomized Sternopygus with either empty SILASTIC capsules (control), one capsule filled with estradiol-17β (E2; low dose), or three capsules of E2 (high dose). Twelve days after implantation, E2-treated fish had plasma E2 levels ~3.3- fold (low dose) or ~7.1-fold (high dose) higher than controls. After implantation, both E2-treated groups had higher EOD frequency and shorter EOD pulse duration than controls and their own preimplantation values. Through immunocytochemistry, we identified immunoreactive estrogen receptors in the nuclei of electrocytes, indicating that these cells are directly responsive to estrogen. In addition, voltage-clamp studies showed that E2 affected the electrocyte ion currents kinetics: the sodium inactivation time constant was significantly lower in E2-treated fish than in controls. Thus, sexual dimorphism in the electrocommunication signal results, at least in part, from estrogens and androgens acting in opposite directions on the same ion current in the electrocytes.