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-17␤ (E 2 ; low dose), or three capsules of E 2 (high dose). Twelve days after implantation, E 2 -treated fish had plasma E 2 levels ϳ3.3-fold (low dose) or ϳ7.1-fold (high dose) higher than controls. After implantation, both E 2 -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 E 2 affected the electrocyte ion currents kinetics: the sodium inactivation time constant was significantly lower in E 2 -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. Key words: estrogen; sodium current; electric fish; estrogen receptor; electric organ; SternopygusIn most vertebrates, steroids have potent influences on the expression of sexually dimorphic reproductive behaviors such as courtship and mating (Kelley, 1988). Many studies have shown that regions of the nervous system and the effector organs that control reproductive behaviors have specific receptors for sex steroids, and more recently researchers have found that steroids can induce changes in the overall extracellular electrical activity in brain nuclei (Becker et al., 1992). Our understanding, however, of how steroids alter the electrical properties in specific, behaviorally relevant cells is still limited.Recent studies on the sexually dimorphic electrocommunication signal of a weakly electric fish, Sternopygus, have demonstrated that androgens alter specific ionic conductances in excitable cells involved in reproductive behavior (Ferrari and Zakon, 1993;Zakon, 1993;Ferrari et al., 1995). This has been possible because the neural circuits and effector cells underlying this behavior are relatively simple and discrete (Bullock and Heiligenberg, 1986), and some cells, the electrocytes of the electric organ, are large and accessible for recording changes in membrane properties by voltage clamp (Ferrari and Zakon, 1993;Ferrari et al., 1995;McAnelly and Zakon, 1996).In ...

Electrocyte physiology: 50 years later

“…Exogenous androgens increase EOD duration by slowing the kinetics of the electrocyte's voltage-gated Na + current (Ferrari et al, 1995) and estrogen treatment feminized (shortened) the EOD waveform by speeding up the inactivation kinetics of the electrocyte's voltage-gated Na + current (Dunlap et al, 1997).…”

“…In addition to uncovering how electrocyte ionic currents are subject to slow modulation by steroid hormones (Dunlap et al, 1997;Ferrari et al, 1995) and rapid modulation by peptide hormones (Markham et al, 2009b), another outcome of this line of research has been the finding that electrocytes in different species express a strikingly varied complement of ion currents.…”

Brain and gonadal aromatase activity and steroid hormone levels in female and polymorphic males of the peacock blenny Salaria pavo

“…For example, the weakly electric fish of the genus Sternopygus communicates using a sexually dimorphic electrical signal produced by a medullary electric organ. Androgens masculinize the properties of the signal (Few and Zakon, 2001;Mills and Zakon, 1991), probably by modifying the expression of voltage-gated ion channels in the cells of the electric organ (reviewed in Stoddard et al, 2006), while estrogens feminize the properties of this signal (Dunlap et al, 1997). Thus, the action of sex steroids on neural circuits may be partially regulated by local aromatization levels.…”

Adrenocorticotropic Hormone Enhances the Masculinity of an Electric Communication Signal by Modulating the Waveform and Timing of Action Potentials within Individual Cells

“…Sexual dimorphism in the EOD waveform develops over days to weeks as steroid hormones alter the duration of EODs, shaping longduration masculine EODs or shorter feminine EODs in many gymnotiform and mormyrid electric fish (Hagedorn and Carr, 1985;Bass and Volman, 1987;Mills and Zakon, 1991;Dunlap et al, 1997;Silva et al, 1999). Steroid hormones induce these waveform modulations by changing the kinetics of the constituent ionic currents of the EOD over a similar time scale (Ferrari et al, 1995;Dunlap et al, 1997). At the other extreme, ultra-rapid EOD modulations on the scale of milliseconds occur during courtship and aggressive interactions, a result of direct neural control of AP firing rate in the electric organ (for review, see Zakon et al, 2002).…”