Human chorionic gonadotropin‐induced shifts in the electrosensory system of the weakly electric fish, <i>Sternopygus</i>

Zakon, Harold H.; Yan, Hong-Young; Thomas, Peter

doi:10.1002/neu.480210515

Cited by 24 publications

(23 citation statements)

References 18 publications

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“…This assay was validated previously for Sternopygus in the Thomas laboratory (Zakon et al, 1990). Each steroid was extracted separately from 100 -200 l of plasma with a 70:30 mixture of hexane and ethyl acetate.…”

Section: Methodsmentioning

confidence: 99%

“…Each sample was incubated overnight at 4°C with the appropriate antiserum (Radioassay Systems Laboratory) and tritiated steroid. Based on previous studies, the estradiol antiserum cross-reacts 22.3% with 16-ketoestradiol, 2.5% with estriol, and 1.3% with estrone, and the T antibody reacts 28.0% with dihydrotestosterone and 17.0% with 11-ketotestosterone (Zakon et al, 1990). The unbound fraction was removed by charcoal and centrifugation, and the bound fraction was counted in a scintillation counter.…”

Section: Methodsmentioning

confidence: 99%

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Estrogen Modifies an Electrocommunication Signal by Altering the Electrocyte Sodium Current in an Electric Fish,Sternopygus

1997

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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 ...

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Estrogen Modifies an Electrocommunication Signal by Altering the Electrocyte Sodium Current in an Electric Fish,Sternopygus

1997

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“…However, it is possible that male-specific androgens play a role in establishing male chirp rates. For example, 1 l-ketotestosterone is the predominant blood androgen in most male teleosts (Idler et al, 1960), and is present in higher concentrations than T in at least one species of electric fish, Sternopygus macrurus (Zakon et al, 1990(Zakon et al, , 1991. Thus, it remains to be determined if male chirping is regulated by a hormonal mechanism involving 1 I-ketotestosterone, or whether other factors are involved.…”

Section: Androgen-induced Changes In Chirp Structurementioning

confidence: 99%

Androgen-induced changes in electrocommunicatory behavior are correlated with changes in substance P-like immunoreactivity in the brain of the electric fish Apteronotus leptorhynchus

1995

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The hormonal regulation of sex differences in electrocommunicatory behavior and brain substance P-like immunoreactivity (SPI-ir) were examined in the weakly electric fish, Apteronotus leptorhynchus. This animal modulates its electric organ discharge (EOD) to produce discrete electric social signals (chirps), which function in aggressive and reproductive displays. Males readily chirp in response to electrosensory stimuli that mimic the presence of a conspecific; females also chirp in response to such stimuli, but do so at much lower rates than males. We have recently demonstrated that androgen treatment enhances chirping behavior in females and may also lead to a change in chirp quality or structure. In this study, we quantified androgen- induced changes in chirp structure and simultaneously examined whether androgens alter the sexually dimorphic pattern of SPI-ir in a brain region (prepacemaker nucleus, PPn) known to control chirping. Our results demonstrate that, in females, androgens cause both the induction of chirping and an alteration of chirp structure; chirps recorded from androgen-implanted females had longer durations and more dramatic frequency and amplitude modulations compared to controls, and appear similar to those reported to be produced during spawning. Moreover, androgen-induced changes in chirping are correlated with increased expression of SPI-ir within specific brain nuclei of females. These changes may underly behavioral changes in chirping, since treated females showed a male-like pattern of SPI-ir in the PPn. However, alterations in SPI-ir were not restricted to the PPn, but also occurred in diencephalic regions related to pituitary function and reproductive behavior. The results suggest that androgens modulate chirping activity and cause both specific and wide-spread changes in SPI-ir that may relate to a functional system that interrelates pituitary function, reproductive behavior, and chirping.

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“…In agreement with this, plasma levels of T and the teleostean androgen 11-ketotestosterone (11 -KT) are high in males with a low EOD frequency [Zakon el al., 1991], Conversely, estradiol-17$ (E2) and human chori onic gonadotropin raise EOD frequency in gonadectomized individuals of both sexes [Meyer, 1983;Zakon et al, 1990]. It is not clear whether human chorionic gonadotropin acts directly on the EOD-generating cir cuitry or via the mediation of another hormone.…”

Section: Hormonal Modulation Of Eod Waveform and Electric Organ Ima' mentioning

confidence: 99%

Hormonal Modulation of Communication Signals in Electric Fish

Zakon¹

1996

Dev Neurosci

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Steroid hormones have profound effects on vertebrate behaviors. Yet, in most cases we can neither identify the neurons responsible for particular behaviors nor how steroids alter their excitability. Electric fish emit sexually dimorphic electric organ discharges (EODs) the waveform of which may be altered by steroid treatment. These communication signals are generated by a medullary pacemaker nucleus (PMN) composed of two cell types. The output neurons of the PMN synapse on spinal cord electromotoneurons which then innervate the electric organ. The PMN receives input from only two sources, and these are responsible for brief modulations that occur during social interactions. The small numbers and stereotyped electrical behaviors of the cells in the EOD-generating circuitry and their access for biophysical recording makes them a convenient model system to study the actions of steroids on identified cells.

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Human chorionic gonadotropin‐induced shifts in the electrosensory system of the weakly electric fish, Sternopygus

Cited by 24 publications

References 18 publications

Estrogen Modifies an Electrocommunication Signal by Altering the Electrocyte Sodium Current in an Electric Fish,Sternopygus

Estrogen Modifies an Electrocommunication Signal by Altering the Electrocyte Sodium Current in an Electric Fish,Sternopygus

Androgen-induced changes in electrocommunicatory behavior are correlated with changes in substance P-like immunoreactivity in the brain of the electric fish Apteronotus leptorhynchus

Hormonal Modulation of Communication Signals in Electric Fish

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