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

Abstract

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.

Influence of long-term social interaction on chirping behavior, steroid levels and neurogenesis in weakly electric fish

“…In A. leptorhynchus, androgen treatment enhances chirp rate in gonadectomized males (Dunlap et al, 1998) and intact females (Dulka et al, 1995) presented artificial stimuli. Similarly, plasma androgen [11-ketotestosterone (11-KT)] concentrations correlate positively with chirp rate during short-term (15min) dyadic encounters between males (Dunlap, 2002), However, long-term social interaction between males, which potentiates chirping, has no effect on plasma 11-KT levels .…”

“…In one common experimental setup, fish are placed in a testing apparatus, a 'chirp chamber', and presented with stimuli whose frequency and amplitude can be easily controlled and standardized (Zupanc and Maler, 1993;Larimer and MacDonald, 1968). In both direct dyadic interactions and chirp chamber responses, chirping is highly sexually dimorphic, with males producing chirps at 10-20 times higher rates than females (Dunlap, 2002;Zupanc and Maler, 1993;Dulka et al, 1995).…”

“…For example, exogenous treatment of fish with arginine vasotocin (Bastian et al, 2001), noradrenaline (Maler and Ellis, 1987), androgens (Dunlap et al, 1998;Dulka et al, 1995) or cortisol (Dunlap et al, 2006) increases chirp rates, while treatment with serotonin inhibits chirping via the 5HT2 receptor (Maler and Ellis, 1987;Telgkamp et al, 2007;Smith and Combs, 2008).…”

Neuroendocrine control of a dynamic communication signal

“…Fish in the genus Apternotus produce rapid EOD modulations in response to social stimuli, behaviors known as chirps. The tendency to produce chirps in response to simulated electronic stimuli is characteristically male; addition of testosterone (T) or DHT leads to enhancement of this behavior (Dulka et al, 1995;Meyer, 1983).…”

“…Earlier studies have quantified androgen-induced changes in electrocyte morphology, waveform frequency and shape, and an individual's response to artificial stimuli rather than interactions with another individual (Dulka et al, 1995;Hagedorn and Heiligenberg, 1985;Zakon, 1996). I know of no published studies to date that examine whether androgens modify behavioral responses of electric fish, using a methodology that combines androgen treatment with social challenges from live conspecifics that interact with focal individuals.…”