Reproductive Hormones Modify Reception of Species-Typical Communication Signals in a Female Anuran

Abstract

In many vertebrates, the production and reception of species-typical courtship signals occurs when gonadotropin and gonadal hormone levels are elevated. These hormones may modify sensory processing in the signal receiver in a way that enhances behavioral responses to the signal. We examined this possibility in female túngara frogs (Physalaemus pustulosus) by treating them with either gonadotropin (which elevated estradiol) or saline and exposing them to either mate choruses or silence. Expression of an activity-dependent gene, egr-1, was quantified within two sub-nuclei of the auditory midbrain to investigate whether gonadotropin plus chorus exposure induced greater egr-1 induction than either of these stimuli alone. The laminar nucleus (LN), a sub-nucleus of the torus semicircularis that contains steroid receptors, exhibited elevated egr-1 induction in response to chorus exposure and gonadotropin treatment. Further analysis revealed that neither chorus exposure nor gonadotropin treatment alone elevated egr-1 expression in comparison to baseline levels whereas gonadotropin + chorus exposure did. This suggests that mate signals and hormones together produce an additive effect so that together they induce more egr-1 expression than either alone. Our previously published studies of female túngara frogs reveal that (1) gonadotropin-induced estradiol elevations also increase behavioral responses to male signals, and (2) reception of male signals elevates estradiol levels in the female. Here, we report data that reveal a novel mechanism by which males exploit female sensory processing to increase behavioral responses to their courtship signals.

Prior experience with conspecific signals enhances auditory midbrain responsiveness to conspecific vocalizations

“…In turn, hormone levels affect behavioral responses to communication signals in frogs, fish, birds, reptiles and mammals (Adkins-Regen, 2005). In the case of acoustic communication, the reception of signals themselves can be influenced by hormones, as hormones have been shown to increase immediate early gene and electrophysiological responses in the auditory system (Arch and Narins, 2009;Lynch and Wilczynski, 2008;Maney and Pinaud, 2011;Penna et al, 1992;Yoder and Vicario, 2012). Here, we found that the responsiveness of the auditory midbrain to acoustic communication signals can be similarly enhanced by chronic exposure to dynamic conspecific signals.…”

“…female phonotaxis and male antiphonal calling behavior (Diekamp and Gerhardt, 1995;Gerhardt, 1974;Gerhardt, 1981a;Gerhardt, 1981b;Gerhardt, 1991;Simmons et al, 1993) mate attraction signals -and synthetic stimuli with similar spectral-temporal features are processed selectively or with enhanced responsiveness by neurons in many brain regions [as revealed in electrophysiology studies (Diekamp and Gerhardt, 1995;Eggermont and Epping, 1986;Elliott et al, 2011;Fuzessery and Feng, 1983;Miranda and Wilczynski, 2009a;Miranda and Wilczynski, 2009b;Rose et al, 1985) and immediate early gene studies (Chakraborty et al, 2010;Hoke et al, 2004;Hoke et al, 2008;Lynch and Wilczynski, 2008;Mangiamele and Burmeister, 2011)]. In anuran amphibians, this is particularly apparent in the midbrain (reviewed in Rose and Gooler, 2007;Wilczynski and Ryan, 2010).…”

“…The torus is sensitive not only to conspecific signals (Hoke et al, 2004) (for review, see Rose and Gooler, 2007) but also to artificial stimuli that contain a frequency step necessary and sufficient for species identification (Mangiamele and Burmeister, 2011), suggesting it plays an important role in acoustically based species recognition. It has been hypothesized that the activation level of the torus may be directly related to the level of acoustically evoked reproductive behaviors, such as phonotaxis (Lynch and Wilczynski, 2008). Therefore, factors that modulate the responsiveness of the torus are expected to have major consequences for reproductive behaviors.…”

“…In fact, both midbrain neural processing (Goense and Feng, 2005;Lynch and Wilczynski, 2008;Miranda and Wilczynski, 2009a;Penna et al, 1992;Yovanof and Feng, 1983) and behavioral responses (Burmeister and Wilczynski, 2001;Chakraborty and Burmeister, 2009;Lynch and Wilczynski, 2006) In many taxa there are reciprocal interactions between communication and hormonal state (Adkins-Regan, 2005). It has been known for some time that the reception of mating signals can alter hormone levels and enhance gonadal development [e.g.…”

Estradiol Shapes Auditory Processing in the Adult Brain by Regulating Inhibitory Transmission and Plasticity-Associated Gene Expression

“…It is clear that the plasma levels of gonadal steroids impact a variety of social behaviors, including the perception of, and responsiveness to, sociosexual signals (Sisneros et al, 2004;Maney et al, 2006;Lynch and Wilczynski, 2008). Such a role of sex steroid hormones in vertebrates results from activity within a "social behavioral network" that includes sexual motivational brain areas such as the medial preoptic area of the hypothalamus and the medial extended amygdala (Newman, 1999;Goodson, 2005).…”