Estrogen and Laryngeal Synaptic Strength in &lt;i&gt;Xenopus laevis:&lt;/i&gt; Opposite Effects of Acute and Chronic Exposure

Wu, Kwok; Tobias, Martha L.; Kelley, Darcy B.

doi:10.1159/000054667

Cited by 34 publications

(25 citation statements)

References 24 publications

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“…1 A); the effect was not yet present at the first hour postinjection. This result is consistent with the previous observation of slow incorporation of hCG into the circulation via the dorsal lymph sac (26). Both androgens [testosterone (T) and dihydrotestosterone (DHT)] supported calling equally well in castrated, hCG-treated males (Wilcoxon rank sum: P Ͼ 0.66).…”

supporting

confidence: 91%

Direct action of gonadotropin in brain integrates behavioral and reproductive functions

Yang¹,

Nasipak²,

Kelley

2007

Proc. Natl. Acad. Sci. U.S.A.

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Essential roles for gonadotropins in gonadal development and reproduction are well established. Over the past decade, however, the expression of luteinizing hormone receptor (LHR) has also been reported in the brain of various mammals and birds. Although suggestive, it has not yet been determined whether this expression pattern supports a novel function for gonadotropins. Here, we demonstrate a CNS-mediated role of gonadotropins in a reproductive behavior: the courtship songs of the South African clawed frog, Xenopus laevis. Male advertisement calling in this species depends on a nongonadal action of gonadotropin. To determine whether this effect is due to action on the CNS, we administered gonadotropin intracerebroventricularly (ICV) or systemically to intact or castrated males with or without concomitant androgen replacement. In intact and androgen-replaced gonadectomized males, gonadotropin significantly increased calling within 1 h after ICV injection. The effective dosage via ICV injections was less than one hundredth of the effective systemic dose. In situ hybridization with a cloned fragment of Xenopus LHR revealed strong expression in ventral forebrain areas important for vocal control. Further, gonadotropin treatment of brain in vitro up-regulates immunoreactivity for the LHR downstream target, egr-1, specifically in these vocal forebrain areas. Up-regulation occurs even when synaptic transmission is suppressed by incubation in Ca 2؉ free/high magnesium saline. These results demonstrate a neural role for gonadotropin in the control of calling behavior, potentially mediated via LHRs in forebrain vocal nuclei. Gonadotropin may play a novel integrative role in modulating both reproductive physiology and behavior.amphibian ͉ luteinizing hormone receptor ͉ neural action ͉ neuromodulator G onadotropins [luteinizing hormone (LH) in particular] play important roles in reproductive physiology across vertebrates. These heterodimeric glycoprotein hormones are typically released from the anterior pituitary in response to gonadotropin releasing hormone (GnRH), although some [e.g., human CG (hCG)] are produced in the placenta (1). LH and hCG stimulate the production of gonadal steroids, and exert their effects through binding to the same seven transmembrane domain G protein-coupled receptor (LHR, (1)). Until recently, LHR expression was believed to be confined to the gonads where it is required for fertility (for a review, see ref.2). However, recent findings of LHR expression in neural tissues in birds (3) and mammals (4), including humans (5-7), suggest potentially important functions for gonadotropins via direct action in the brain (8).To date, neural expression of LHRs in various mammalian and avian species has been documented in the hypothalamus, hippocampus, brainstem, cortex, choroid plexus, and pituitary (4). Based on these receptor distributions, several functions for LHRs have been hypothesized, including regulation of GnRH expressing cells (9-11), sensory information processing (12), modulation of hippocam...

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supporting

confidence: 91%

Direct action of gonadotropin in brain integrates behavioral and reproductive functions

Yang¹,

Nasipak²,

Kelley

2007

Proc. Natl. Acad. Sci. U.S.A.

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“…In the túngara frog, a previous study showed that hCG, which stimulates production of gonadal steroids (Lynch et al, 2006;Wu et al, 2001), increases egr-1 expression in the laminar nucleus of the torus (Lynch and Wilczynski, 2008). Our findings suggest that the effect observed by Lynch and Wilczynski (2008) was mediated by estradiol and not by direct effects of gonadotropins (Yang et al, 2007) or through changes in other steroids, such as progesterone or androgens.…”

Section: Discussionsupporting

confidence: 50%

“…Furthermore, in the auditory midbrain and parts of the limbic forebrain, estradiol receptor expression is sexually dimorphic , suggesting that estradiol is an important modulator of neural circuits underlying female-typical behavior. In addition, injections of human chorionic gonadotropins (hCGs), which stimulate production of gonadal steroids (Lynch et al, 2006;Wu et al, 2001), increase neural responses to conspecific social signals in the auditory midbrain (i.e. torus semicircularis) (Lynch and Wilczynski, 2008), suggesting that one way that estradiol modulates behavioral responses to conspecific calls is through modulation of auditory responses (Lynch and Wilczynski, 2008) or through integration of auditory and motor systems (see Hoke and Pitts, 2012).…”

Section: Introductionmentioning

confidence: 99%

Effects of estradiol on neural responses to social signals in female túngara frogs

Chakraborty

Burmeister

2015

Journal of Experimental Biology

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Estradiol plays an important role in mediating changes in female sexual behavior across reproductive cycles. In the tuńgara frog [Physalaemus (=Engystomops) pustulosus], the relationship between gonadal activity and female sexual behavior, as expressed by phonotaxis, is mediated primarily by estradiol. Estradiol receptors are expressed in auditory and motivational brain areas and the hormone could serve as an important modulator of neural responses to conspecific calls. To better understand how estradiol modifies neural responses to conspecific social signals, we manipulated estradiol levels and measured expression of the immediate early gene egr-1 in the auditory midbrain, thalamus and limbic forebrain in response to conspecific or heterospecific calls. We found that estradiol and conspecific calls increased egr-1 expression in the auditory midbrain and limbic forebrain, but in the thalamus, only conspecific calls were effective. In the preoptic area, estradiol enhanced the effect of the conspecific call on egr-1 expression, suggesting that the preoptic area could act as a hormonal gatekeeper to phonotaxis. Overall, the results suggest that estradiol has broad influences on the neural circuit involved in female reproduction, particularly those implicated in phonotaxis.

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“…For the most part, the sexually differentiated characteristics of the vocal system are due to the secretion of androgen from the testes; androgen controls developmental programs that determine cell number and type. One feature of this system, however, is controlled by secretion of estrogen from the ovary of mature or nearly mature females: estrogen regulates the strength of the synapse between laryngeal motor neurons and their target vocal muscles [12, 13]. …”

Section: Introductionmentioning

confidence: 99%

Estrogen Receptor Expression in Laryngeal Muscle in Relation to Estrogen-Dependent Increases in Synapse Strength

Tobias

Kelley³

2003

Neuroendocrinology

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In Xenopus laevis, the laryngeal neuromuscular synapse is the final effector for sexually differentiated song production. Females have stronger laryngeal synapses than males, and synapse strength is estrogen dependent. Estrogen-induced increases in synaptic strength require at least 3 weeks of exposure, suggesting that the hormone acts via a classical genomic mechanism involving the estrogen receptor (ER). The locus of the sex difference in synapse strength, determined using quantal analysis, is presynaptic, leading to the prediction that estrogen acts directly on vocal motor neurons. However, laryngeal motor neurons do not accumulate estrogen. Estrogen might instead affect motor neuron transmitter release via a retrograde signal from its target muscle. To test this hypothesis, we determined whether laryngeal muscle expresses ER. With RT-PCR using primers that recognize highly conserved domains of the ERα, mRNA products of the predicted size were amplified from laryngeal muscle as well as from other classical target tissues (forebrain and oviduct). Northern blots using a portion of the PCR product as primer revealed the same-sized band in oviduct and laryngeal muscle. Immunocytochemistry and Western blots confirmed the presence of ER protein in laryngeal muscle fibers and revealed several proteins in laryngeal muscle, brain and liver; among these was an approximately 66-kD protein – presumed to be full-length ER – that was the only one found in oviduct. Estrogen treatment of juveniles resulted in an upregulation of the 66-kD ER protein concomitant with an increase in quantal content. Taken together, these experiments strongly suggest that the ER is expressed by laryngeal muscle; this receptor could mediate estrogen-dependent changes in synaptic strength via retrograde signaling.

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Estrogen and Laryngeal Synaptic Strength in <i>Xenopus laevis:</i> Opposite Effects of Acute and Chronic Exposure

Cited by 34 publications

References 24 publications

Direct action of gonadotropin in brain integrates behavioral and reproductive functions

Direct action of gonadotropin in brain integrates behavioral and reproductive functions

Effects of estradiol on neural responses to social signals in female túngara frogs

Estrogen Receptor Expression in Laryngeal Muscle in Relation to Estrogen-Dependent Increases in Synapse Strength

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