Abstract

BackgroundGonadal and stress-related steroid hormones are known to influence auditory function across vertebrates but the cellular and molecular mechanisms responsible for steroid-mediated auditory plasticity at the level of the inner ear remain unknown. The presence of steroid receptors in the ear suggests a direct pathway for hormones to act on the peripheral auditory system, but little is known about which receptors are expressed in the ear or whether their expression levels change with internal physiological state or external social cues. We used qRT-PCR to measure mRNA expression levels of multiple steroid receptor subtypes (estrogen receptors: ERα, ERβa, ERβb; androgen receptors: ARα, ARβ; corticosteroid receptors: GR2, GR1a/b, MR) and aromatase in the main hearing organ of the inner ear (saccule) in the highly social African cichlid fish Astatotilapia burtoni, and tested whether these receptor levels were correlated with circulating steroid concentrations.ResultsWe show that multiple steroid receptor subtypes are expressed within the main hearing organ of a single vertebrate species, and that expression levels differ between the sexes. We also show that steroid receptor subtype-specific changes in mRNA expression are associated with reproductive phase in females and social status in males. Sex-steroid receptor mRNA levels were negatively correlated with circulating estradiol and androgens in both males and females, suggesting possible ligand down-regulation of receptors in the inner ear. In contrast, saccular changes in corticosteroid receptor mRNA levels were not related to serum cortisol levels. Circulating steroid levels and receptor subtype mRNA levels were not as tightly correlated in males as compared to females, suggesting different regulatory mechanisms between sexes.ConclusionsThis is the most comprehensive study of sex-, social-, and reproductive-related steroid receptor mRNA expression in the peripheral auditory system of any single vertebrate. Our data suggest that changes in steroid receptor mRNA expression in the inner ear could be a regulatory mechanism for physiological state-dependent auditory plasticity across vertebrates.

Highlights

  • Gonadal and stress-related steroid hormones are known to influence auditory function across vertebrates but the cellular and molecular mechanisms responsible for steroid-mediated auditory plasticity at the level of the inner ear remain unknown

  • GSI and circulating steroid levels GSI differed among all three reproductive stages in females (KW, H = 28.10, p < 0.001; Dunn's test, p < 0.05), where gravid females had mean values about four-fold greater than recovering females and ten-fold greater than brooding females (Figure 2A)

  • Serum E2 levels differed among all three female reproductive phases where gravid individuals had concentrations two-fold higher than recovering and over 10-fold higher than brooding individuals (ANOVA, F = 14.09, p < 0.001) (Figure 2C)

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Summary

Introduction

Gonadal and stress-related steroid hormones are known to influence auditory function across vertebrates but the cellular and molecular mechanisms responsible for steroid-mediated auditory plasticity at the level of the inner ear remain unknown. The peripheral and central auditory system of vertebrates is sensitive to sex- and stress-related steroid hormones, which can have profound effects on how an animal perceives acoustic information and behaves during social interactions While steroids such as estradiol are known to influence hearing in many vertebrate taxa [1,2,3,4], the cellular and molecular mechanisms responsible for steroid-mediated auditory plasticity at the level of the inner ear remain unknown. Postmenopausal women who are on estrogen-based hormone replacement therapy (HRT) have better hearing than those who are not [1], while progestin-based HRT can diminish hearing ability [5,6] These sex and female ovarian cycle variations in auditory ability are attributed to the protective effects of estrogen and may be partially related to estrogen receptor (ER) expression in the cochlea.

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