Brain estrogen signaling effects acute modulation of acoustic communication behaviors: A working hypothesis

Abstract

Summary Although estrogens are widely considered circulating ‘sex steroid hormones’ typically associated with female reproduction, recent evidence suggests that estrogens can act as local modulators of brain circuits in both males and females. Functional implications of this newly-characterized estrogen signaling system have begun to emerge. This essay summarizes evidence in support of the hypothesis that the rapid production of estrogens in brain circuits can drive acute changes in both the production and perception of acoustic communication behaviors. These studies reveal two fundamental neurobiological concepts: 1) estrogens can be produced locally in brain circuits independent of levels in nearby circuits and in the circulation, and 2) estrogens can have very rapid effects within these brain circuits to modulate social vocalizations, acoustic processing, and sensorimotor integration. This research relies on a vertebrate-wide span of investigations, including vocalizing fishes, amphibians and birds, emphasizing the importance of comparative model systems in understanding principles of neurobiology.

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

“…Our results for the auditory midbrain parallel a number of studies from other taxa that describe an important role for estradiol in sensory processing of social signals and of audition (Arch and Narins, 2009;Caras, 2013;Earp and Maney, 2012;Maney, 2013;Maney et al, 2006Maney et al, , 2008Maney and Pinaud, 2011;Petrulis, 2013;Remage-Healey, 2012, 2014Sanford et al, 2010;Sisneros, 2009c;Tremere et al, 2009;Walpurger et al, 2004;Yovanof and Feng, 1983). 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).…”

“…There are also broad correspondences between egr-1 (also known as ZENK) expression and electrophysiological activity in songbirds: ZENK expression is selective for conspecific social signals (song) over tones only in the presence of estradiol in female white-throated sparrows (Zonotrichia albicolis) (Maney et al, 2006(Maney et al, , 2008Maney and Pinaud, 2011). Estradiol also enhances auditory encoding of song, sometimes through rapid effects of brain-derived estradiol (Krentzel and Remage-Healey, 2015;Remage-Healey, 2012, 2014RemageHealey et al, 2010;Tremere and Pinaud, 2011). In zebra finches, the impact of estradiol extends further to the song control system, as estradiol enhances the neural selectivity for the bird's own song (BOS) but not to conspecific songs and fadrozole injections reduce this selectivity (Remage-Healey and Joshi, 2012).…”

“…For example, estradiol shapes auditory tuning in midshipmen fish so that, during the breeding season, females are more sensitive to the harmonics in the calls of courting males, which enhances the adaptive coupling of the sender and the receiver for reproductive success (Sisneros, 2009a,b,c;Sisneros et al, 2004). Similar mechanisms of estradiol-dependent modulation of acoustic communication circuits are present in birds in response to plasma estradiol (Maney et al, 2006(Maney et al, , 2008Maney and Pinaud, 2011;Sanford et al, 2010) and locally produced neuroestrogens (Krentzel and Remage-Healey, 2015;Pawlisch and Remage-Healey, 2015;Remage-Healey, 2012, 2014RemageHealey et al, 2010RemageHealey et al, , 2008Remage-Healey and Joshi, 2012).…”

Male fidelity expressed through rapid testosterone suppression of ultrasonic vocalizations to novel females in the monogamous California mouse

“…5 Although most studies of T and mating effort have examined long-term changes in baseline T, recent attention has been given to the dynamic changes in T and other steroid hormones on sexual behavior on smaller time scales that can induce rapid changes in behavior, particularly in response to dynamic social conditions (Cross and Roselli, 1999;Mangiamele and Thompson, 2012;Remage-Healey and Bass, 2010;Remage-Healey, 2012). In rodents, like other mammals, transient increases (henceforth "pulses") of T have been widely observed among males in response to encounters with females (Batty, 1978;Coquelin and Bronson, 1980;James et al, 2006;Macrides et al, 1975;Nyby, 2008;reviewed by Gleason et al, 2009), but the consequences of these T pulses are not well understood, and even less so regarding extra-pair mating in monogamous species.…”

Whither the gonads? (Comment on DOI 10.1002/bies.201200081)

“…In this issue of BioEssays, RemageHealey describes an elegant body of work demonstrating that estradiol, traditionally considered an ovarian hormone, is synthesized within the brain and affects local neuronal activity [1]. In zebra finches, hearing conspecific song induces estradiol release in the auditory forebrain, which rapidly alters firing properties both in that area and in downstream sensorimotor regions.…”