Estradiol-dependent modulation of auditory processing and selectivity in songbirds

Maney, Donna L.; Pinaud, Raphael

doi:10.1016/j.yfrne.2010.12.002

Cited by 95 publications

(118 citation statements)

References 226 publications

(333 reference statements)

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“…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.…”

Section: Discussionsupporting

confidence: 51%

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

Gall

Wilczynski

2014

Journal of Experimental Biology

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There is a long history in neuroethology of investigating how communication signals influence the brain and behavior. It has become increasingly clear that brain areas associated with sensory processing are plastic in adults and that this plasticity is related to reproductive condition. However, the role of communication signal reception in adult auditory plasticity has received relatively little attention. Here, we investigated whether the reception of communication signals (a frog chorus) could enhance the responsiveness of the auditory system to future reception of communication signals (a single male call). We found that animals that had been exposed to 10 days of a male chorus had stronger auditory midbrain immediate early gene expression than animals that had been exposed to 10 days of random tones when tested with 30 min of male calls or 30 min of tones. Our results suggest that exposure to dynamic social stimuli, like frog choruses, may play an important role in shaping the neural and behavioral responses to communication signals.

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Section: Discussionsupporting

confidence: 51%

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

Gall

Wilczynski

2014

Journal of Experimental Biology

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“…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).…”

Section: Discussionsupporting

confidence: 87%

“…That is, both reproductive activity (Miranda and Wilczynski, 2009) and estradiol treatment (Yovanof and Feng, 1983) increase auditory responses to sounds in frogs, including biologically irrelevant sounds (noise burst, tones) as well as conspecific calls. 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).…”

Section: Discussionmentioning

confidence: 99%

“…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).…”

Section: Introductionmentioning

confidence: 99%

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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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“…Steroid hormones can induce variation in physiological state that dramatically affects responses to socially relevant stimuli (1,36,37). Steroids can also modify cognitive processes ranging from attention (38) to learning (2, 3) that affect the probability and quality of a particular behavioral response.…”

Section: Discussionmentioning

confidence: 99%

Differential effects of global versus local testosterone on singing behavior and its underlying neural substrate

Alward

Balthazart

Ball

2013

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

118

144

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Steroid hormones regulate multiple but distinct aspects of social behaviors. Testosterone (T) has multiple effects on learned courtship song in that it regulates both the motivation to sing in a particular social context as well as the quality of song produced. The neural substrate(s) where T acts to regulate the motivation to sing as opposed to other aspects of song has not been definitively characterized. We show here that T implants in the medial preoptic nucleus (POM) of castrated male canaries (Serinus canaria) increase song rate but do not enhance acoustic features such as song stereotypy compared with birds receiving peripheral T that can act globally throughout the brain. Strikingly, T action in the POM increased song control nuclei volume, consistent with the hypothesis that singing activity induces neuroplasticity in the song control system independent of T acting in these nuclei. When presented with a female canary, POM-T birds copulated at a rate comparable to birds receiving systemic T but produced fewer calls and songs in her presence. Thus, POM is a key site where T acts to activate copulation and increase song rate, an appetitive sexual behavior in songbirds, but T action in other areas of the brain or periphery (e.g., HVC, dopaminergic cell groups, or the syrinx) is required to enhance the quality of song (i.e., stereotypy) as well as regulate context-specific vocalizations. These results have broad implications for research concerning how steroids act at multiple brain loci to regulate distinct sociosexual behaviors and the associated neuroplasticity.activity-driven plasticity | singing motivation | preoptic area S teroid hormones such as testosterone (T) can have multiple effects on physiology, morphology, and behavior (1-4). These pleiotropic effects of steroids allow coordinating suites of traits into an organized functional response (5, 6). In the case of the regulation of behavior, both motivational and performance aspects of behavior as well cognitive components are often activated by the same hormone (2, 7). The neural sites of steroid action coordinating these distinct aspects of an integrated behavioral response have not been well characterized. In this study, we investigated the site of hormone action in relation to the activation of different aspects of birdsong to illustrate how such an integrated regulation can occur.Birdsong is a species-typical, stereotypic set of usually long, learned, complex vocalizations produced in reproductive contexts (8). A discrete network of interconnected brain nuclei orchestrates song learning and production (from here on called the song control system or SCS) (3, 9-11). Areas such as HVC (acronym is proper name) and the robust nucleus of the arcopallium (RA) regulate the production of song, whereas areas such as Area X and LMAN are involved in song learning. These forebrain nuclei can undergo remarkable plasticity in response to seasonally changing T (12, 13; see refs. 2 and 14 for review). There is also evidence that other factors such as singing ac...

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Estradiol-dependent modulation of auditory processing and selectivity in songbirds

Cited by 95 publications

References 226 publications

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

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

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

Differential effects of global versus local testosterone on singing behavior and its underlying neural substrate

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