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Effects of Song Experience and Song Quality on Immediate Early Gene Expression in Female Canaries (Serinus Canaria)

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Effects of Song Experience and Song Quality on Immediate Early Gene Expression in Female Canaries (Serinus Canaria) Effects of Song Experience and Song Quality on Immediate Early Gene Expression in Female Canaries (Serinus canaria) Chelsea M. Haakenson , Farrah N. Madison, Gregory F. Ball Program in Neuroscience and Cognitive Science, Department of Psychology, University of Maryland, College Park, Maryland 20742 Received 2 January 2019; revised 6 March 2019; accepted 1 May 2019 ABSTRACT: Female songbirds are thought to make song with or without special syllables for 14 days. After mate choices based on aspects of male song quality. Male transfer to individual housing, birds were played one of canaries (Serinus canaria) produce songs with “special” the aforementioned stimuli or silence. ZENK expression syllables that have been shown to be highly salient to in CMM and NCM was equivalent for song with and female listeners – eliciting high rates of sexual displays without special syllables, but significantly lower for and enhanced immediate early gene (IEG) expression. silence. Females who experienced song with special Immunohistochemistry for the IEG ZENK was used to syllables had lower plasma estradiol concentrations after examine the effects of experience with these syllables on final song playback. This study indicates that CMM activity in the caudal mesopallium (CMM) and nidocaudal exhibits an IEG response bias to special syllables in mesopallium (NCM), two auditory areas important in limited acoustic contexts, but not in full song, which may processing conspecific song. Photostimulated female contain additional biologically relevant information. canaries were housed in sound attenuated chambers Furthermore, estradiol concentrations may mediate and played pseudosongs containing either three special changes in song responses, serving as a mechanism for syllables or three non-special syllables, an intro, and modulating mate choice in differing song environments. an outro sequence. Females that heard special syllable © 2019 Wiley Periodicals, Inc. Develop Neurobiol 79: 521–535, 2019 pseudosongs exhibited higher ZENK expression in CMM. Keywords: immediate early gene; auditory perception; To assess the effects of experience, photostimulated bird song; female choice; sexual selection; canary; females were pair housed and exposed to playback of Serinus canaria INTRODUCTION syllables (Searcy, 1992; Vallet et al., 1998; Gentner and Hulse, 2000). Females choose males with songs When songbirds are making mating decisions, song containing these particular features, since they can quality serves as an essential factor in the decision serve as an honest signal of mate quality (Gil and process (Searcy, 1986; Kroodsma and Byers, 1991). Gahr, 2002). However, it is unclear to what extent Different songbird species have particular song fea- these decisions are due to an innate preference for spe- tures that are of preeminent importance for mate cific song features or due to preferences determined choice, such as song length, repertoire size, or special by experience of a particular social environment. One way to examine the relative weights of these factors at the cellular level is by measuring dif- Correspondence to: C. M. Haakenson ([email protected]) ferences in expression of immediate early genes Contract grant sponsor: National Institute of Neurological (IEGs). IEGs are transcription factors that are rapidly Disorders and Stroke; contract grant number: 1 R01 NS104008-01. © 2019 Wiley Periodicals, Inc. induced following the activation of a neuron and Published online 16 May 2019 in Wiley Online Library are, therefore, useful molecular markers of neuronal (wileyonlinelibrary.com). activation (Farivar et al., 2004). In particular, ZENK DOI 10.1002/dneu.22685 521 522 Haakenson et al. ((an acronym for zif-268 (Christy et al., 1988), egr-1, lead to increased selectivity through repeated activa- (Sukhatme et al., 1988), ngfi-a, (Milbrandt, 1987), and tion of ZENK and its downstream targets, promoting krox-24, (LeMaire et al., 1988)) has been shown to be synaptic plasticity. a robust example of a song-inducible gene (Mello et Another possible mechanism for this experience-de- al., 1992; Mello and Clayton, 1994; Mello and Ribeiro, pendent plasticity and the consequent variation in 1998; Leitner et al., 2005). In several songbird species, song preferences are catecholamine-mediated changes the magnitude of the ZENK response in auditory pro- in neuronal response properties. The catecholamines cessing areas has been found to correlate with song dopamine (DA) and norepinephrine (NE) are influen- attractiveness and behavioral measures of female mate tial in determining response properties of the auditory preferences. For example, white-crowned sparrows system in a context-dependent manner (Cirelli et al., exhibit greater ZENK expression in the caudal meso- 1996; Dave et al., 1998; Bao et al., 2001; Cardin and pallium (CMM) and dorsal nidocaudal mesopallium Schmidt, 2004; Cirelli and Tononi, 2004; Castelino (NCMd) in response to playback of song in their hatch and Ball, 2005). Furthermore, behavioral and neural dialect, which is correlated with copulation solicitation selectivity for attractive song is reduced following nor- displays and other preference behaviors (Maney et al., adrenergic denervation (Appeltants et al., 2002; Lynch 2003). Wild-caught house finches have an enhanced and Ball, 2008). Female starlings exposed to long songs induction of ZENK in CMM, NCMd, and NCMv fol- exhibited elevated levels of the norepinephrine metab- lowing playback of conspecific song versus heterospe- olite, 3-Methoxy-4-hydroxyphenylglycol (MHPG), cific song (Hernandez and MacDougall-Shackleton, the dopamine metabolite, 3,4-Dihydroxyphenylacetic 2004). In addition, activity in the caudocentral ni- acid (DOPAC), and had an increased probability of dopallium (NCC) has been shown to be higher when fibers immunoreactive for dopamine beta hydroxy- female zebra finches hear female-directed song rather lase (DBH) in NCM (Sockman and Salvante, 2008). than undirected song (Van Ruijssevelt et al., 2018). Therefore, in environments with an abundance of Therefore, differences in ZENK expression following high quality song, increased catecholamine innerva- presentation of a variety of song types can indicate the tion in auditory areas may support increased female relative levels of preference for these songs. selectivity. In addition to serving as a marker of neuronal ac- Estrogenic effects on auditory processing may also tivation, song-induced expression of ZENK may also be involved in this process. Estradiol is important represent a molecular mechanism necessary for the for modulating selectivity for specific song features. cellular plasticity that produces experience-depen- Selective ZENK responses for conspecific song de- dent variation in auditory processing. The induction of pend on circulating estradiol above non-breeding ZENK is subject to habituation, as repeated playback baseline levels (Maney et al., 2006). In addition, hear- of the same song results in diminished ZENK expres- ing song leads to increases in estradiol concentrations sion (Jarvis et al., 1995). ZENK induction has also in NCM (Remage-Healey et al., 2008). Repeated ex- been implicated in the molecular cascade responsible posure to song could lead to increases in estradiol that for the formation and stability of long-term memories promote selectivity in subsequent responses to song. (Clayton, 2000; Jones et al., 2001). Differences in song These proposed mechanisms – ZENK-induced quality in the social environment could lead to re- cellular plasticity, catecholamine innervation, and peated differences in song-induced ZENK expression, estrogenic-mediated selectivity – are all highly inter- which could then influence later ZENK expression twined. Estradiol treatment increases the density of at the time of mate selection through this signaling fibers immunoreactive for tyrosine hydroxylase (TH) cascade. In one songbird species, European starlings or DBH (Sanford et al., 2010). Additionally, estradiol (Sturnus vulgaris), females prefer males that produce can induce ZENK expression (Tremere et al., 2009). long-bout songs compared to short-bout songs, as as- Therefore, experience-dependent variation in song se- sessed by both behavioral preference and IEG expres- lectivity may be due to some combination of all three. sion in the auditory telencephalon (Gentner and Hulse, In the present study, we examine if these mecha- 2000; Gentner et al., 2001). However, female starlings nisms of song selectivity are also efficacious in song exposed to only short-bout songs for one week exhib- selectivity canaries (Serinus canaria). Canary males ited a reduction in the selectivity of ZENK response to produce songs with “sexy” or “special” syllables that long-bout songs in comparison to female starlings ex- are composed of two simultaneous high-frequency posed to long-bout songs, who continued to exhibit a notes with a high-repetition rate (Vallet, 1995; Vallet selective response to long-bout songs (Sockman et al., et al., 1998). They are difficult to produce because 2002). Repeated exposure to especially salient song they require rapid sequential use of both sides of the features, such as long-bout songs in starlings, may syrinx (Suthers et al., 2012). These special syllables Developmental Neurobiology Effects of Song Experience and Quality 523 are highly salient to female listeners and elicit high Experiment 1: Pseudosong Experiment. For the experi- rates of sexual copulation solicitation displays (Vallet ment examining differences in
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