Estradiol modulates brainstem catecholaminergic cell groups and projections to the auditory forebrain in a female songbird

LeBlanc, Meredith M.; Goode, Christopher T.; MacDougall‐Shackleton, Elizabeth A.; Maney, Donna L.

doi:10.1016/j.brainres.2007.06.086

Cited by 52 publications

(81 citation statements)

References 59 publications

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“…Similarly, the selectivity of song-induced zenk responses in many hypothalamic and catecholaminergic brainstem cell groups, some of which may project directly to NCM, depends on E2 (Maney et al, 2008). We hypothesize that enhanced selectivity in E2-treated animals is driven at least partly by catecholaminergic innervation of NCM, since this innervation is E2-dependent (LeBlanc et al, 2007) and necessary for a selective zenk response (Lynch and Ball, 2008). Whether catecholaminergic innervation is modulated by E2 in the same domains of NCM as is ZENK-IR will be an interesting area of future research.…”

Section: Discussionmentioning

confidence: 94%

Topography of estradiol‐modulated genomic responses in the songbird auditory forebrain

Sanford

Lange

Maney

2009

Developmental Neurobiology

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Sex steroids facilitate dramatic changes in behavioral responses to sociosexual signals and are increasingly implicated in the sensory processing of those signals. Our previous work demonstrated that in female white-throated sparrows, which are seasonal breeders, genomic responses in the auditory forebrain are selective for conspecific song over frequency-matched tones only when plasma estradiol (E2) reaches breeding levels. Here, we sought to map this E2-dependent selectivity in the best-studied area of the auditory forebrain, the caudomedial nidopallium (NCM). Nonbreeding females with low endogenous levels of E2 were treated with E2 or a placebo and exposed to conspecific song, tones, or no sound playback. Immunoreactive protein product of the immediate early gene zenk (egr-1) was then quantified within seven distinct subregions, or domains, of NCM. We report three main findings: (1) regardless of hormone treatment, the zenk response is significantly higher in dorsal than in ventral NCM, and higher in medial than in lateral NCM; (2) E2-dependent selectivity of the response is limited to the rostral and medial domains of NCM; in the more caudal domains, song induces more zenk expression than tones regardless of hormone treatment; (3) even when no sound stimuli were presented, E2 treatment significantly increased zenk expression in the rostral, but not the caudal, domains of NCM. Together, the latter two findings suggest that E2-dependent plasticity in NCM is concentrated in rostral NCM, which is hodologically and neurochemically distinct from caudal NCM. Activity in rostral NCM may therefore be seasonally regulated in this species.

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Section: Discussionmentioning

confidence: 94%

Topography of estradiol‐modulated genomic responses in the songbird auditory forebrain

Sanford

Lange

Maney

2009

Developmental Neurobiology

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“…This finding likely reflects direct hormonal regulation, because the VTA expresses both androgen and estrogen receptors (40), and manipulations of sex steroids influence the number of TH-ir neurons in the VTA and TH-ir fiber density in telencephalic song regions (41,42).…”

Section: Da Neurons Of the Cg Are Strongly Coupled To Song And Reflectmentioning

confidence: 99%

Midbrain dopamine neurons reflect affiliation phenotypes in finches and are tightly coupled to courtship

Goodson

Kabelik

Kelly

et al. 2009

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

101

134

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Mesolimbic dopamine (DA) circuits mediate a wide range of goaloriented behavioral processes, and DA strongly influences appetitive and consummatory aspects of male sexual behavior. In both birds and mammals, mesolimbic projections arise primarily from the ventral tegmental area (VTA), with a smaller contribution from the midbrain central gray (CG). Despite the well known importance of the VTA cell group for incentive motivation functions, relationships of VTA subpopulations to specific aspects of social phenotype remain wholly undescribed. We now show that in male zebra finches (Estrildidae: Taeniopygia guttata), Fos activity within a subpopulation of tyrosine hydroxylase-immunoreactive (TH-ir; presumably dopaminergic) neurons in the caudal VTA is significantly correlated with courtship singing and coupled to gonadal state. In addition, the number of TH-ir neurons in this caudal subpopulation dichotomously differentiates courting from noncourting male phenotypes, and evolves in relation to sociality (flocking vs. territorial) across several related finch species. Combined, these findings for the VTA suggest that divergent social phenotypes may arise due to the differential assignment of ''incentive value'' to conspecific stimuli. TH-ir neurons of the CG (a population of unknown function in mammals) exhibit properties that are even more selectively and tightly coupled to the expression of courtship phenotypes (and appetitive courtship singing), both in terms of TH-ir cell number, which correlates significantly with constitutive levels of courtship motivation, and with TH-Fos colocalization, which increases in direct proportion to the phasic expression of song. We propose that these neurons may be core components of social communication circuits across diverse vertebrate taxa.song ͉ evolution ͉ periaqueductal gray ͉ vocalization A ffiliation behaviors such as courtship, pair bonding, grouping, and parental care can vary dramatically across individuals and species. However, despite the fact that we now know a good deal about the neurobiology of affiliation behaviors (1, 2), we still know very little about the phenotypic variations in neural mechanisms that underlie phenotypic differences in behavior. In fact, nonapeptide systems (the vasopressin-and oxytocin-like peptides) arguably provide the only examples from tetrapod vertebrates in which neural mechanisms have been systematically studied in relation to species-specific social structure (e.g., mating system and sociality) and individual differences in affiliation (3, 4).Among the many other neurochemical systems that regulate motivational and behavioral states, mesolimbic dopamine (DA) circuits are perhaps the strongest candidates as generators of phenotypic diversity. DA influences numerous affiliation behaviors such as pair bonding (5), sexual communication (6-8), and copulation (9-11). Of particular interest are DA cells in the ventral tegmental area (VTA), which are well known to regulate incentive and reward-related processes (12, 13). These cells project o...

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“…In female songbirds as in female rats and mice, catecholamines, their receptors, and/or synthetic enzymes are dense within the VMH, VTA, POM, and the striatum [1,10,30,34,38], and several lines of research implicate these areas in appetitive female responses to male courtship song. In female white-throated sparrows, estradiol increased the numbers of cells labeled for tyrosine hydroxylase (TH; the rate limiting enzyme in catecholamine synthesis) in VTA [34] and modified neural responses of the immediate early gene product ZENK (egr-1) to playback of male song in VTA, VMH, and POM [36].…”

Section: Introductionmentioning

confidence: 99%

Behavioral indices of breeding readiness in female European starlings correlate with immunolabeling for catecholamine markers in brain areas involved in sexual motivation

Pawlisch

Kelm‐Nelson

Stevenson

et al. 2012

General and Comparative Endocrinology

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Estradiol modulates brainstem catecholaminergic cell groups and projections to the auditory forebrain in a female songbird

Cited by 52 publications

References 59 publications

Topography of estradiol‐modulated genomic responses in the songbird auditory forebrain

Topography of estradiol‐modulated genomic responses in the songbird auditory forebrain

Midbrain dopamine neurons reflect affiliation phenotypes in finches and are tightly coupled to courtship

Behavioral indices of breeding readiness in female European starlings correlate with immunolabeling for catecholamine markers in brain areas involved in sexual motivation

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