Testosterone alters genomic responses to song and monoaminergic innervation of auditory areas in a seasonally breeding songbird

Matragrano, Lisa L.; LeBlanc, Meredith M.; Chitrapu, Anjani; Blanton, Zane E.; Maney, Donna L.

doi:10.1002/dneu.22072

Cited by 23 publications

(19 citation statements)

References 99 publications

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“…In contrast, expression of OTR mRNA increased in RA in birds of the TS morph but not the WS morph. Morph-dependent effects of T on the brain are consistent with the findings of Matragrano et al (2013), who reported that T administration reduced serotonergic innervation of the auditory forebrain in WS but not TS males.…”

Section: Discussionsupporting

confidence: 89%

“…We are currently mapping and characterizing the effects of morph on the expression of both genes in the brain, which may ultimately shed light on the mechanisms underlying morph-dependent effects of T-treatment on VTR expression. Our current results, together with the findings of Matragrano et al (2013) on serotonin fiber density, demonstrate a clear mechanism by which hormones may interact with genotype to affect social behavior.…”

Section: Discussionsupporting

confidence: 71%

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Hormonal regulation of vasotocin receptor mRNA in a seasonally breeding songbird

Grozhik

Horoszko

Horton

et al. 2014

Hormones and Behavior

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Behaviors associated with breeding are seasonally modulated in a variety of species. These changes in behavior are mediated by sex steroids, levels of which likewise vary with season. The effects of androgens on behaviors associated with breeding may in turn be partly mediated by the nonapeptides vasopressin (VP) and oxytocin (OT) in mammals, and vasotocin (VT) in birds. The effects of testosterone (T) on production of these neuropeptides have been well-studied; however, the regulation of VT receptors by T is not well understood. In this study, we investigated steroid-dependent regulation of VT receptor (VTR) mRNA in a seasonally breeding songbird, the white-throated sparrow (Zonotrichia albicollis). We focused on VTR subtypes that have been most strongly implicated in social behavior: V1a and oxytocin-like receptor (OTR). Using in situ hybridization, we show that T-treatment of non-breeding males altered V1a and OTR mRNA expression in several regions associated with seasonal reproductive behaviors. For example, T-treatment increased V1a mRNA expression in the medial preoptic area, bed nucleus of the stria terminalis, and ventromedial hypothalamus. T-treatment also affected both V1a and OTR mRNA expression in nuclei of the song system; some of these effects depended on the presence or absence of a chromosomal rearrangement that affects singing behavior, plasma T, and VT immunolabeling in this species. Overall, our results strengthen evidence that VT helps mediate the behavioral effects of T in songbirds, and suggest that the chromosomal rearrangement in this species may affect the sensitivity of the VT system to seasonal changes in T.

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Section: Discussionsupporting

confidence: 89%

Section: Discussionsupporting

confidence: 71%

Hormonal regulation of vasotocin receptor mRNA in a seasonally breeding songbird

Grozhik

Horoszko

Horton

et al. 2014

Hormones and Behavior

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“…Thresholding was based on the contrast in pixel intensity between specific staining and background and was consistent across brain regions. Threshold levels were checked by eye to ensure that fiber staining corresponded to the pixels selected by ImageJ (Lorentz et al 2010; Matragrano et al 2013). For each image, the area occupied by pixels with an intensity value above the background level was converted to mm 2 and averaged across the group.…”

Section: Methodsmentioning

confidence: 99%

Differential roles for cortical versus sub-cortical noradrenaline and modulation of impulsivity in the rat

Benn

Robinson

2016

Psychopharmacology

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RationaleAtomoxetine is a noradrenaline re-uptake inhibitor licensed for the treatment of adult and childhood attention deficit hyperactivity disorder. Although atomoxetine has established efficacy, the mechanisms which mediate its effects are not well understood.ObjectivesIn this study, we investigated the role of cortical versus sub-cortical noradrenaline by using focal dopamine beta hydroxylase-saporin-induced lesions, to the prefrontal cortex (n = 16) or nucleus accumbens shell (n = 18).MethodsHealthy animals were tested by using the forced-choice serial reaction time task to assess the impact of the lesion on baseline performance and the response to atomoxetine and the psychostimulant amphetamine.ResultsWe observed attenuation in the efficacy of atomoxetine in animals with lesions to the nucleus accumbens shell, but not the prefrontal cortex. Amphetamine-induced increases in premature responses were potentiated in animals with lesions to the prefrontal cortex, but not the nucleus accumbens shell.ConclusionsThese data suggest that noradrenaline in the nucleus accumbens shell plays an important role in the effects of atomoxetine. Under these conditions, prefrontal cortex noradrenaline did not appear to contribute to atomoxetine’s effects suggesting a lack of cortical-mediated “top-down” modulation. Noradrenaline in the prefrontal cortex appears to contribute to the modulation of impulsive responding in amphetamine-treated animals, with a loss of noradrenaline associated with potentiation of its effects. These data demonstrate a potential dissociation between cortical and sub-cortical noradrenergic mechanisms and impulse control in terms of the actions of atomoxetine and amphetamine.Electronic supplementary materialThe online version of this article (doi:10.1007/s00213-016-4458-8) contains supplementary material, which is available to authorized users.

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“…However, relationships between TH-ir and circuitry underlying alternative male reproductive behavior are unexplored. Brain CA nuclei and fiber densities are known to be regulated by steroid hormones [Wilczynski et al, 2003; LeBlanc et al, 2007; Kabelik et al, 2011; Matragrano et al, 2013; Barth et al, 2015], and forebrain dopaminergic neurons in midshipman are located in areas replete with androgen and estrogen receptors and aromatase (estrogen synthase) [Forlano et al, 2001, 2005, 2010, 2014]. Importantly, steroid hormone profiles, estrogen receptor expression, as well as aromatase activity and expression are different between male morphs [Brantley et al, 1993; Schlinger et al, 1999; Forlano and Bass, 2005; Fergus and Bass 2013], which may regulate morph differences in CA neuron number and/or their innervation patterns.…”

Section: Introductionmentioning

confidence: 99%

Catecholaminergic Fiber Innervation of the Vocal Motor System Is Intrasexually Dimorphic in a Teleost with Alternative Reproductive Tactics

Ghahramani

Timothy²,

Kaur

et al. 2015

Brain Behav Evol

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Catecholamines, which include the neurotransmitters dopamine and noradrenaline, are known modulators of sensorimotor function, reproduction, and sexually motivated behaviors across vertebrates, including vocal-acoustic communication. Recently, we demonstrated robust catecholaminergic (CA) innervation throughout the vocal motor system in the plainfin midshipman fish Porichthys notatus, a seasonal breeding marine teleost that produces vocal signals for social communication. There are 2 distinct male reproductive morphs in this species: type I males establish nests and court females with a long-duration advertisement call, while type II males sneak spawn to steal fertilizations from type I males. Like females, type II males can only produce brief, agonistic, grunt type vocalizations. Here, we tested the hypothesis that intrasexual differences in the number of CA neurons and their fiber innervation patterns throughout the vocal motor pathway may provide neural substrates underlying divergence in reproductive behavior between morphs. We employed immunofluorescence (-ir) histochemistry to measure tyrosine hydroxylase (TH; a rate-limiting enzyme in catecholamine synthesis) neuron numbers in several forebrain and hindbrain nuclei as well as TH-ir fiber innervation throughout the vocal pathway in type I and type II males collected from nests during the summer reproductive season. After controlling for differences in body size, only one group of CA neurons displayed an unequivocal difference between male morphs: the extraventricular vagal-associated TH-ir neurons, located just lateral to the dimorphic vocal motor nucleus (VMN), were significantly greater in number in type II males. In addition, type II males exhibited greater TH-ir fiber density within the VMN and greater numbers of TH-ir varicosities with putative contacts on vocal motor neurons. This strong inverse relationship between the predominant vocal morphotype and the CA innervation of vocal motor neurons suggests that catecholamines may function to inhibit vocal output in midshipman. These findings support catecholamines as direct modulators of vocal behavior, and differential CA input appears reflective of social and reproductive behavioral divergence between male midshipman morphs.

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Testosterone alters genomic responses to song and monoaminergic innervation of auditory areas in a seasonally breeding songbird

Cited by 23 publications

References 99 publications

Hormonal regulation of vasotocin receptor mRNA in a seasonally breeding songbird

Hormonal regulation of vasotocin receptor mRNA in a seasonally breeding songbird

Differential roles for cortical versus sub-cortical noradrenaline and modulation of impulsivity in the rat

Catecholaminergic Fiber Innervation of the Vocal Motor System Is Intrasexually Dimorphic in a Teleost with Alternative Reproductive Tactics

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