Testosterone alters genomic responses to song and monoaminergic innervation of auditory areas in a seasonally breeding songbird
Article first published online: 18 MAR 2013
Copyright © 2013 Wiley Periodicals, Inc.
Volume 73, Issue 6, pages 455–468, June 2013
How to Cite
Matragrano, L. L., LeBlanc, M. M., Chitrapu, A., Blanton, Z. E. and Maney, D. L. (2013), Testosterone alters genomic responses to song and monoaminergic innervation of auditory areas in a seasonally breeding songbird. Devel Neurobio, 73: 455–468. doi: 10.1002/dneu.22072
- Issue published online: 17 APR 2013
- Article first published online: 18 MAR 2013
- Accepted manuscript online: 30 JAN 2013 05:19AM EST
- Manuscript Accepted: 12 JAN 2013
- Manuscript Revised: 16 NOV 2012
- Manuscript Received: 11 SEP 2012
- NSF. Grant Number: IBN-0346984
- Center for Behavioral Neuroscience. Grant Number: IBN-9876754 (to D.L.M.)
- 2002. Noradrenergic control of auditory information processing in female canaries. Behav Brain Res 133:221–235. , , .
- 1972. Dopamine-beta-hydroxylase: Regulation of its synthesis and release from nerve terminals. Pharmacol Rev 24:233–43. .
- 1993. The catecholaminergic system of the quail brain: Immunocytochemical studies of dopamine beta-hydroxylase and tyrosine hydroxylase. J Comp Neurol 329:230–256. , .
- 1992. Immunocytochemical localization of androgen receptors in the male songbird and quail brain. J Comp Neurol 317:407–420. , , , .
- 1996. Distribution of aromatase-immunoreactive cells in the forebrain of zebra finches (Taeniopygia guttata): Implications for the neural action of steroids and nuclear definition in the avian hypothalamus. J Neurobiol 31:129–148. , , , , , .
- 1998. Distribution of androgen receptor-immunoreactive cells in the quail forebrain and their relationship with aromatase immunoreactivity. J Neurobiol 35:323–340. , , , , .
- 1990. Differential modulation of monoamine levels and turnover rates by estrogen and/or androgen in hypothalamic and vocal control nuclei of male zebra finches. Brain Res 523:251–262. , .
- 1987. Gonadal influences on spinal cord and brain monoamines in male rats. Brain Res 425:391–394. , , , .
- 1999. Androgen receptor, estrogen receptor alpha, and estrogen receptor beta show distinct patterns of expression in forebrain song control nuclei of European starlings. Endocrinology 140:4633–4643. , , , , .
- 1991. Modification of gonadectomy-induced increases in brain monoamine metabolism by steroid hormones in male and female rats. Psychoneuroendocrinology 16:547–557. , , , .
- 1993. Subordination stress: behavioral, brain, and neuroendocrine correlates. Behav Brain Res 58:113–121. , , , , .
- 1982. Dissociation of the effects of gonadal steroids on brain serotonin metabolism and sexual behavior in the male rat. Neuroendocrinology 34:38–45. , , .
- 2010. Peripheral auditory processing changes seasonally in Gambel's white-crowned sparrow. J Comp Physiol A 196: 581–599. , , .
- 2011. Differential effects of testosterone, dihydrotestosterone and estradiol on carotenoid deposition in an avian sexually selected signal. J Comp Physiol A 197:1–13. , , , , .
- 2005. A role for norepinephrine in the regulation of context-dependent ZENK expression in male zebra finches (Taeniopygia guttata). Eur J Neurosci 21:1962–1972. , .
- 2010. What birdsong can teach us about the central noradrenergic system. J Chem Neuroanat 39:96–111. , .
- 2006. Estradiol rapidly activates male sexual behavior and affects brain monoamine levels in the quail brain. Behav Brain Res 166:110–123. , , , , .
- 1992. The shell region of the nucleus ovoidalis: A subdivision of the avian auditory thalamus. J Comp Neurol 323:495–518. , , .
- 2007. Elevated testosterone and reduced 5-HIAA concentrations are associated with wounding and hantavirus infection in male Norway rats. Horm Behav 52:474–481. , , , , .
- 2000. Intermale competition in sexually mature arctic charr: effects on brain monoamines, endocrine stress responses, sex hormone levels, and behavior. Gen Comp Endocrinol 118:450–460. , , , .
- 2010. White-Throated Sparrow (Zonotrichia albicollis). In: Poole A, editor. The Birds of North America Online 128. Ithaca: Cornell Lab of Ornithology. , .
- 1988. Chronic morphine and testosterone treatment: effects on norepinephrine and serotonin metabolism and gonadotropin secretion in male rats. Brain Res 447:200–203. , , , , .
- 2001. Distribution of sex steroid hormone receptors in the avian brain: Functional implications for neural sex differences and sexual behaviors. Microsc Res Tech 55:1–11. .
- 1993. Estrogen receptors in the avian brain: Survey reveals general distribution and forebrain areas unique to songbirds. J Comp Neurol 327:112–122. , , .
- 2001. Response biases in auditory forebrain regions of female songbirds following exposure to sexually relevant variation in male song. J Neurobiol 46:48–58. , , , .
- 1998. A DNA test to sex most birds. Mol Ecol 7:1071–1075. , , ,
- 2006. Prolonged alterations in the serotonin neural system following the cessation of adolescent anabolic-androgenic steroid exposure in hamsters (Mesocricetus auratus). Behav Neurosci 120:1242–1251. , .
- 2000. Appreciating the difference between design-based and model-based sampling strategies in quantitative morphology of the nervous system. J Comp Neurol 427:333–339. .
- 2002. Effects of acute 17alpha-methyltestosterone, acute 17beta-estradiol, and chronic 17alpha-methyltestosterone on dopamine, norepinephrine and serotonin levels in the pituitary, hypothalamus and telencephalon of rainbow trout (Oncorhynchus mykiss). J Comp Physiol B 172: 659–667. , .
- 2008. The importance of titrating antibodies for immunocytochemical methods. Curr Prot Neurosci 45:12.11–12.26. , , .
- 2010. Sexually dimorphic sensory gating drives behavioral differences in túngara frogs. J Exp Biol 213:3463–3472. , , .
- 2011. Context-dependent modulation of auditory processing by serotonin. Hearing Res 279:74–84. , .
- 2004. A matter of focus: monoaminergic modulation of stimulus coding in mammalian sensory networks. Curr Opin Neurobiol 14:488–495. , , .
- 1984. Sex differences in plasma concentrations of steroids during the sensitive period for brain differentiation in the zebra finch. J Endocrinol 103:363–369. , , .
- 1991. Effects of active immunization against gonadotrophin-releasing hormone on the concentrations of noradrenaline, dopamine, 5-hydroxytryptamine and some of their metabolites in the brain and sexual organs of male rats. Neuroendocrinology 54:49–54. , , , ,
- 2011. Estrogenic regulation of dopaminergic neurons in the opportunistically breeding zebra finch. Gen Comp Endocrinol 173:96–104. , , , .
- 1996. Light and electron microscopic immunohistochemical study of dopaminergic terminals in the striatal portion of the pigeon basal ganglia using antisera against tyrosine hydroxylase and dopamine. J Comp Neurol 369:109–124. , , , .
- 1967. The organization of the ascending auditory pathway in the pigeon (Columba livia). I. Diencephalic projections of the inferior colliculus (nucleus mesencephalicus lateralis, pars dorsalis). Brain Res 6:409–427. .
- 2003. Long-term gonadectomy affects the density of tyrosine hydroxylase- but not dopamine-beta-hydroxylase-, choline acetyltransferase- or serotonin-immunoreactive axons in the medial prefrontal cortices of adult male rats. Cereb Cortex 13:282–296. .
- 1998. Ovarian hormones influence the morphology, distribution, and density of tyrosine hydroxylase immunoreactive axons in the dorsolateral prefrontal cortex of adult Rhesus monkeys. J Comp Neurol 395: 1–17. , .
- 1999. Ovarian hormones differentially influence immunoreactivity for dopamine beta-hydroxylase, choline acetyltransferase, and serotonin in the dorsolateral prefrontal cortex of adult rhesus monkeys. J Comp Neurol 409:438–451. , .
- 2007. Estradiol modulates brainstem catecholaminergic cell groups and projections to the auditory forebrain in a female songbird. Brain Res 1171:93–103. , , , .
- 2002. A comparative study of avian auditory brainstem responses: correlations with phylogeny and vocal complexity, and seasonal effects. J Comp Physiol A 188:981–992. , , , .
- 2007. Seasonal variation in avian auditory evoked responses to tones: A comparative analysis of Carolina chickadees, tufted titmice, and white-breasted nuthatches. J Comp Physiol A 193:201–215. , , , .
- 2008. Noradrenergic deficits alter processing of communication signals in female songbirds. Brain Behav Evol 72:207–214. , .
- 2008. Endocrine and genomic architecture of life history trade-offs in an avian model of social behavior. Gen Comp Endocrinol 157:275–282. .
- 2010. Hormonal control of sexual behavior in female nonmammalian vertebrates. In: Breed MD, Moore J, editors. Encyclopedia of Animal Behavior, Vol. 1. Oxford: Elsevier. pp. 697–703. .
- 2011. Neurogenomic mechanisms of aggression in songbirds. Adv Genet 75:83–119. , .
- 2011. Estradiol-dependent modulation of auditory processing and selectivity in songbirds. Front Neuroendocrinol 32:287–302. , .
- 2001. Gonadal steroid receptor mRNA in catecholaminergic nuclei of the canary brainstem. Neurosci Lett 311:189–192. , , .
- 2003. Immediate early gene response to hearing song correlates with receptive behavior and depends on dialect in a female songbird. J Comp Physiol A 189:667–674. , , , , .
- 2006. Estrogen-dependent selectivity of genomic responses to birdsong. Eur J Neurosci 23:1523–1529. , , .
- 2008. Estradiol modulates neural responses to song in a seasonal songbird. J Comp Neurol 511:173–186. , , , , .
- 2009. Behavioral phenotypes persist after gonadal steroid manipulation in white-throated sparrows. Horm Behav 55:113–120. , , , .
- 2011. Estradiol-dependent catecholaminergic innervation of auditory areas in a seasonally breeding songbird. Eur J Neurosci 34:416–425. , , , , .
- 2012a. Estradiol-dependent modulation of serotonergic markers in auditory areas of a seasonally breeding songbird. Behav Neurosci 126:110–122. , , , , , .
- 2012b. Rapid effects of hearing song on catecholaminergic activity in the songbird auditory pathway. PLoS One 7:e39388. , , , , , , .
- 1999. Serotonin transporter (SERT) mRNA and binding site densities in male rat brain affected by sex steroids. Brain Res Mol Brain Res 63:241–247. , , , .
- 2007. Steroid hormones act transsynaptically within the forebrain to regulate neuronal phenotype and song stereotypy. J Neurosci 27:12045–12057. , , , , .
- 1998. ZENK protein regulation by song in the brain of songbirds. J Comp Neurol 393:426–438. , .
- 1999. Distribution of aromatase, estrogen receptor, and androgen receptor mRNA in the forebrain of songbirds and nonsongbirds. J Comp Neurol 407:115–129. , , .
- 2007. A genotyping assay to determine plumage morph in the White-throated Sparrow (Zonotrichia albicollis). Auk 124:1330–1335. , , , .
- 2011. GnRH—A missing link between testosterone concentrations in yolk and plasma and its intergenerational effects. PLoS One 6:e22675. , , , .
- 2006. Immunodetection of the serotonin transporter protein is a more valid marker for serotonergic fibers than serotonin. Synapse 59:270–276. , , , .
- 2011. Examining a pathway for hormone mediated maternal effects—Yolk testosterone affects androgen receptor expression and endogenous testosterone production in young chicks (Gallus gallus domesticus). Gen Comp Endocrinol 172:487–493. , , , , , .
- 2011. Zenk expression in auditory regions changes with breeding condition in male Black-capped chickadees (Poecile atricapillus). Behav Brain Res 225:464–472. , , .
- 2008. A songbird forebrain area potentially involved in auditory discrimination and memory formation. J Biosci 33:145–155. , .
- 2011. Own song selectivity in the songbird auditory pathway: suppression by norepinephrine. PLoS ONE 6:e20131. , , , , , , , .
- 2004. Revised nomenclature for avian telencephalon and some related brainstem nuclei. J Comp Neurol 473:377–414. , , , , , , , et al.
- 2012. Neural sensitivity to sex steroids predicts individual differences in aggression: Implications for behavioural evolution. Proc Biol Sci 279:3547–3555. , , , , , , .
- 2010. Gonadotrophin-releasing hormone neurones in a photoperiodic songbird express Fos and Egr-1 protein after a single long day. J Neuroendocrinol 22:196–207. , , .
- 2007. Exogenous testosterone increases female aggression in the European starling (Sturnus vulgaris). Beh Ecol Sociobiol 62:255–262. .
- 2010. Topography of estradiol-modulated genomic responses in the songbird auditory forebrain. Dev Neurobiol 70:73–86. , , .
- 1992. Plasma estrogens and brain aromatase in winter White-crowned Sparrows. Ornis Scand 23:292–297. , , .
- 1988. The glucose oxidase-DAB-nickel method in peroxidase histochemistry of the nervous system. Neurosci Lett 85:169–171. , , .
- 2008. The integration of song environment by catecholaminergic systems innervating the auditory telencephalon of adult female European starlings. Dev Neurobiol 68:656–668. , .
- 2003. Brain aromatase, 5-alpha reductase, and 5-beta reductase change seasonally in wild male song sparrows: Relationship to aggressive and sexual behavior. J Neurobiol 56:209–221. , , , .
- 2006. Endocrine correlates of alternative phenotypes in the white-throated sparrow (Zonotrichia albicollis). Horm Behav 50:762–771. , , .
- 2012. Variation in the gonadotrophin-releasing hormone-1 and the song control system in the tropical breeding rufous-collared sparrow (Zonotrichia capensis) is dependent on sex and reproductive state. Gen Comp Endocrinol 178:1–7. , , , .
- 1974. The telencephalon, diencephalon, and mesencephalon of the canary, Serinus canaria, in stereotaxic coordinates. J Comp Neurol 156:337–374. , , .
- 2001. Development of song responses in the zebra finch caudomedial neostriatum: role of genomic and electrophysiological activities. J Neurobiol 48:163–180. , , .
- 1998. Testosterone as well as estrogen increases serotonin2A receptor mRNA and binding site densities in the male rat brain. Brain Res Mol Brain Res 59:205–214. , .
- 2008. Interaction of testosterone, corticosterone and corticosterone binding globulin in the white-throated sparrow (Zonotrichia albicollis). Comp Biochem Physiol A 151:226–231. , .
- 2006. Localized brain activation specific to auditory memory in a female songbird. J Comp Neurol 494:784–791. , , , ,
- 2008. The chromosomal polymorphism linked to variation in social behavior in the white-throated sparrow (Zonotrichia albicollis) is a complex rearrangement that suppresses recombination. Genetics 179:1455–1468. , , , , , , , et al.
- 1975. A cytogenetic study of the white-throated sparrow, Zonotrichia albicollis. Evolution 29:611–621. .
- 2009. Estradiol shapes auditory processing in the adult brain by regulating inhibitory transmission and plasticity-associated gene expression. J Neurosci 29:5949–5963. , , .
- 1996. Auditory pathways of caudal telencephalon and their relation to the song system of adult male zebra finches. J Comp Neurol 366:613–642. , , , .
- 2012. Noradrenergic control of gene expression and long-term neuronal adaptation evoked by learned vocalizations in songbirds. PLoS One 7:e36276. , , , , , .
- 2008. Noradrenergic neurotoxin, N-(2-chloroethyl)-N-ethyl-2-bromobenzylamine hydrochloride (DSP-4), treatment eliminates estrogenic effects on song responsiveness in female zebra finches (Taeniopygia guttata). Behav Neurosci 122:1148–1157. , , , , .
- 1958. Regulation of refractory period in the photoperiodic responses of the white-throated sparrow. J Exp Zool 139:349–379. .
- 1998. Immunohistochemical localization of serotonin transporter in normal and colchicine treated rat brain. Neurosci Res 32:305–312. , , , , , .
- 2007. Distinction of neurochemistry between the cores and their shells of auditory nuclei in tetrapod species. Brain Behav Evol 70:1–20. , , , .