Brain estrogens rapidly strengthen auditory encoding and guide song preference in a songbird

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 8, 2010, Pages 3852-3857

  Remage Healey, Luke ^a   Coleman, Melissa J ^b   Oyama, Randi K ^a   Schlinger, Barney A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b KECK GRADUATE INSTITUTE   (United States)

Author keywords

Birdsong; Microdialysis; Neurotransmission; Nongenomic; Sex steroid

Indexed keywords

ESTRADIOL;

ACOUSTIC NERVE FIBER; ANIMAL BEHAVIOR; ARTICLE; AUDITORY STIMULATION; BRAIN CORTEX; BRAIN REGION; ESTROGEN SYNTHESIS; EVOKED AUDITORY RESPONSE; IN VIVO STUDY; MALE; NEUROMODULATION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SONGBIRD; SOUND TRANSMISSION;

ACOUSTIC STIMULATION; ANIMALS; AROMATASE; AUDITORY PERCEPTION; BRAIN; COGNITION; ESTROGENS; FINCHES; MALE; VOCALIZATION, ANIMAL;

PASSERI; VERTEBRATA;

EID: 77649257390     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0906572107     Document Type: Article

References (44)

1. Woolley CS (2007) Acute effects of estrogen on neuronal physiology. Annu Rev Pharmacol Toxicol 47:657-680.
2. Remage-Healey L, Bass AH (2006) A rapid neuromodulatory role for steroid hormones in the control of reproductive behavior. Brain Res 1126:27-35.
3. Balthazart J, Ball GF (2006) Is brain estradiol a hormone or a neurotransmitter? Trends Neurosci 29:241-249.
4. Gobes SMH, Bolhuis JJ (2007) Birdsong memory: A neural dissociation between song recognition and production. Curr Biol 17:789-793.
5. Holveck MJ, Riebel K (2007) Preferred songs predict preferred males: Consistency and repeatability of zebra finch females across three test contexts. Anim Behav 74:297-309.
6. Peterson RS, Yarram L, Schlinger BA, Saldanha CJ (2005) Aromatase is pre-synaptic and sexually dimorphic in the adult zebra finch brain. Proc Biol Sci 272:2089-2096.
7. Garcia-Segura LM (2008) Aromatase in the brain: Not just for reproduction anymore. J Neuroendocrinol 20:705-712.
8. Bolhuis JJ, Gahr M (2006) Neural mechanisms of birdsong memory. Nat Rev Neurosci 7:347-357.
9. London SE, Clayton DF (2008) Functional identification of sensory mechanisms required for developmental song learning. Nat Neurosci 11:579-586.
10. Terleph TA, Lu K, Vicario DS (2008) Response properties of the auditory telencephalon in songbirds change with recent experience and season. PLoS One 3:e2854.
11. Gentner TQ, Margoliash D (2003) Neuronal populations and single cells representing learned auditory objects. Nature 424:669-674.
12. Saldanha CJ, et al. (2000) Distribution and regulation of telencephalic aromatase expression in the zebra finch revealed with a specific antibody. J Comp Neurol 423:619-630.
13. Remage-Healey L, Maidment NT, Schlinger BA (2008) Forebrain steroid levels fluctuate rapidly during social interactions. Nat Neurosci 11:1327-1334.
14. Freking F, Ramachandran B, Schlinger BA (1998) Regulation of aromatase, 5 alpha- and 5 beta-reductase in primary cell cultures of developing zebra finch telencephalon. J Neurobiol 36:30-40.
15. Cynx J, Williams H, Nottebohm F (1992) Hemispheric differences in avian song discrimination. Proc Natl Acad Sci USA 89:1372-1375.
16. Voss HU, et al. (2007) Functional MRI of the zebra finch brain during song stimulation suggests a lateralized response topography. Proc Natl Acad Sci USA 104:10667-10672.
17. Weis S, et al. (2008) Estradiol modulates functional brain organization during the menstrual cycle: An analysis of interhemispheric inhibition. J Neurosci 28:13401-13410.
18. Hausmann M, Güntürkün O (2000) Steroid fluctuations modify functional cerebral asymmetries: The hypothesis of progesterone-mediated interhemispheric decoupling. Neuropsychologia 38:1362-1374.
19. Halpern ME, Güntürkün O, Hopkins WD, Rogers LJ (2005) Lateralization of the vertebrate brain: Taking the side of model systems. J Neurosci 25:10351-10357.
20. Krahe R, Gabbiani F (2004) Burst firing in sensory systems. Nat Rev Neurosci 5:13-23.
21. Tremere LA, Jeong JK, Pinaud R (2009) Estradiol shapes auditory processing in the adult brain by regulating inhibitory transmission and plasticity-associated gene expression. J Neurosci 29:5949-5963.
22. Yu AC, Margoliash D (1996) Temporal hierarchical control of singing in birds. Science 273:1871-1875.
23. Steriade M, McCormick DA, Sejnowski TJ (1993) Thalamocortical oscillations in the sleeping and aroused brain. Science 262:679-685.
24. Lewicki MS, Konishi M (1995) Mechanisms underlying the sensitivity of songbird forebrain neurons to temporal order. Proc Natl Acad Sci USA 92:5582-5586.
25. Kao MH, Wright BD, Doupe AJ (2008) Neurons in a forebrain nucleus required for vocal plasticity rapidly switch between precise firing and variable bursting depending on social context. J Neurosci 28:13232-13247.
26. Hahnloser RHR, Kozhevnikov AA, Fee MS (2002) An ultra-sparse code underlies the generation of neural sequences in a songbird. Nature 419:65-70.
27. Hahnloser RHR, Wang CZH, Nager A, Naie K (2008) Spikes and bursts in two types of thalamic projection neurons differentially shape sleep patterns and auditory responses in a songbird. J Neurosci 28:5040-5052.
28. Sherman SM (2001) Tonic and burst firing: Dual modes of thalamocortical relay. Trends Neurosci 24:122-126.
29. Remy S, Spruston N (2007) Dendritic spikes induce single-burst long-term potentiation. Proc Natl Acad Sci USA 104:17192-17197.
30. Wozny C, Maier N, Schmitz D, Behr J (2008) Two different forms of long-term potentiation at CA1-subiculum synapses. J Physiol 586:2725-2734.
31. Sarter M, Parikh V, Howe WM (2009) Phasic acetylcholine release and the volume transmission hypothesis: Time to move on. Nat Rev Neurosci 10:383-390.
32. Marder E, Bucher D (2007) Understanding circuit dynamics using the stomatogastric nervous system of lobsters and crabs. Annu Rev Physiol 69:291-316.
33. Eberling JL, Wu C, Tong-Turnbeaugh R, Jagust WJ (2004) Estrogen- and tamoxifenassociated effects on brain structure and function. Neuroimage 21:364-371.
34. Bender CM, et al. (2006) Cognitive impairment associated with adjuvant therapy in breast cancer. Psychooncology 15:422-430.
35. Jenkins V, Shilling V, Fallowfield L, Howell A, Hutton S (2004) Does hormone therapy for the treatment of breast cancer have a detrimental effect on memory and cognition? A pilot study. Psychooncology 13:61-66.
36. Riebel K, Smallegange IM (2003) Does zebra finch (Taeniopygia guttata) preference for the (familiar) father's song generalize to the songs of unfamiliar brothers? J Comp Psychol 117:61-66.
37. 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 Biol Sci 269:729-733.
38. Zann RA (1996) The Zebra Finch (Oxford Univ Press, New York).
39. Wade J, Schlinger BA, Hodges L, Arnold AP (1994) Fadrozole: A potent and specific inhibitor of aromatase in the zebra finch brain. Gen Comp Endocrinol 94:53-61.
40. 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 two periods of protein synthesis in the songbird forebrain. Proc Natl Acad Sci USA 92:3406-3410.
41. Vockel A, Pröve E, Balthazart J (1990) Effects of castration and testosterone treatment on the activity of testosterone-metabolizing enzymes in the brain of male and female zebra finches. J Neurobiol 21:808-825.
42. Coleman MJ, Mooney R (2004) Synaptic transformations underlying highly selective auditory representations of learned birdsong. J Neurosci 24:7251-7265.
43. Coleman MJ, Roy A, Wild JM, Mooney R (2007) Thalamic gating of auditory responses in telencephalic song control nuclei. J Neurosci 27:10024-10036.
44. Bauer EE, et al. (2008) A synaptic basis for auditory-vocal integration in the songbird. J Neurosci 28:1509-1522.