Estradiol induces region-specific inhibition of ZENK but does not affect the behavioral preference for tutored song in adult female zebra finches

Behavioural Brain Research

Volumn 199, Issue 2, 2009, Pages 298-306

  Svec, Lace A ^a   Wade, Juli ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Auditory perception; Estrogen; Immediate early gene; Song preference; Songbird

Indexed keywords

ESTRADIOL; ESTROGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR CONTROL; BEHAVIORAL RESEARCH; BRAIN REGION; CONTROLLED STUDY; DOPAMINERGIC SYSTEM; EXPOSURE; FEMALE; FINCH; GENE CONTROL; GENE LOCATION; GENETIC ANALYSIS; HEARING; HEARING TEST; IMMEDIATE EARLY GENE; IMMUNOREACTIVITY; NERVE CELL; NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; SOCIAL BEHAVIOR; VOCALIZATION; ZONA INCERTA;

ANIMALS; AUDITORY PERCEPTION; ESTRADIOL; FEMALE; FINCHES; GENES, IMMEDIATE-EARLY; HYPOTHALAMUS; MALE; MATING PREFERENCE, ANIMAL; SOCIAL BEHAVIOR; VOCALIZATION, ANIMAL;

EID: 61349195120     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2008.12.006     Document Type: Article

References (95)

1. Bailey D.J. Neurobiology of song learning and perception in the zebra finch (Taeniopygia guttata), with a focus on the role of the hippocampus, in Department of Psychology (2006), Michigan State University, East Lansing p. 190
2. Bailey D.J., Rosebush J.C., and Wade J. The hippocampus and caudomedial neostriatum show selective responsiveness to conspecific song in the female zebra finch. J Neurobiol 52 (2002) 43-51
3. Bailey D.J., and Wade J. Differential expression of the immediate early genes FOS and ZENK following auditory stimulation in the juvenile male and female zebra finch. Mol Brain Res 116 (2003) 147-154
4. Bailey D.J., and Wade J. FOS and ZENK responses in 45-day-old zebra finches vary with auditory stimulus and brain region, but not sex. Behav Brain Res 162 1 (2005) 108-115
5. Ballentine B., Hyman J., and Nowicki S. Vocal performance influences female response to male bird song: an experimental test. Behav Ecol 15 1 (2004) 163-168
6. Balthazart J., Gahr M., and Surlemont C. Distribution of estrogen receptors in the brain of the Japanese quail: an immunocytochemical study. Brain Res 501 2 (1989) 205-214
7. Baptista L.F., and Petrinovich L. Song development in the white-crowned sparrow-social-factors and sex-differences. Anim Behav 34 5 (1986) 1359-1371
8. Braaten R.F., and Reynolds K. Auditory preference for conspecific song in isolation-reared zebra finches. Anim Behav 58 1 (1999) 105-111
9. Buchanan K.L., and Catchpole C.K. Song as an indicator of male parental effort in the sedge warbler. Proc Biol Sci 267 1441 (2000) 321-326
10. Calhoun S., Hulse S.H., Braaten R.F., Page S.C., and Nelson R.J. Responsiveness to conspecific and alien song by canaries (Serinus canaria) and European starlings (Sturnus vulgaris) as a function of photoperiod. J Comp Psychol 107 3 (1993) 235-241
11. Cattaneo E., and Maggi A. c-fos induction by estrogen in specific rat brain areas. Eur J Pharmacol 188 2-3 (1990) 153-159
12. Cheng M., Chaiken M., Zuo M., and Miller H. Nucleus taenia of the amygdala of birds: anatomical and functional studies in ring doves (Streptopelia risoria) and European starlings (Sturnus vulgaris). Brain Behav Evol 53 5-6 (1999) 243-270
13. Cheng M.F., and Peng J.P. Reciprocal talk between the auditory thalamus and the hypothalamus: an antidromic study. Neuroreport 8 3 (1997) 653-658
14. Cheng M.F., Peng J.P., and Johnson P. Hypothalamic neurons preferentially respond to female nest coo stimulation: demonstration of direct acoustic stimulation of luteinizing hormone release. J Neurosci 18 14 (1998) 5477-5489
15. Chew S.J., Mello C.V., Nottebohm F., Jarvis E., and Vicario D.S. 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 92 8 (1995) 3406-3410
16. Clayton N. Song discrimination learning in zebra finches. Anim Behav 36 (1988) 1016-1024
17. Clayton N., and Prove E. Song discrimination in female zebra finches and Bengalese finches. Anim Behav 38 (1989) 352-362
18. Dolby A.S., Clarkson C.E., Haas E.T., Miller J.K., Havens L.E., and Cox B.K. Do song-phrase production rate and song versatility honestly communicate male parental quality in the Gray Catbird?. J Field Ornithol 76 3 (2005) 287-292
19. Domenici L., Waldvogel H.J., Matute C., and Streit P. Distribution of GABA-like immunoreactivity in the pigeon brain. Neuroscience 25 3 (1988) 931-950
20. DonCarlos L.L., Monroy E., and Morrell J.I. Distribution of estrogen receptor-immunoreactive cells in the forebrain of the female guinea pig. J Comp Neurol 305 4 (1991) 591-612
21. Durstewitz D., Kroner S., and Gunturkun O. The dopaminergic innervation of the avian telencephalon. Prog Neurobiol 59 2 (1999) 161-195
22. Gahr M., Guttinger H.R., and Kroodsma D.E. Estrogen receptors in the avian brain: survey reveals general distribution and forebrain areas unique to songbirds. J Comp Neurol 327 1 (1993) 112-122
23. Gahr M., and Metzdorf R. Distribution and dynamics in the expression of androgen and estrogen receptors in vocal control systems of songbirds. Brain Res Bull 44 4 (1997) 509-517
24. Gentner T.Q., Hulse S.H., Duffy D., and Ball G.F. Response biases in auditory forebrain regions of female songbirds following exposure to sexually relevant variation in male song. J Neurobiol 46 (2001) 48-58
25. Gibson M.J., and Cheng M.F. Neural mediation of estrogen-dependent courtship behavior in female ring doves. J Comp Physiol Psychol 93 (1979) 855-867
26. Goodson J.L., Evans A.K., Lindberg L., and Allen C.D. Neuro-evolutionary patterning of sociality. Proc Biol Sci 272 1560 (2005) 227-235
27. Granda R.H., and Crossland W.J. GABA-like immunoreactivity of neurons in the chicken diencephalon and mesencephalon. J Comp Neurol 287 4 (1989) 455-469
28. Halldin K., Axelsson J., Holmgren C., and Brunstrom B. Localization of estrogen receptor-alpha and -betamRNA in brain areas controlling sexual behavior in Japanese quail. J Neurobiol 66 2 (2006) 148-154
29. Hasselquist D., Bensch S., and von Schantz T. Correlation between male song repertoire, extra-pair paternity and offspring survival in the great reed warbler. Nature 381 (1996) 229-232
30. Heimovics S.A., and Riters L.V. Breeding-context-dependent relationships between song and cFOS labeling within social behavior brain regions in male European starlings (Sturnus vulgaris). Horm Behav 50 5 (2006) 726-735
31. Houx B.B., and ten Cate C. Do stimulus-stimulus contingencies affect song learning in zebra finches (Taeniopygia guttata)?. J Comp Psychol 113 3 (1999) 235-242
32. Houx B.B., and ten Cate C. Song learning from playback in zebra finches: is there an effect of operant contingency?. Anim Behav 57 4 (1999) 837-845
33. Insel T.R. Regional induction of c-fos-like protein in rat brain after estradiol administration. Endocrinology 126 4 (1990) 1849-1853
34. Jacobs E.C., Arnold A.P., and Campagnoni A.T. Zebra finch estrogen receptor cDNA: cloning and mRNA expression. J Steroid Biochem Mol Biol 59 2 (1996) 135-145
35. Kern M.D., and King J.R. Testosterone-induced singing in female white-crowned sparrows. Condor 74 2 (1972) 204-209
36. Koch M., and Ehret G. Immunocytochemical localization and quantitation of estrogen-binding cells in the male and female (virgin, pregnant, lactating) mouse brain. Brain Res 489 1 (1989) 101-112
37. Korenbrot C.C., Schomberg D.W., and Erickson C.J. Radioimmunoassay of plasma estradiol during the breeding cycle of ring doves (Streptopelia risoria). Endocrinology 94 (1974) 1126-1132
38. Lagrange A.H., Wagner E.J., Ronnekleiv O.K., and Kelly M.J. Estrogen rapidly attenuates a GABAB response in hypothalamic neurons. Neuroendocrinology 64 2 (1996) 114-123
39. Lauay C., Gerlach N.M., Adkins-Regan E., and DeVoogd T.J. Female zebra finches require early song exposure to prefer high-quality song as adults. Anim Behav 68 (2004) 1249-1255
40. Lauber A.H., Mobbs C.V., Muramatsu M., and Pfaff D.W. Estrogen receptor messenger RNA expression in rat hypothalamus as a function of genetic sex and estrogen dose. Endocrinology 129 6 (1991) 3180-3186
41. LeBlanc M.M., Goode C.T., MacDougall-Shackleton E.A., and Maney D.L. Estradiol modulates brainstem catecholaminergic cell groups and projections to the auditory forebrain in a female songbird. Brain Res 1171 (2007) 93-103
42. Leboucher D., Kreutzer M., and Dittami J. Copulation-solicitation displays in female canaries (Serinus canaria): are oestradiol implants necessary?. Ethology 97 (1994) 190-197
43. Leitner S., Voigt C., Garcia-Segura L.M., Van't Hof T., and Gahr M. Seasonal activation and inactivation of song motor memories in wild canaries is not reflected in neuroanatomical changes of forebrain song areas. Horm Behav 40 2 (2001) 160-168
44. Leitner S., Voigt C., Metzdorf R., and Catchpole C.K. Immediate early gene (ZENK, Arc) expression in the auditory forebrain of female canaries varies in response to male song quality. J Neurobiol 64 3 (2005) 275-284
45. Lovern M.B., and Wade J. Sex steroids in green anoles (Anolis carolinensis): uncoupled maternal plasma and yolking follicle concentrations, potential embryonic steroidogenesis, and evolutionary implications. Gen Comp Endocrinol 134 2 (2003) 109-115
46. Luine V.N., Grattan D.R., and Selmanoff M. Gonadal hormones alter hypothalamic GABA and glutamate levels. Brain Res 747 1 (1997) 165-168
47. Maney D.L., Bernard D.J., and Ball G.F. Gonadal steroid receptor mRNA in catecholaminergic nuclei of the canary brainstem. Neurosci Lett 311 3 (2001) 189-192
48. Maney D.L., Cho E., and Goode C.T. Estrogen-dependent selectivity of genomic responses to birdsong. Eur J Neurosci 23 6 (2006) 1523-1529
49. Maney D.L., Goode C.T., Lange H.S., Sanford S.E., and Solomon B.L. Estradiol modulates neural responses to song in a seasonal songbird. J Comp Neurol 511 2 (2008) 173-186
50. Maney D.L., MacDougall-Shackleton E.A., MacDougall-Shackleton S.A., Ball G.F., and Hahn T.P. Immediate early gene response to hearing song correlates with receptive behavior and depends on dialect in a female songbird. J Comp Physiol A 189 (2003) 667-674
51. Marler P., and Tamura M. Culturally transmitted patterns of vocal behavior in sparrows. Science 146 (1964) 1483-1486
52. Mello C.V., and Clayton D.F. Song-induced ZENK gene expression in auditory pathways of songbird brain and its relation to the song control system. J Neurosci 14 11 Pt 1 (1994) 6652-6666
53. Mello C.V., Vicario D.S., and Clayton D.F. Song presentation induces gene expression in the songbird forebrain. Proc Natl Acad Sci 89 (1992) 6818-6822
54. Mermelstein P.G., and Becker J.B. Increased extracellular dopamine in the nucleus accumbens and striatum of the female rat during paced copulatory behavior. Behav Neurosci 109 2 (1995) 354-365
55. Metzdorf R., Gahr M., and Fusani L. Distribution of aromatase, estrogen receptor, and androgen receptor mRNA in the forebrain of songbirds and nonsong birds. J Comp Neurol 407 1 (1999) 115-129
56. Miller D.B. The acoustic basis of mate recognition by female zebra finches (Taeniopygia guttata). Anim Behav 27 2 (1979) 376-380
57. Mitchell J.B., and Gratton A. Involvement of mesolimbic dopamine neurons in sexual behaviors: implications for the neurobiology of motivation. Rev Neurosci 5 4 (1994) 317-329
58. Nagle L., Kreutzer M.L., and Vallet E. Obtaining copulation solicitation displays in female canaries without estradiol implants. Experientia 49 (1993) 1022-1023
59. Neal J.K., and Wade J. Effects of season, testosterone and female exposure on c-fos expression in the preoptic area and amygdala of male green anoles. Brain Res 1166 (2007) 124-131
60. Neubauer R.L. Super-normal length song preferences of female zebra finches (Taeniopygia guttata) and a theory of the evolution of bird song. Evol Ecol 13 (1999) 365-380
61. Newman S.W. The medial extended amygdala in male reproductive behavior. A node in the mammalian social behavior network. Ann NY Acad Sci 877 (1999) 242-257
62. Nolan P.M., and Hill G.E. Female choice for song characteristics in the house finch. Anim Behav 67 (2004) 403-410
63. Nowicki S., Searcy W.A., and Peters S. Brain development, song learning and mate choice in birds: a review and experimental test of the "nutritional stress hypothesis". J Comp Physiol A 188 (2002) 1003-1014
64. O'Connor L.H., Nock B., and McEwen B.S. Regional specificity of gamma-aminobutyric acid receptor regulation by estradiol. Neuroendocrinology 47 6 (1988) 473-481
65. Pavlova D., Pinxten R., and Eens M. Female song in European starlings: sex differences, complexity, and composition. Condor 107 (2005) 559-569
66. Pfaff D., and Keiner M. Atlas of estradiol-concentrating cells in the central nervous system of the female rat. J Comp Neurol 151 2 (1973) 121-158
67. Pfaff D.W., Schwartz-Giblin S., McCarthy M.M., and Kow L.M. Cellular and molecular mechanisms of female reproductive behaviors. In: Knobil E., and Neill J.D. (Eds). The physiology of reproduction (1994), Raven Press, Ltd., New York 107-220
68. Pfaus J.G., Damsma G., Wenkstern D., and Fibiger H.C. Sexual activity increases dopamine transmission in the nucleus accumbens and striatum of female rats. Brain Res 693 1-2 (1995) 21-30
69. Pfaus J.G., and Heeb M.M. Implications of immediate-early gene induction in the brain following sexual stimulation of female and male rodents. Brain Res Bull 44 4 (1997) 397-407
70. Pfaus J.G., Marcangione C., Smith W.J., Manitt C., and Abillamaa H. Differential induction of Fos in the female rat brain following different amounts of vaginocervical stimulation: modulation by steroid hormones. Brain Res 741 1-2 (1996) 314-330
71. Pinaud R., and Mello C.V. GABA immunoreactivity in auditory and song control brain areas of zebra finches. J Chem Neuroanat 34 1-2 (2007) 1-21
72. Pinaud R., Velho T.A., Jeong J.K., Tremere L.A., Leao R.M., von Gersdorff H., et al. GABAergic neurons participate in the brain's response to birdsong auditory stimulation. Eur J Neurosci 20 5 (2004) 1318-1330
73. Price P. Developmental determinants of structure in zebra finch song. J Comp Physiol Psychol 93 (1979) 260-277
74. Reiner A., Perkel D.J., Bruce L.L., Butler A.B., Csillag A., Kuenzel W., et al. Revised nomenclature for avian telencephalon and some related brainstem nuclei. J Comp Neurol 473 3 (2004) 377-414
75. Riebel K., and Smallegange I.M. Does zebra finch (Taeniopygia guttata) preference for the (Familiar) father's song generalize to the songs of unfamiliar brothers. J Comp Psychol 117 1 (2003) 61-66
76. Riebel K., Smallegange I.M., Terpstra N.J., and Bolhuis J.J. Sexual equality in zebra finch song preference: evidence for a dissociation between song recognition and production learning. Proc R Soc Lond B 269 (2002) 729-733
77. Riters L.V., Eens M., Pinxten R., Duffy D.L., Balthazart J., and Ball G.F. Seasonal changes in courtship song and the medial preoptic area in male European starlings (Sturnus vulgaris). Horm Behav 38 4 (2000) 250-261
78. Riters L.V., Olesen K.M., and Auger C.J. Evidence that female endocrine state influences catecholamine responses to male courtship song in European starlings. Gen Comp Endocrinol 154 1-3 (2007) 137-149
79. Riters L.V., Teague D.P., Schroeder M.B., and Cummings S.E. Vocal production in different social contexts relates to variation in immediate early gene immunoreactivity within and outside of the song control system. Behav Brain Res 155 2 (2004) 307-318
80. Searcy W.A., and Capp M.S. Estradiol dosage and the solicitation display assay in red-winged blackbirds. Condor 99 (1997) 826-828
81. Searcy W.A., and Marler P. A test for responsiveness to song structure and programming in female sparrows. Science 213 4510 (1981) 926-928
82. Shughrue P., Scrimo P., Lane M., Askew R., and Merchenthaler I. The distribution of estrogen receptor-beta mRNA in forebrain regions of the estrogen receptor-alpha knockout mouse. Endocrinology 138 12 (1997) 5649-5652
83. Simerly R.B., Chang C., Muramatsu M., and Swanson L.W. Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study. J Comp Neurol 294 1 (1990) 76-95
84. Simmons D.A., and Yahr P. GABA and glutamate in mating-activated cells in the preoptic area and medial amygdala of male gerbils. J Comp Neurol 459 3 (2003) 290-300
85. Smith G.T., Brenowitz E.A., Wingfield J.C., and Baptista L.F. Seasonal changes in song nuclei and song behavior in Gambel's white-crowned sparrows. J Neurobiol 28 1 (1995) 114-125
86. Sockman K.W., Gentner T.Q., and Ball G.F. Complementary neural systems for the experience-dependent integration of mate-choice cues in European starlings. J Neurobiol 62 (2005) 72-81
87. Sockman K.W., and Schwabl H. Daily estradiol and progesterone levels relative to laying and onset of incubation in canaries. Gen Comp Endocrinol 114 (1999) 257-268
88. Tchernichovski O., Schwabl H., and Nottebohm F. Context determines the sex appeal of male zebra finch song. Anim Behav 55 (1998) 1003-1010
89. Tetel M.J., Getzinger M.J., and Blaustein J.D. Estradiol and progesterone influence the response of ventromedial hypothalamic neurons to tactile stimuli associated with female reproduction. Brain Res 646 2 (1994) 267-272
90. Tomaszycki M.L., and Adkins-Regan E. Experimental alteration of male song quality and output affects female mate choice and pair bond formation in zebra finches. Anim Behav 70 4 (2005) 785-794
91. Tomaszycki M.L., Sluzas E.M., Sundberg K.A., Newman S.W., and DeVoogd T.J. Immediate early gene (ZENK) responses to song in juvenile female and male zebra finches: effects of rearing environment. J Neurobiol 66 11 (2006) 1175-1182
92. Vallet E., Kreutzer M., and Gahr M. Testosterone induces sexual release quality in the song of female canaries. Ethology 102 (1996) 617-628
93. Velho T.A., Pinaud R., Rodrigues P.V., and Mello C.V. Co-induction of activity-dependent genes in songbirds. Eur J Neurosci 22 7 (2005) 1667-1678
94. Vito C.C., DeBold J.F., and Fox T.O. Androgen and estrogen receptors in adult hamster brain. Brain Res 264 1 (1983) 132-137
95. Zann R.A. The zebra finch: a synthesis of field and laboratory studies. In: Perrins C.M. (Ed). Oxford Ornithology Series (1996), Oxford University Press, New York