Estrogenic regulation of dopaminergic neurons in the opportunistically breeding zebra finch

General and Comparative Endocrinology

Volumn 173, Issue 1, 2011, Pages 96-104

  Kabelik, David ^a   Schrock, Sara E ^a   Ayres, Lauren C ^a   Goodson, James L ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

Bird; Dopamine; Estradiol; Fos; Opportunistic breeder; Zebra finch

Indexed keywords

CATECHOLAMINE; DOPAMINE; ESTROGEN; LETROZOLE; PROLACTIN; PROTEIN FOS; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BREEDING; CATECHOLAMINE SYNTHESIS; CELL COUNT; CELL MANIPULATION; CENTRAL GRAY MATTER; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; ENZYME LOCALIZATION; ESTROGEN ACTIVITY; FEMALE; FINCH; IMMUNOCOMPETENT CELL; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; TAENIOPYGIA GUTTATA; TUBER CINEREUM; VENTRAL TEGMENTUM;

EID: 80955177605     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2011.04.026     Document Type: Article

References (88)

1. Alger S.J., Maasch S.N., Riters L.V. Lesions to the medial preoptic nucleus affect immediate early gene immunolabeling in brain regions involved in song control and social behavior in male European starlings. Eur. J. Neurosci. 2009, 29:970-982.
2. Appeltants D., Absil P., Balthazart J., Ball G.F. Identification of the origin of catecholaminergic inputs to HVc in canaries by retrograde tract tracing combined with tyrosine hydroxylase immunocytochemistry. J. Chem. Neuroanat. 2000, 18:117-133.
3. Appeltants D., Ball G.F., Balthazart J. The distribution of tyrosine hydroxylase in the canary brain: demonstration of a specific and sexually dimorphic catecholaminergic innervation of the telencephalic song control nuclei. Cell Tissue Res. 2001, 304:237-259.
4. Appeltants D., Ball G.F., Balthazart J. The origin of catecholaminergic inputs to the song control nucleus RA in canaries. Neuroreport 2002, 13:649-653.
5. Aragona B.J., Wang Z. Dopamine regulation of social choice in a monogamous rodent species. Front. Behav. Neurosci. 2009, 3:15.
6. Balfour M.E., Yu L., Coolen L.M. Sexual behavior and sex-associated environmental cues activate the mesolimbic system in male rats. Neuropsychopharmacology 2004, 29:718-730.
7. Ball G.F., Balthazart J. Seasonal and hormonal modulation of neurotransmitter systems in the song control circuit. J. Chem. Neuroanat. 2010, 39:82-95.
8. Balthazart J., Absil P. Identification of catecholaminergic inputs to and outputs from aromatase-containing brain areas of the Japanese quail by tract tracing combined with tyrosine hydroxylase immunocytochemistry. J. Comp. Neurol. 1997, 382:401-428.
9. Balthazart J., Castagna C., Ball G.F. Differential effects of D1 and D2 dopamine-receptor agonists and antagonists on appetitive and consummatory aspects of male sexual behavior in Japanese quail. Physiol. Behav. 1997, 62:571-580.
10. Balthazart J., Foidart A., Baillien M., Harada N., Ball G.F. Anatomical relationships between aromatase and tyrosine hydroxylase in the quail brain: double-label immunocytochemical studies. J. Comp. Neurol. 1998, 391:214-226.
11. Barclay S.R., Harding C.F. 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. 1990, 523:251-262.
12. Batailler M., Blache D., Thibault J., Tillet Y. Immunohistochemical colocalization of tyrosine hydroxylase and estradiol receptors in the sheep arcuate nucleus. Neurosci. Lett. 1992, 146:125-130.
13. Becker J.B., Beer M.E. The influence of estrogen on nigrostriatal dopamine activity: behavioral and neurochemical evidence for both pre- and postsynaptic components. Behav. Brain Res. 1986, 19:27-33.
14. Becker J.B., Cha J.H. Estrous cycle-dependent variation in amphetamine-induced behaviors and striatal dopamine release assessed with microdialysis. Behav. Brain Res. 1989, 35:117-125.
15. Bharati I.S., Goodson J.L. Fos responses of dopamine neurons to sociosexual stimuli in male zebra finches. Neuroscience 2006, 143:661-670.
16. Björklund A., Dunnett S.B. Dopamine neuron systems in the brain: an update. Trends Neurosci. 2007, 30:194-202.
17. Bottjer S.W. The distribution of tyrosine hydroxylase immunoreactivity in the brains of male and female zebra finches. J. Neurobiol. 1993, 24:51-69.
18. Charlier T.D., Ball G.F., Balthazart J. Sexual behavior activates the expression of the immediate early genes c-fos and Zenk (egr-1) in catecholaminergic neurons of male Japanese quail. Neuroscience 2005, 131:13-30.
19. Chavez C., Hollaus M., Scarr E., Pavey G., Gogos A., van den Buuse M. The effect of estrogen on dopamine and serotonin receptor and transporter levels in the brain: an autoradiography study. Brain Res. 2010, 1321:51-59.
20. Creutz L.M., Kritzer M.F. Estrogen receptor-β immunoreactivity in the midbrain of adult rats: regional, subregional, and cellular localization in the A10, A9, and A8 dopamine cell groups. J. Comp. Neurol. 2002, 446:288-300.
21. Cynx J. Effects of humidity on reproductive behavior in male and female zebra finches (Taeniopygia guttata). J. Comp. Psychol. 2001, 115:196-200.
22. De Vries G.J., Panzica G.C. Sexual differentiation of central vasopressin and vasotocin systems in vertebrates: different mechanisms, similar endpoints. Neuroscience 2006, 138:947-955.
23. Deng Y.F., Chen X.X., Zhou Z.L., Hou J.F. Letrozole inhibits the osteogenesis of medullary bone in prelay pullets. Poult. Sci. 2010, 89:917-923.
24. Dominguez J.M., Hull E.M. Dopamine, the medial preoptic area, and male sexual behavior. Physiol. Behav. 2005, 86:356-368.
25. Du J., Hull E.M. Effects of testosterone on neuronal nitric oxide synthase and tyrosine hydroxylase. Brain Res. 1999, 836:90-98.
26. Du J., Lorrain D.S., Hull E.M. Castration decreases extracellular, but increases intracellular, dopamine in medial preoptic area of male rats. Brain Res. 1998, 782:11-17.
27. Gale S.D., Perkel D.J. Physiological properties of zebra finch ventral tegmental area and substantia nigra pars compacta neurons. J. Neurophysiol. 2006, 96:2295-2306.
28. Goodson J.L., Bass A.H. Social behavior functions and related anatomical characteristics of vasotocin/vasopressin systems in vertebrates. Brain Res. Brain Res. Rev. 2001, 35:246-265.
29. Goodson J.L., Kabelik D., Kelly A.M., Rinaldi J., Klatt J.D. Midbrain dopamine neurons reflect affiliation phenotypes in finches and are tightly coupled to courtship. Proc. Natl. Acad. Sci. USA 2009, 106:8737-8742.
30. Hahn T.P., Watts H.E., Cornelius J.M., Brazeal K.R., MacDougall-Shackleton S.A. Evolution of environmental cue response mechanisms: adaptive variation in photorefractoriness. Gen. Comp. Endocrinol. 2009, 163:193-200.
31. Heimovics S.A., Riters L.V. Evidence that dopamine within motivation and song control brain regions regulates birdsong context-dependently. Physiol. Behav. 2008, 95:258-266.
32. Huang Y.C., Hessler N.A. Social modulation during songbird courtship potentiates midbrain dopaminergic neurons. PLoS One 2008, 3:e3281.
33. Hull E.M., Du J., Lorrain D.S., Matuszewich L. Extracellular dopamine in the medial preoptic area: implications for sexual motivation and hormonal control of copulation. J. Neurosci. 1995, 15:7465-7471.
34. Ivanova T., Beyer C. Estrogen regulates tyrosine hydroxylase expression in the neonate mouse midbrain. J. Neurobiol. 2003, 54:638-647.
35. Kabelik D., Kelly A.M., Goodson J.L. Dopaminergic regulation of mate competition aggression and aromatase-Fos colocalization in vasotocin neurons. Neuropharmacology 2010, 58:862-866.
36. Kabelik D., Morrison J.A., Goodson J.L. Cryptic regulation of vasotocin neuronal activity but not anatomy by sex steroids and social stimuli in opportunistic desert finches. Brain Behav. Evol. 2010, 75:71-84.
37. Kabelik D., Weiss S.L., Moore M.C. Arginine vasotocin (AVT) immunoreactivity relates to testosterone but not territorial aggression in the tree lizard, Urosaurus ornatus. Brain Behav. Evol. 2008, 72:283-294.
38. Kil K.E., Biegon A., Ding Y.S., Fischer A., Ferrieri R.A., Kim S.W., Pareto D., Schueller M.J., Fowler J.S. Synthesis and PET studies of [(11)C-cyano]letrozole (Femara), an aromatase inhibitor drug. Nucl. Med. Biol. 2009, 36:215-223.
39. Kritzer M.F. Selective colocalization of immunoreactivity for intracellular gonadal hormone receptors and tyrosine hydroxylase in the ventral tegmental area, substantia nigra, and retrorubral fields in the rat. J. Comp. Neurol. 1997, 379:247-260.
40. Kritzer M.F., Kohama S.G. 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. 1998, 395:1-17.
41. Kuppers E., Ivanova T., Karolczak M., Beyer C. Estrogen: a multifunctional messenger to nigrostriatal dopaminergic neurons. J. Neurocytol. 2000, 29:375-385.
42. Lammel S., Hetzel A., Hackel O., Jones I., Liss B., Roeper J. Unique properties of mesoprefrontal neurons within a dual mesocorticolimbic dopamine system. Neuron 2008, 57:760-773.
43. Lansing S.W., Lonstein J.S. Tyrosine hydroxylase-synthesizing cells in the hypothalamus of prairie voles (Microtus ochrogaster): sex differences in the anteroventral periventricular preoptic area and effects of adult gonadectomy or neonatal gonadal hormones. J. Neurobiol. 2006, 66:197-204.
44. Lea R.W., Clark J.A., Tsutsui K. Changes in central steroid receptor expression, steroid synthesis, and dopaminergic activity related to the reproductive cycle of the ring dove. Microsc. Res. Tech. 2001, 55:12-26.
45. LeBlanc M.M., Goode C.T., MacDougall-Shackleton E.A., Maney D.L. Estradiol modulates brainstem catecholaminergic cell groups and projections to the auditory forebrain in a female songbird. Brain Res. 2007, 1171:93-103.
46. Lee D.W., Fernando G., Peterson R.S., Allen T.A., Schlinger B.A. Estrogen mediation of injury-induced cell birth in neuroproliferative regions of the adult zebra finch brain. Dev. Neurobiol. 2007, 67:1107-1117.
47. Lehman M.N., Durham D.M., Jansen H.T., Adrian B., Goodman R.L. Dopaminergic A14/A15 neurons are activated during estradiol negative feedback in anestrous, but not breeding season, ewes. Endocrinology 1996, 137:4443-4450.
48. Lynch K.S., Diekamp B., Ball G.F. Catecholaminergic cell groups and vocal communication in male songbirds. Physiol. Behav. 2008, 93:870-876.
49. Maney D.L., Bernard D.J., Ball G.F. Gonadal steroid receptor mRNA in catecholaminergic nuclei of the canary brainstem. Neurosci. Lett. 2001, 311:189-192.
50. Maney D.L., Cho E., Goode C.T. Estrogen-dependent selectivity of genomic responses to birdsong. Eur. J. Neurosci. 2006, 23:1523-1529.
51. Maney D.L., Goode C.T., Lange H.S., Sanford S.E., Solomon B.L. Estradiol modulates neural responses to song in a seasonal songbird. J. Comp. Neurol. 2008, 511:173-186.
52. Mello C.V., Pinaud R., Ribeiro S. Noradrenergic system of the zebra finch brain: immunocytochemical study of dopamine-beta-hydroxylase. J. Comp. Neurol. 1998, 400:207-228.
53. Miczek K.A., Fish E.W., De Bold J.F., De Almeida R.M. Social and neural determinants of aggressive behavior: pharmacotherapeutic targets at serotonin, dopamine and gamma-aminobutyric acid systems. Psychopharmacology (Berl) 2002, 163:434-458.
54. Mitchell J.B., Stewart J. Effects of castration, steroid replacement, and sexual experience on mesolimbic dopamine and sexual behaviors in the male rat. Brain Res. 1989, 491:116-127.
55. Northcutt K.V., Lonstein J.S. Social contact elicits immediate-early gene expression in dopaminergic cells of the male prairie vole extended olfactory amygdala. Neuroscience 2009, 163:9-22.
56. Numan M., Stolzenberg D.S. Medial preoptic area interactions with dopamine neural systems in the control of the onset and maintenance of maternal behavior in rats. Front. Neuroendocrinol. 2009, 30:46-64.
57. Pappas S.S., Tiernan C.T., Behrouz B., Jordan C.L., Breedlove S.M., Goudreau J.L., Lookingland K.J. Neonatal androgen-dependent sex differences in lumbar spinal cord dopamine concentrations and the number of A11 diencephalospinal dopamine neurons. J. Comp. Neurol. 2010, 518:2423-2436.
58. Pasqualini C., Olivier V., Guibert B., Frain O., Leviel V. Acute stimulatory effect of estradiol on striatal dopamine synthesis. J. Neurochem. 1995, 65:1651-1657.
59. Pawlisch B.A., Riters L.V. Selective behavioral responses to male song are affected by the dopamine agonist GBR-12909 in female European starlings (Sturnus vulgaris). Brain Res. 2010, 1353:113-124.
60. Perfito N., Zann R.A., Bentley G.E., Hau M. Opportunism at work: habitat predictability affects reproductive readiness in free-living zebra finches. Funct. Ecol. 2007, 21:291-301.
61. Putnam S.K., Du J., Sato S., Hull E.M. Testosterone restoration of copulatory behavior correlates with medial preoptic dopamine release in castrated male rats. Horm. Behav. 2001, 39:216-224.
62. Putnam S.K., Sato S., Hull E.M. Effects of testosterone metabolites on copulation and medial preoptic dopamine release in castrated male rats. Horm. Behav. 2003, 44:419-426.
63. Putnam S.K., Sato S., Riolo J.V., Hull E.M. Effects of testosterone metabolites on copulation, medial preoptic dopamine, and NOS-immunoreactivity in castrated male rats. Horm. Behav. 2005, 47:513-522.
64. Reiner A., Karle E.J., Anderson K.D., Medina L. Catecholaminergic perikarya and fibers in the avian nervous system. Phylogeny and Development of Catecholamine Systems in the CNS of Vertebrates 1994, 135-181. Cambridge University Press, Cambridge. W.J. Smeets, A. Reiner (Eds.).
65. Reiner A., Medina L., Veenman C.L. Structural and functional evolution of the basal ganglia in vertebrates. Brain Res. Brain Res. Rev. 1998, 28:235-285.
66. Renner K., Luine V. Analysis of temporal and dose-dependent effects of estrogen on monoamines in brain nuclei. Brain Res. 1986, 366:64-71.
67. Riters L.V., Olesen K.M., Auger C.J. Evidence that female endocrine state influences catecholamine responses to male courtship song in European starlings. Gen. Comp. Endocrinol. 2007, 154:137-149.
68. Rodriguiz R.M., Chu R., Caron M.G., Wetsel W.C. Aberrant responses in social interaction of dopamine transporter knockout mice. Behav. Brain Res. 2004, 148:185-198.
69. Saigusa T., Takada K., Baker S.C., Kumar R., Stephenson J.D. Dopamine efflux in the rat nucleus accumbens evoked by dopamine receptor stimulation in the entorhinal cortex is modulated by oestradiol and progesterone. Synapse 1997, 25:37-43.
70. Sar M. Estradiol is concentrated in tyrosine hydroxylase-containing neurons of the hypothalamus. Science 1984, 223:938-940.
71. Sato Y., Shibuya A., Adachi H., Kato R., Horita H., Tsukamoto T. Restoration of sexual behavior and dopaminergic neurotransmission by long term exogenous testosterone replacement in aged male rats. J. Urol. 1998, 160:1572-1575.
72. Serova L.I., Maharjan S., Huang A., Sun D., Kaley G., Sabban E.L. Response of tyrosine hydroxylase and GTP cyclohydrolase I gene expression to estrogen in brain catecholaminergic regions varies with mode of administration. Brain Res. 2004, 1015:1-8.
73. Simerly R.B. Hormonal control of the development and regulation of tyrosine hydroxylase expression within a sexually dimorphic population of dopaminergic cells in the hypothalamus. Brain Res. Mol. Brain Res. 1989, 6:297-310.
74. Soma K.K., Sullivan K., Wingfield J. Combined aromatase inhibitor and antiandrogen treatment decreases territorial aggression in a wild songbird during the nonbreeding season. Gen. Comp. Endocrinol. 1999, 115:442-453.
75. Svec L.A., Lookingland K.J., Wade J. Estradiol and song affect female zebra finch behavior independent of dopamine in the striatum. Physiol. Behav. 2009, 98:386-392.
76. Svec L.A., Wade J. Estradiol induces region-specific inhibition of ZENK but does not affect the behavioral preference for tutored song in adult female zebra finches. Behav. Brain Res. 2009, 199:298-306.
77. Thompson T.L., Moss R.L. Modulation of mesolimbic dopaminergic activity over the rat estrous cycle. Neurosci. Lett. 1997, 229:145-148.
78. Trainor B.C., Kyomen H.H., Marler C.A. Estrogenic encounters: how interactions between aromatase and the environment modulate aggression. Front. Neuroendocrinol. 2006, 27:170-179.
79. Tramontin A.D., Smith G.T., Breuner C.W., Brenowitz E.A. Seasonal plasticity and sexual dimorphism in the avian song control system: stereological measurement of neuron density and number. J. Comp. Neurol. 1998, 396:186-192.
80. Triemstra J.L., Nagatani S., Wood R.I. Chemosensory cues are essential for mating-induced dopamine release in MPOA of male Syrian hamsters. Neuropsychopharmacology 2005, 30:1436-1442.
81. Van Hartesveldt C., Joyce J.N. Effects of estrogen on the basal ganglia. Neurosci. Biobehav. Rev. 1986, 10:1-14.
82. Walters M.J., Harding C.F. The effects of an aromatization inhibitor on the reproductive behavior of male zebra finches. Horm. Behav. 1988, 22:207-218.
83. Watt M.J., Forster G.L., Korzan W.J., Renner K.J., Summers C.H. Rapid neuroendocrine responses evoked at the onset of social challenge. Physiol. Behav. 2007, 90:567-575.
84. Woolley S.C., Sakata J.T., Gupta A., Crews D. Evolutionary changes in dopaminergic modulation of courtship behavior in Cnemidophorus whiptail lizards. Horm. Behav. 2001, 40:483-489.
85. Young K.A., Liu Y., Wang Z. The neurobiology of social attachment: a comparative approach to behavioral, neuroanatomical, and neurochemical studies. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2008, 148:401-410.
86. Youngren O.M., Chaiseha Y., El Halawani M.E. Regulation of prolactin secretion by dopamine and vasoactive intestinal peptide at the level of the pituitary in the turkey. Neuroendocrinology 1998, 68:319-325.
87. Zann R.A. The Zebra Finch: A Synthesis of Field and Laboratory Studies 1996, Oxford University Press, Oxford.
88. Zsarnovszky A., Scalise T.J., Horvath T.L., Naftolin F. Estrogen effects on tyrosine hydroxylase-immunoreactive cells in the ventral mesencephalon of the female rat: further evidence for the two cell hypothesis of dopamine function. Brain Res. 2000, 868:363-366.