Behavioral effects of brain-derived estrogens in birds

Annals of the New York Academy of Sciences

Volumn 1163, Issue , 2009, Pages 31-48

  Balthazart, Jacques ^a   Taziaux, Melanie ^a   Holloway, Kevin ^b   Ball, Gregory F ^c   Cornil, Charlotte A ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b VASSAR COLLEGE   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Appetitive sexual behavior; Aromatase; Cloacal gland sphincter; Copulatory behavior; Estrogens; Japanese quail; Medial preoptic area; Nongenomic effects; Sexual learning; Steroids

Indexed keywords

AROMATASE; CALCIUM; ESTROGEN DERIVATIVE; ESTROGEN RECEPTOR; TESTOSTERONE;

APPETITE; AROMATIZATION; BEHAVIOR CHANGE; BIRD; CALCIUM CELL LEVEL; CLOACA; COITUS; CONFERENCE PAPER; DOWN REGULATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENETIC TRANSCRIPTION; GENOMICS; HORMONAL REGULATION; HORMONE ACTION; MUSCLE CONTRACTION; NEUROTRANSMISSION; NONHUMAN; QUAIL; SEXUAL BEHAVIOR; SPHINCTER; UPREGULATION;

AVES; COTURNIX JAPONICA; PHASIANIDAE; RODENTIA; VERTEBRATA;

EID: 65449142495     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1111/j.1749-6632.2008.03637.x     Document Type: Conference Paper

References (94)

1. Beach, F.A. 1948. Hormones and Behavior. Paul B. Hoeber, Inc. New York.
2. Beyer, C. et al. 1976. Effect of some antiestrogens and aromatase inhibitors on androgen-induced sexual behavior in castrated male rats. Horm. Behav. 7 : 353 363. (Pubitemid 8021077)
3. MacLusky, N.J. F. Naftolin. 1981. Sexual differentiation of the central nervous system. Science 211 : 1294 1303.
4. Balthazart, J. 1989. Steroid metabolism and the activation of social behavior. In Advances in Comparative and Environmental Physiology, Vol. 3. J. Balthazart, Ed. : 105 159. Springer Verlag. Berlin.
5. Naftolin, F., K.J. Ryan Z. Petro. 1972. Aromatization of androstenedione by the anterior hypothalamus of adult male and female rats. Endocrinology 90 : 295 298.
6. Naftolin, F. et al. 1975. The formation of estrogens by central neuroendocrine tissues. Rec. Prog. Horm. Res. 31 : 295 319.
7. Steimer, T. J.B. Hutchison. 1981. Androgen increases formation of behaviourally effective oestrogen in dove brain. Nature 292 : 345 347. (Pubitemid 11050337)
8. Schumacher, M. J. Balthazart. 1986. Testosterone-induced brain aromatase is sexually dimorphic. Brain Res 370 : 285 293. (Pubitemid 16055068)
9. Roselli, C.E. J.A. Resko. 1984. Androgens regulate brain aromatase activity in adult male rats through a receptor mechanism. Endocrinology 114 : 2183 2189. (Pubitemid 14120272)
10. Ball, G.F. J. Balthazart. 2002. Neuroendocrine mechanisms regulating reproductive cycles and reproductive behavior in birds. In Hormones, Brain and Behavior, Vol. 2. D.W. Pfaff, et al., Eds. : 649 798. Academic Press. San Diego.
11. Lisk, R.D. 1962. Diencephalic placement of estradiol and sexual receptivity in the female rat. Am. J. Physiol. 203 : 493 496.
12. Hutchison, J.B. 1978. Hypothalamic regulation of male sexual responsiveness to androgen. In Biological Determinants of Sexual Behaviour. J.B. Hutchison, Ed. : 277 319. John Wiley. Chichester.
13. Balthazart, J. G.F. Ball. 2007. Topography in the preoptic region: differential regulation of appetitive and consummatory male sexual behaviors. Front. Neuroendocrinol. 28 : 161 178. (Pubitemid 47404635)
14. Watson, J.T. E. Adkins-Regan. 1989. Activation of sexual behavior by implantation of testosterone propionate and estradiol benzoate into the preoptic area of the male Japanese quail (Coturnix japonica). Horm. Behav. 23 : 251 268. (Pubitemid 19147106)
15. Panzica, G.C. et al. 1987. Sexual differentiation and hormonal control of the sexually dimorphic preoptic medial nucleus in quail. Brain Res. 416 : 59 68. (Pubitemid 17102247)
16. Balthazart, J. C. Surlemont. 1990. Copulatory behavior is controlled by the sexually dimorphic nucleus of the quail POA. Brain Res. Bull. 25 : 7 14. (Pubitemid 20246608)
17. Balthazart, J., C. Surlemont N. Harada. 1992. Aromatase as a cellular marker of testosterone action in the preoptic area. Physiol. Behav. 51 : 395 409.
18. Balthazart, J. C. Surlemont. 1990. Androgen and estrogen action in the preoptic area and activation of copulatory behavior in quail. Physiol. Behav. 48 : 599 609.
19. Watson, J.T. E. Adkins-Regan. 1989. Testosterone implanted in the preoptic area of male Japanese quail must be aromatized to activate copulation. Horm. Behav. 23 : 432 447. (Pubitemid 19229836)
20. Balthazart, J., L. Evrard C. Surlemont. 1990. Effects of the non-steroidal aromatase inhibitor, R76713 on testosterone-induced sexual behavior in the Japanese quail (Coturnix coturnix japonica). Horm. Behav. 24 : 510 531.
21. Timberlake, W. K.M. Silva. 1995. Appetitive behavior in ethology, psychology, and behavior systems. In Perspectives in Ethology, Volume 11: Behavioral Design. N.S. Thompson, Ed. : 211 253. Plenum Press. New York.
22. Beach, F.A. 1956. Characteristics of masculine "sex drive". Nebraska Symposium on Motivation 4 : 1 32.
23. Ball, G.F. J. Balthazart. 2008. How useful is the appetitive and consummatory distinction for our understanding of the neuroendocrine control of sexual behavior? Horm. Behav. 53 : 307 311.
24. Sachs, B.D. 2008. The appetitive-consummatory distinction: is this 100-year-old baby worth saving? Reply to Ball and Balthazart. Horm. Behav. 53 : 315 318.
25. Everitt, B.J. 1990. Sexual motivation: a neural and behavioural analysis of the mechanisms underlying appetitive and copulatory responses in male rats. Neurosci. Biobehav. Rev. 14 : 217 232. (Pubitemid 20159558)
26. Everitt, B.J. 1995. Neuroendocrine mechanisms underlying appetitive and consummatory elements of masculine sexual behavior. In The Pharmacology of Sexual Function and Dysfunction. J. Bancroft, Ed. : 15 31. Elsevier. Amsterdam.
27. Domjan, M. K.L. Hollis. 1988. Reproductive behavior: a potential model system for adaptative specializations in learning. In Evolution and Learning. R.C. Bolles & M.D. Beecher, Eds. : 213 237. Lawrence Erlbaum. Hillsdale, NJ.
28. Domjan, M. S. Hall. 1986. Determinants of social proximity in Japanese quail (Coturnix coturnix japonica): male behavior. J. Comp. Psychol. 100 : 59 67.
29. Domjan, M. S. Hall. 1986. Sexual dimorphism in the social proximity behavior of Japanese quail (Coturnix coturnix japonica). J. Comp. Psychol. 100 : 68 71.
30. Domjan, M. 1987. Photoperiodic and endocrine control of social proximity behavior in male Japanese quail (Coturnix coturnix japonica). Behav. Neurosci. 101 : 385 392.
31. Balthazart, J. G.F. Ball. 1998. The Japanese quail as a model system for the investigation of steroid-catecholamine interactions mediating appetitive and consummatory aspects of male sexual behavior. Ann. Rev. Sex Res. 9 : 96 176.
32. Balthazart, J. et al. 1995. Appetitive as well as consummatory aspects of male sexual behavior in quail are activated by androgens and estrogens. Behav. Neurosci. 109 : 485 501.
33. Balthazart, J., C. Castagna G.F. Ball. 1997. Aromatase inhibition blocks the activation and sexual differentiation of appetitive male sexual behavior in Japanese quail. Behav. Neurosci. 111 : 381 397. (Pubitemid 27169328)
34. Holloway, K.S. M. Domjan. 1993. Sexual approach conditioning: tests of unconditional stimulus devaluation using hormone manipulations. J. Exp. Psychol. 19 : 47 55.
35. Thompson, R.R. et al. 1998. Role of the archistriatal nucleus taeniae in the sexual behavior of male Japanese quail (Coturnix japonica): a comparison of function with the medial nucleus of the amygdala in mammals. Brain Behav. Evol. 51 : 215 229. (Pubitemid 128469688)
36. Seiwert, C.M. E. Adkins-Regan. 1998. The foam production system of the male Japanese quail: characterization of structure and function. Brain Behav. Evol. 52 : 61 80. (Pubitemid 128469184)
37. Cheng, K.M., A.R. Hickman C.R. Nichols. 1989. Role of the proctodeal gland foam of male Japanese quail in natural copulations. The Auk 106 : 279 285.
38. Birkhead, T.R. F. Fletcher. 1994. Sperm storage and the release of sperm from the sperm storage tubules in Japanese quail. Ibis 136 : 101 105. (Pubitemid 2036387)
39. Doi, O. et al. 1980. Changes in the pituitary and plasma LH, plasma and follicular progesterone, and estradiol, and plasma testosterone and estrone concentrations during the ovulatory cycle of the quail (Coturnix coturnix japonica). Gen. Comp. Endocrinol. 41 : 156 163.
40. Delville, Y., J. Sulon J. Balthazart. 1986. Diurnal variations of sexual receptivity in the the female Japanese quail. Horm. Behav. 20 : 13 33.
41. Adkins-Regan, E. 1999. Foam produced by male Coturnix quail: what is its function? The Auk 116 : 184 193. (Pubitemid 29060286)
42. Sachs, B.D. 1967. Photoperiodic control of the cloacal gland of the Japanese quail. Science 157 : 201 203.
43. Balthazart, J. et al. 1998. Appetitive and consummatory male sexual behavior in Japanese quail are differentially regulated by subregions of the preoptic medial nucleus. J. Neurosci. 18 : 6512 6527. (Pubitemid 28373253)
44. Taziaux, M., C.A. Cornil J. Balthazart. 2004. Aromatase inhibition blocks the expression of sexually-motivated cloacal gland movements in male quail. Behav. Processes 67 : 461 469. (Pubitemid 39420152)
45. Adkins-Regan, E. E.A. MacKillop. 2003. Japanese quail (Coturnix japonica) inseminations are more likely to fertilize eggs in a context predicting mating opportunities. Proc. Biol. Sci. 270 : 1685 1689. (Pubitemid 37041288)
46. Holloway, K.S., J. Balthazart C.A. Cornil. 2005. Androgen mediation of conditioned rhythmic cloacal sphincter movements in Japanse quail (Coturnix japonica). J. Comp. Psychol. 119 : 49 57. (Pubitemid 40390353)
47. Cornil, C.A. et al. 2004. The effects of aromatase inhibition on testosterone-dependent conditioned rhythmic cloacal sphincter movements in male Japanese quail. Physiol. Behav. 83 : 99 105. (Pubitemid 39387698)
48. Foidart, A. et al. 1995. Critical re-examination of the distribution of aromatase-immunoreactive cells in the quail forebrain using antibodies raised against human placental aromatase and against the recombinant quail, mouse or human enzyme. J. Chem. Neuroanat. 8 : 267 282. (Pubitemid 124019971)
49. Balthazart, J. G.F. Ball. 1998. New insights into the regulation and function of brain estrogen synthase (aromatase). Trends Neurosci. 21 : 243 249. (Pubitemid 28239981)
50. Balthazart, J. et al. 2004. Preoptic aromatase modulates male sexual behavior: slow and fast mechanisms of action. Physiol Behav. 83 : 247 270. (Pubitemid 39361569)
51. Naftolin, F., T.L. Horvath J. Balthazart. 2001. Estrogen synthetase (aromatase) immunohistochemistry reveals concordance between avian and rodent limbic systems and hypothalami. Proc. Soc. Exp. Biol. Med. 226 : 717 725. (Pubitemid 32785966)
52. Abdelgadir, S.E. et al. 1994. Androgens regulate aromatase cytochrome P450 messenger ribonucleic acid in rat brain. Endocrinology 135 : 395 401. (Pubitemid 24203843)
53. Balthazart, J. A. Foidart. 1993. Brain aromatase and the control of male sexual behavior. J. Steroid Biochem. Mol. Biol. 44 : 521 540. (Pubitemid 23126623)
54. Balthazart, J. et al. 2008. Estradiol, a key endocrine signal in the sexual diferentiation and activation of reproductive behavior in quail. J. Exp. Zool Pt. A, Ecol. Genetics and Physiol. 309A. Epub ahead of print.
55. Roselli, C.E., L.E. Horton J.A. Resko. 1987. Time-course and steroid specificity of aromatase induction in rat hypothalamus-preoptic area. Biol. Reprod. 37 : 628 633.
56. Hutchison, J.B. T.H. Steimer. 1986. Formation of behaviorally effective 17beta-estradiol in the dove brain: steroid control of preoptic aromatase. Endocrinology 118 : 2180 2187. (Pubitemid 16058381)
57. Harada, N. et al. 1993. Synergism between androgens and estrogens in the induction of aromatase and its messenger RNA in the brain. Brain Res. 622 : 243 256. (Pubitemid 23264971)
58. Absil, P. et al. 2001. The control of preoptic aromatase activity by afferent inputs in Japanese quail. Brain Res. Rev. 37 : 38 58. (Pubitemid 34023592)
59. Albert, K.A. et al. 1984. Calcium/phospholipid-dependent protein kinase (protein kinase C) phosphorylates and activates tyrosine hydroxylase. Proc. Natl. Acad. Sci. USA 81 : 7713 7717. (Pubitemid 15169131)
60. Daubner, S.C. et al. 1992. Site-directed mutagenesis of serine 40 of rat tyrosine hydroxylase. J. Biol. Chem. 267 : 12639 12646. (Pubitemid 23013973)
61. Onagbesan, O.M. M.J. Podie. 1989. Calcium-dependent stimulation of estrogen secretion by FSH from theca cells of the domestic hen (Gallus domesticus). Gen. Comp. Endocrinol. 75 : 177 186. (Pubitemid 19199725)
62. Hochberg, Z. et al. 1986. The dual effect of calcium on aromatization by cultured human trophoblast. J. Steroid Biochem. 24 : 1217 1219.
63. Steimer, T. J.B. Hutchison. 1991. Micromethods for the in vitro study of steroid metabolism in the brain using radiolabelled tracers. In Neuroendocrine Research Methods, Vol. 2. B. Greenstein, Ed. : 875 919. Harwood Academic Publishers. Chur, Switzerland.
64. Ames, M.M., P. Lerner W. Lovenberg. 1978. Tyrosine hydroxylase: activation by protein phosphorylation and end product inhibition. J. Biol. Chem. 253 : 27 31.
65. Balthazart, J., M. Baillien G.F. Ball. 2001. Rapid and reversible inhibition of brain aromatase activity. J. Neuroendocrinol. 13 : 61 71. (Pubitemid 32046821)
66. Balthazart, J. et al. 2003. Calcium-dependent phosphorylation processes control brain aromatase in quail. Eur. J. Neurosci. 17 : 1591 1606. (Pubitemid 36628128)
67. Corbin, C.J. et al. 1988. Isolation of a full-length cDNA insert encoding human aromatase system cytochrome P-450 and its expression in nonsteroidogenic cells. Proc. Natl. Acad. Sci. USA 85 : 8948 8952. (Pubitemid 19001822)
68. Harada, N. 1988. Cloning of a complete cDNA encoding human aromatase: immunochemical identification and sequence analysis. Biochem. Biophys. Res. Commun. 156 : 725 732. (Pubitemid 18263890)
69. Shen, P. et al. 1994. Isolation and characterization of a zebra finch aromatase cDNA: in situ hybridization reveals high aromatase expression in brain. Mol. Brain Res. 24 : 227 237. (Pubitemid 24202860)
70. Harada, N. 1988. Novel properties of human placental aromatase as cytochrome P-450: purification and characterization of a unique form of aromatase. J. Biochem. 103 : 106 113. (Pubitemid 18031248)
71. McPhaul, M.J. et al. 1988. The expression of a functional cDNA encoding the chicken cytochrome P-450arom (aromatase) that catalyzes the formation of estrogen from androgen. J. Biol. Chem. 263 : 16358 16363. (Pubitemid 18262057)
72. Means, G.D. et al. 1989. Structural analysis of the gene encoding human aromatase cytochrome P-450, the enzyme responsible for estrogen biosynthesis. J. Biol. Chem. 264 : 19385 19391. (Pubitemid 19285850)
73. Balthazart, J., M. Baillien G.F. Ball. 2006. Rapid control of brain aromatase activity by glutamatergic inputs. Endocrinology 147 : 359 366. (Pubitemid 43004289)
74. Cornil, C.A. et al. 2005. Rapid decreases in preoptic aromatase activity and brain monoamine concentrations after engaging in male sexual behavior. Endocrinology 146 : 3809 3820. (Pubitemid 41175749)
75. Balthazart, J., A. Foidart J.C. Hendrick. 1990. The induction by testosterone of aromatase activity in the preoptic area and activation of copulatory behavior. Physiol. Behav. 47 : 83 94. (Pubitemid 20049451)
76. Balthazart, J. et al. 2005. Effects of calmodulin on aromatase activity in the preoptic area. J. Neuroendocrinol. 17 : 664 671. (Pubitemid 41341644)
77. Adkins, E.K. B.L. Nock. 1976. The effects of the antiestrogen CI-628 on sexual behavior activated by androgen and estrogen in quail. Horm. Behav. 7 : 417 429. (Pubitemid 8021081)
78. Schlinger, B.A. G. V. Callard. 1989. Localization of aromatase in synaptosomal and microsomal subfractions of quail (Coturnix coturnix japonica) brain. Neuroendocrinology 49 : 434 441. (Pubitemid 19111288)
79. Naftolin, F. et al. 1996. Aromatase immunoreactivity in axon terminals of the vertebrate brain - an immunocytochemical study on quail, rat, monkey and human tissues. Neuroendocrinology 63 : 149 155. (Pubitemid 26049626)
80. Cross, E. C.E. Roselli. 1999. 17beta-estradiol rapidly facilitates chemoinvestigation and mounting in castrated male rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 276 : R1346 R1350. (Pubitemid 29249658)
81. Cornil, C.A., G.F. Ball J. Balthazart. 2006. Functional significance of the rapid regulation of brain estrogen action: where do the estrogens come from? Brain Res. 1126 : 2 26.
82. Balthazart, J. G.F. Ball. 2006. Is brain estradiol a hormone or a neurotransmitter? Trends Neurosci. 29 : 241 249.
83. De Coster, R. et al. 1990. New non-steroidal aromatase inhibitors: focus on R76713. J. Steroid Biochem. 37 : 335 341.
84. Cornil, C.A. et al. 2006. Rapid effects of aromatase inhibition on male reproductive behaviors in Japanese quail. Horm. Behav. 49 : 45 67. (Pubitemid 41821870)
85. Cornil, C.A. et al. 2006. Estradiol rapidly activates male sexual behavior and affects brain monoamine levels in the quail brain. Behav. Brain Res. 166 : 110 123. (Pubitemid 41677367)
86. Kow, L.-M. D.W. Pfaff. 2004. The membrane actions of estrogens can potentiate their lordosis behavior-facilitating genomic actions. PNAS 101 : 12354 12357. (Pubitemid 39145447)
87. Vasudevan, N. D.W. Pfaff. 2008. Non-genomic actions of estrogens and their interaction with genomic actions in the brain. Front. Neuroendocrinol. 29 : 238 257.
88. Evrard, H.C. J. Balthazart. 2004. Rapid regulation of pain by estrogens synthesized in spinal dorsal horn neurons. J. Neurosci. 24 : 7225 7229. (Pubitemid 39100692)
89. Taziaux, M. et al. 2007. Sexual behavior activity tracks rapid changes in brain estrogen concentrations. J. Neurosci. 27 : 6563 6572. (Pubitemid 46920383)
90. Remage-Healey, L. A.H. Bass. 2004. Rapid, hierarchical modulation of vocal patterning by steroid hormones. J. Neurosci. 24 : 5892 5900. (Pubitemid 38859386)
91. Ball, G.F. J. Balthazart. 2004. Hormonal regulation of brain circuits mediating male sexual behavior in birds. Physiol. Behav. 83 : 329 346. (Pubitemid 39366014)
92. Spencer, J.L. et al. 2008. Uncovering the mechanisms of estrogen effects on hippocampal function. Front. Neuroendocrinol. 29 : 219 237.
93. Woolley, C.S. 2007. Acute effects of estrogen on neuronal physiology. Annu. Rev. Pharmacol. Toxicol. 47 : 657 680. (Pubitemid 46272142)
94. Qiu, J., O.K. Ronnekleiv M.J. Kelly. 2008. Modulation of hypothalamic neuronal activity through a novel G-protein-coupled estrogen membrane receptor. Steroids 73 : 985 991.