Sex differences in projections from preoptic area aromatase cells to the periaqueductal gray in Japanese quail

Journal of Comparative Neurology

Volumn 500, Issue 5, 2007, Pages 894-907

  Carere, Claudio ^a   Ball, Gregory F ^b   Balthazart, Jacques ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Medial preoptic nucleus; Mesencephalic central gray; Retrograde tracing; Sexual behavior; Sexual differentiation

Indexed keywords

AROMATASE; ESTRADIOL; MICROSPHERE; TESTOSTERONE; TRACER;

ANIMAL EXPERIMENT; ANIMAL TISSUE; AROMATIZATION; ARTICLE; COITUS; CONTROLLED STUDY; COTURNIX; COTURNIX JAPONICA; FEMALE; HORMONE RESPONSE; IMMUNOCYTOCHEMISTRY; MALE; MEDIAL PREOPTIC AREA; NERVE PROJECTION; NONHUMAN; PERIAQUEDUCTAL GRAY MATTER; PREMOTOR CORTEX; PREOPTIC AREA; PRIORITY JOURNAL; SENSORIMOTOR INTEGRATION; SENSORY NERVE; SEX DIFFERENCE; SEXUAL BEHAVIOR;

ANALYSIS OF VARIANCE; ANIMALS; COPULATION; COTURNIX; FEMALE; MALE; NEURAL PATHWAYS; PERIAQUEDUCTAL GRAY; PREOPTIC AREA; SEX CHARACTERISTICS; TESTOSTERONE;

EID: 33846343538     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21210     Document Type: Article

References (70)

1. Abercrombie M. 1946. Estimation of nuclear population from microtome sections. Anat Rec 94:239-247.
2. Absil P, Riters LV, Balthazart J. 2001. Preoptic aromatase cells project to the mesencephalic central gray in the male Japanese quail (Coturnix japonica). Horm Behav 40:369-383.
3. Adkins EK. 1975. Hormonal basis of sexual differentiation in the Japanese quail. J Comp Physiol Psychol 89:61-71.
4. Adkins EK, Adler NT. 1972. Hormonal control of behavior in the Japanese quail. J Comp Physiol Psychol 81:27-36.
5. Aste N, Panzica GC, Aimar P, Viglietti-Panzica C, Harada N, Foidart A, Balthazart J. 1994. Morphometric studies demonstrate that aromatase- immunoreactive cells are the main target of androgens and estrogens in the quail medial preoptic nucleus. Exp Brain Res 101:241-252.
6. Aste N, Panzica GC, Viglietti-Panzica C, Harada N, Balthazart J. 1998. Distribution and effects of testosterone on aromatase mRNA in the quail forebrain: a non-radioactive in situ hybridization study. J Chem Neuroanat 14:103-115.
7. Ball GF, Balthazart J. 2004. Hormonal regulation of brain circuits mediating male sexual behavior in birds. Physiol Behav 83:323-346.
8. Ball GF, MacDougall-Shackleton SA. 2001. Sex differences in songbirds 25 years later: what have we learned and where do we go? Microsc Res Tech 54:327-334.
9. Balthazart J, Absil P. 1997. 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 382:401-428.
10. Balthazart J, Adkins-Regan E. 2002. Sexual differentiation of brain and behavior in birds. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT, editors. Hormones, brain and behavior. San Diego: Academic Press, p 223-301.
11. Balthazart J, Ball GF. 1998. The Japanese quail as a model system for the investigation of steroid-catecholamine interactions mediating appetitive and consummatory aspects of male sexual behavior. Annu Rev Sex Res 9:96-176.
12. Balthazart J, Foidart A. 1993. Brain aromatase and the control of male sexual behavior. J Steroid Biochem Mol Biol 44:521-540.
13. Balthazart J, Schumacher M, Ottinger MA. 1983. Sexual differences in the Japanese quail: behavior, morphology and intracellular metabolism of testosterone. Gen Comp Endocrinol 51:191-207.
14. Balthazart J, Foidart A, Harada N. 1990. Immunocytochemical localization of aromatase in the brain. Brain Res 514:327-333.
15. Balthazart J, De Clerck A, Foidart A. 1992a. Behavioral demasculinization of female quail is induced by estrogens: studies with the new aromatase inhibitor, R76713. Horm Behav 26:179-203.
16. Balthazart J, Surlemont C, Harada N. 1992b. Aromatase as a cellular marker of testosterone action in the preoptic area. Physiol Behav 51:395-409.
17. Balthazart J, Dupiereux V, Aste N, Viglietti-Panzica C, Barrese M, Panzica GC. 1994. Afferent and efferent connections of the sexually dimorphic medial preoptic nucleus of the male quail revealed by in vitro transport of DiI. Cell Tissue Res 276:455-475.
18. Balthazart J, Tlemçani O, Ball GF. 1996a. Do sex differences in the brain explain sex differences in the hormonal induction of reproductive behavior? What 25 years of research on the Japanese quail tells us. Horm Behav 30:627-661.
19. Balthazart J, Tlemçani O, Harada N. 1996b. Localization of testosterone-sensitive and sexually dimorphic aromatase-immunoreactive cells in the quail preoptic area. J Chem Neuroanat 11:147-171.
20. Balthazart J, Foidart A, Baillien M, Harada N, Ball GF. 1998. Anatomical relationships between aromatase and tyrosine hydroxylase in the quail brain: double-label immunocytochemical studies. J Comp Neurol 391:214-226.
21. Balthazart J, Baillien M, Charlier TD, Ball GF. 2003. Calcium-dependent phosphorylation processes control brain aromatase in quail. Eur J Neurosci 17:1591-1606.
22. Balthazart J, Baillien M, Cornil CA, Ball GF. 2004. Preoptic aromatase modulates male sexual behavior: slow and fast mechanisms of action. Physiol Behav 83:247-270.
23. Bandler R, Shipley MT. 1994. Columnar organization in the midbrain periaqueductal gray: modules for emotional expression? Trends Neurosci 17:379-389.
24. Baylé JD, Ramade F, Oliver J. 1974. Stereotaxic topography of the brain of the quail. J Physiol (Paris) 68:219-241.
25. Brackett NL, Iuvone PM, Edwards DA. 1986. Midbrain lesions, dopamine and male sexual behavior. Behav Brain Res 20:231-240.
26. Breedlove SM. 1992. Sexual dimorphism in the vertebrate nervous system. J Neurosci 12:4133-4142.
27. Calizo LH, Flanagan-Cato LM. 2002. Estrogen-induced dendritic spine elimination on female rat ventromedial hypothalamic neurons that project to the periaqueductal gray. J Comp Neurol 447:234-248.
28. Charlier TD, Ball GF, Balthazart J. 2005a. Inhibition of steroid receptor coactivator-1 blocks estrogen and androgen action on male sex behavior and associated brain plasticity. J Neurosci 25:906-913.
29. Charlier TD, Ball GF, Balthazart J. 2005b. Sexual behavior activates the expression of the immediate early genes c-fos and Zenk (egr-1) in catecholaminergic neurons of male Japanese quail. Neuroscience 131:13-30.
30. De Vries GJ, Simerly RB. 2002. Anatomy, development, and function of sexually dimorphic neural circuits in the mammalian brain. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT, editors. Hormones, brain and behavior. San Diego: Academic Press, p 137-191.
31. Foidart A, De Clerck A, Harada N, Balthazart J. 1994. Aromatase-immunoreactive cells in the quail brain: effects of testosterone and sex dimorphism. Physiol Behav 55:453-464.
32. Foidart A, Reid J, Absil P, Yoshimura N, Harada N, Balthazart J. 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.
33. Gu GB, Simerly RB. 1997. Projections of the sexually dimorphic anteroventral periventricular nucleus in the female rat. J Comp Neurol 384:142-164.
34. Gu G, Cornea A, Simerly RB. 2003. Sexual differentiation of projections from the principal nucleus of the bed nuclei of the stria terminalis. J Comp Neurol 460:542-562.
35. Harada N. 1988. Cloning of a complete cDNA encoding human aromatase: immunochemical identification and sequence analysis. Biochem Biophys Res Commun 156:725-732.
36. Harada N, Yamada K, Foidart A, Balthazart J. 1992. Regulation of aromatase cytochrome P-450 (estrogen synthetase) transcripts in the quail brain by testosterone. Mol Brain Res 15:129-126.
37. Holloway CC, Clayton DE. 2001. Estrogen synthesis in the male brain triggers development of the avian song control pathway in vitro. Nat Neurosci 4:170-175.
38. Hull EM, Meisel RL, Sachs BD. 2002. Male sexual behavior. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT, editors. Hormones, brain and behavior. San Diego: Academic Press, p 1-137.
39. Hutchison RE. 1978. Hormonal differentiation of sexual behavior in Japanese quail. Horm Behav 11:363-387.
40. Jost A. 1978. Basic sexual trends in the development of vertebrates. Ciba Found Symp 62:5-18.
41. Jost A, Vigier B, Prepin J, Perchellet JP. 1973. Studies on sex differentiation in mammals. Recent Prog Horm Res 29:1-41.
42. Kelley D. 1988. Sexually dimorphic behaviors. Annu Rev Neurosci 11:225-251.
43. Konishi M, Akutagawa E. 1985. Neuronal growth, atrophy an death in a sexually dimorphic song nucleus in the zebra finch. Nature 315:145-147.
44. Lisciotto CA, Morrell JI. 1994. Sex differences in the distribution and projections of testosterone target neurons in the medial preoptic area and the bed nucleus of the stria terminalis of rats. Horm Behav 28:492-502.
45. Lonstein JS, de Vries GJ. 2000. Sex differences in the parental behavior of rodents. Neurosci Biobehav Rev 24:669-686.
46. MacDougall-Shackleton SA, Ball GF. 1999. Comparative studies of sex differences in the song-control system of songbirds. Trends Neurosci 22:432-436.
47. Marson L, List MS, McKenna KE. 1992. Lesions of the nucleus paragigantocellularis alter ex copula penile reflexes. Brain Res 592:187-192.
48. McKenna KE. 2000. Some proposals regarding the organization of the central nervous system control of penile erection. Neurosci Biobehav Rev 24:535-540.
49. Meddle SL, King VM, Follett BK, Wingfield JC, Ramenofsky M, Foidart A, Balthazart J. 1997. Copulation activates Fos-like immunoreactivity in the male quail forebrain. Behav Brain Res 85:143-159.
50. Murphy AZ, Hoffman GE. 2001. Distribution of gonadal steroid receptor-containing neurons in the preoptic-periaqueductal gray-brainstem pathway: a potential circuit for the initiation of male sexual behavior. J Comp Neurol 438:191-212.
51. Murphy AZ, Rizvi TA, Ennis M, Shipley MT. 1999. The organization of preoptic-medullary circuits in the male rat: evidence for interconnectivity of neural structures involved in reproductive behavior, antinociception and cardiovascular regulation. Neuroscience 91:1103-1116.
52. Nordeen EJ, Nordeen KW. 1988. Sex and regional differences in the incorporation of neurons born during song learning in zebra finches. J Neurosci 8:2869-2874.
53. Nordeen EJ, Grace A, Burek MJ, Nordeen KW. 1992. Sex-dependent loss of projection neurons involved in avian song learning. J Neurobiol 23:671-679.
54. Nottebohm F, Arnold AP. 1976. Sexual dimorphism in vocal control areas of the songbird brain. Science 194:211-213.
55. Panzica GC, Viglietti-Panzica C, Calcagni M, Anselmetti GC, Schumacher M, Balthazart J. 1987. Sexual differentiation and hormonal control of the sexually dimorphic preoptic medial nucleus in quail. Brain Res 416:59-68.
56. Panzica GC, Viglietti-Panzica C, Sanchez F, Sante P, Balthazart J. 1991. Effects of testosterone on a selected neuronal population within the preoptic sexually dimorphic nucleus of the Japanese quail. J Comp Neurol 303:443-456.
57. Panzica GC, Viglietti-Panzica C, Balthazart J. 1996. The sexually dimorphic medial preoptic nucleus of quail: a key brain area mediating steroid action on male sexual behavior. Front Neuroendocrinol 17:51-125.
58. Panzica GC, Castagna C, Viglietti-Panzica C, Russo C, Tlemçani O, Balthazart J. 1998. Organizational effects of estrogens on brain vasotocin and sexual behavior in quail. J Neurobiol 37:684-699.
59. Polston EK, Gu G, Simerly RB. 2004. Neurons in the principal nucleus of the bed nuclei of the stria terminalis provide a sexually dimorphic GABAergic input to the anteroventral periventricular nucleus of the hypothalamus. Neuroscience 123:793-803.
60. Raisman G, Field PM. 1971. Sexual dimorphism in the preoptic area of the rat. Science 173:731-733.
61. Reiner AD, Perkel J, Bruce L, Butler A, Csillag A, Kuenzel W, Medina L, Paxinos G, Shimizu T, Striedter G, Wild M, Ball GF, Durand S, Guntürkün O, Lee DW, Mello CV, White SA, Hough G, Kubikova L, Smulders TV, Wada K, Dugas-Ford J, Husband S, Yamamoto K, Yu J. 2004. Revised nomenclature for avian telencephalon and some related brainstem nuclei. J Comp Neurol 473:377-414.
62. Schumacher M, Balthazart J. 1986. Testosterone-induced brain aromatase is sexually dimorphic. Brain Res 370:285-293.
63. Schwartz-Giblin S, McCarthy MM. 1995. A sexual column in the PAG? Trends Neurosci 18:129.
64. Short RV, Balaban E. 1994. The differences between the sexes. New York: Cambridge University Press.
65. Simerly RB. 2002. Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu Rev Neurosci 25:507-536.
66. Simpson HB, Vicario DS. 1991. Early estrogen treatment of female zebra finches masculinizes the brain pathway for learned vocalizations. J Neurobiol 22:777-793.
67. Taziaux M, Cornil CA, Dejace C, Arckens L, Ball GF, Balthazart J. 2006. Neuroanatomical specificity in the expression of the immediate early gene c-fos following expression of appetitive and consummatory male sexual behavior in Japanese quail. Eur J Neurosci 23:1869-1887.
68. Voigt C, Ball GF, Balthazart J. 2006. Neuroanatomical specificity of sex differences in expression of aromatase mRNA in the quail brain. Soc Neurosci Abst. Program No. 2694. 2006 Neuroscience Meeting Planner, Atlanta, GA.
69. Williams H. 1985. Sexual dimorphism of auditory activity in the zebra finch song system. Behav Neural Biol 44:470-484.
70. Zann RA. 1996. The zebra finch: a synthesis of field and laboratory studies. Oxford: Oxford University Press.