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Development of Sex Differences in the Nervous System

  • Nancy G. Forger
Part of the Handbook of Behavioral Neurobiology book series (HBNE, volume 13)

Abstract

Before launching into a review of sexual differentiation, it seems appropriate to consider for a moment why there are two sexes. Sexual reproduction pervades the world of living organisms and yet sex itself remains a mystery. When an organism reproduces sexually only half of the population produces any offspring—a consequence that [Maynard-Smith (1978)] has referred to as “the cost of producing males” The sacrifice that sex entails can be appreciated by considering that a female could have twice as many grandchildren were she and her offspring to reproduce asexually. For the selfish gene, this would seem to be an enormous cost! So what maintains sex despite this major advantage of asexual reproduction?

Keywords

Androgen Receptor Sexual Differentiation Zebra Finch Preoptic Area Gonadal Steroid 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Adkins-Regan, E., & Aenzi, M. (1990). Sexual differentiation of behavior in the zebra finch: Effect of early gonadectomy or androgen treatment. Hormones and Behavior, 24, 114–127PubMedGoogle Scholar
  2. Adkins-Regan, E., Abdelnabi, M., Mobarek, M., & Ottinger, M. A. (1990). Sex steroid levels in developing and adult male and female zebra finches (Poephila guttata). General and Comparative Endocrinology, 78, 93–109PubMedGoogle Scholar
  3. Ahdieh, H. B., & Feder, H. H. (1988). Sex differences in nucular androgen receptors in guinea pig brain and the effects of an a2 nor adrenergic blocker on androgen receptors. Brain Research, 456, 275–279PubMedGoogle Scholar
  4. Aigner, L., Arber, S., Kapfhammer, J. P., Laux, T., Schneider, C., Botteri, E, Brenner, H.-R., & Caroni, P. (1995). Overexpression of the neural growth-associated protein GAP-43 induces nerve sprouting in the adult nervous system of transgenic mice. Cell, 83, 269–278PubMedGoogle Scholar
  5. Allen, L. S., Hines, M., Shryne, J. E., & Gorski, R. A. (1989). Two sexually dimorphic cell groups in the human brain. J ournal of Neuro&ience, 9, 497–506Google Scholar
  6. Al-Shamma, H., & De Vries, G. J. (1996). Neurogenesis of the sexually dimorphic vasopressin cells of the bed nucleus of the stria terminalis and amygdala of rats. Journal of Neurobiology, 29, 91–98PubMedGoogle Scholar
  7. Alvarez-Buylla, A., & Nottebohm, F. (1988). Migration of young neurons in adult avian brain. Nature, 335, 353–354PubMedGoogle Scholar
  8. Anderson, C. H., & Greenwald, G. S. (1969). Autoradiographic analysis of estradiol uptake in the brain and pituitary of the female rat. Endocrinology, 85, 1160–1165PubMedGoogle Scholar
  9. Arai, Y., Sekine, Y., & Murakami, S. (1996). Estrogen and apoptosis in the developing sexually dimorphic preoptic area in female rats. Neuro&ience Research, 25, 403–407Google Scholar
  10. Arendash, G. W., & Gorski, R A. (1983). Effects of di&rete lesions of the sexually dimorphic nucleus of the preoptic area or other medial preoptic regions on the sexual behavior of male rats. Brain Research Bulletin, 10, 147–154PubMedGoogle Scholar
  11. Arnold, A. P. (1975). The effects of castration on song development in zebra finches (Poephila guttata). Journal of Experimental Zoology, 191, 261–277PubMedGoogle Scholar
  12. Arnold, A. P. (1996). Genetically triggered sexual differentiation of brain and behavior. Hormones and Behavior, 30, 495–505PubMedGoogle Scholar
  13. Arnold, A. P., & Schlinger, B. A. (1993). Sexual differentiation of brain and behavior: The zebra finch is not just a flying rat. Brain Behavior and Evolution, 42, 231–241Google Scholar
  14. Baarends, W. M., van Helmond, M. J. L., Post, M., van der Schoot, J. C. M., Hoogerbrugghe, J. W., de Winter, J. P., Uilenbroek, J. T. J., Karels, B., Wilming, L. G., Meijers, J. H. C., Themmen, A. P. N., & Grootegoed, J. A. (1994). A novel member of the transmembrane serine/threonine kinase receptor family is specifically expressed in the gonads and in mesenchymal cells adjacent to the Müllerian duct. Development,120, 189–197PubMedGoogle Scholar
  15. Bakker, J., Pool, C. W., Sonnemans, M., van Leeuwen, E W., & Slob, A. K. (1997). Quantitative estimation of estrogen and androgen receptor-inamunoreactive cells in the forebrain of neonatally estrogen-deprived male rats. Neuro&ience, 77, 911–919Google Scholar
  16. Balthazart, J. (1989). Correlation between the sexually dimorphic aromatase of the preoptic area and sexual behavior in quail: Effects of neonatal manipulations of the hormonal milieu. Archives Intern tionales de Physiologie de Biochimie, 97, 465–481Google Scholar
  17. Balthazart, J., Absil, P., Fiasse, V., & Ball, G. F. (1995). Effects of the aromatase inhibitor R76713 on sexual differentiation of brain and behavior in zebra finches. Behavior, 131, 225–255Google Scholar
  18. Barraclough, C. A. (1961). Production of arrovulatory sterile rats by single injections of testosterone propionate. Endocrinology, 68, 62–67PubMedGoogle Scholar
  19. Barraclough, C. A. (1967). Modifications in reproductive function after exposure to hormones during the prenatal and early postnatal period. In L. Martini, & W. F. Ganong (Eds.), Neuroendocrinology (pp. 6199). New York: Academic PressGoogle Scholar
  20. Barraclough, C. A., & Gorski, R. A. (1961). Evidence that the hypothalamus is responsible for androgen-induced sterility of the female rat. Endocrinology,68, 68–79PubMedGoogle Scholar
  21. Baum, M. J., Woutersen, P. J. A., & Slob, A. K. (1991). Sex difference in whole-body androgen content in rats on fetal days 18 and 19 without evidence that androgen passes from males to females. Biology of Reproduction, 44, 747–751PubMedGoogle Scholar
  22. Beato, M. (1989). Gene regulation by steroid hormones. Cell, 56, 335–344PubMedGoogle Scholar
  23. Behringer, R. R., Cate, R. L., Froelick, G. J., Palmiter, R. D., & Brinster, R. L. (1990). Abnormal sexual development in transgenic mice chronically expressing Müllerian inhibiting substance. Nature, 345, 167–170PubMedGoogle Scholar
  24. Behringer, R. R., Finegold, M. J., & Cate, R. L. (1994). Müllerian inhibiting substance function during mammalian sexual development. Cell, 79, 415–425PubMedGoogle Scholar
  25. Bell, G. (1982). The masterpiece of nature Berkeley, CA: University of California PressGoogle Scholar
  26. Belote, J. M. (1989). The control of sexual development in Drosophilia melanogaster Genetic and molecular analysis of a genetic regulatory hierarchy-A minireview. Gene, 82, 161–167PubMedGoogle Scholar
  27. Beyer, C., Euster&hulte, B., Pilgrim, C., & Reisert, I. (1992). Sex steroids do not alter sex differences in tyrosine hydroxylase activity of dopaminergic neurons in vitro. Cell Tissue Research, 270, 547–552PubMedGoogle Scholar
  28. Bleier, R., Byne, W., & Siggelkow, I. (1982). Cytoarchitectonic sexual dimorphisms of the medial preoptic and anterior hypothalamic areas in guinea pig, rat, hamster, and mouse. Journal of Comparative Neurology, 212, 118–130PubMedGoogle Scholar
  29. Bluthe, R., & Dantzer, R. (1990). Social recognition does not involve vasopressinergic neurotransmission in female rats. Brain Research,535, 301–304PubMedGoogle Scholar
  30. Breedlove, S. M. (1997). Neonatal androgen and estrogen treatments ma&ulinize the size of motoneurons in the rat spinal nucleus of the bulbocavernosus. Cellular and Molecular Neurobiology, 17, 687–697PubMedGoogle Scholar
  31. Breedlove, S. M., & Arnold, A. P. (1980). Hormone accumulation in a sexually dimorphic motor nucleus in the rat spinal cord. &ience, 210, 564–566Google Scholar
  32. Breedlove, S. M., & Arnold, A. P. (1981). Sexually dimorphic motor nucleus in the rat lumbar spinal cord: Response to adult hormone manipulation, absence in androgen-insensitive rats. Brain Research, 225, 297–307Google Scholar
  33. Breedlove, S. M., & Arnold, A. P. (1983). Hormonal control of a developing neuromu&ular system. I. Complete dema&ulinization of the male rat spinal nucleus of the bulbocavernosus using the anti-androgen flutamide. Journal of Neuro&ience, 3, 417–423Google Scholar
  34. Breedlove, S. M., Jordan, C. L., &Arnold, A. P. (1983). Neurogenesis of motoneurons in the sexually dimorphic spinal nucleus of the bulbocavernosus in rats, Developmental Brain Research, 9, 39–43Google Scholar
  35. Brinton, R D. (1993). 173-Estradiol induction of filopodial growth in cultured hippocampal neurons within minutes of exposure. Molecular and Cellular Neuro&iences, 4, 36–46Google Scholar
  36. Brinton, R. D., Tran, J., Proffitt, P., & Montoya, M. (1997), 173-Estradiol enhances the outgrowth and survival of neocortical neurons in culture. Neurochemical Research, 22, 1339–1351PubMedGoogle Scholar
  37. Brown, S. D., Johnson, F., & Bottjer, S. W. (1993). Neurogenesis in adult canary telencephalon is independent of gonadal hormone levels. Journal of Neuro&ience, 13, 2024–2032Google Scholar
  38. Brown, T. J., Hochberg, R. B., Zielinski, J. E., & MacLusky, N. J. (1988). Regional sex differences in cell nuclear estrogen-binding capacity in the rat hypothalamus and preoptic area. Endocrinology, 123, 1761–1770PubMedGoogle Scholar
  39. Brown, T.J., Naftolin, F., & MacLusky, N.J. (1992). Sex differences in estrogen receptor binding in the rat hypothalamus: Effects of subsaturating pulses of estradiol. Brain Research, 578, 129–134PubMedGoogle Scholar
  40. Brown, T. J., Yu, J., Gagnon, M., Sharma, M., & MacLusky, N. J. (1996). Sex differences in estrogen receptor and progestin receptor induction in the guinea pig hypothalamus and preoptic area. Brain Research, 725, 37–48PubMedGoogle Scholar
  41. Bull, J. J., & Vogt, R. C. (1979). Temperature-dependent sex determination in turtles. &ience,206, 1186–1188Google Scholar
  42. Byne, W., & Bleier, R (1987). Medial preoptic sexual dimorphisms in the guinea pig. I. An investigation of their hormonal dependence. Journal of Neuro&ience, 7, 2688–2696Google Scholar
  43. Catlin, E. A., Powell, S. M., Manganaro, T. E, Hudson, P. L., Ragin, R. C., Epstein, J., & Donahoe, P. K. (1990). Sex-specific fetal lung development and Müllerian inhibiting substance. American Review of Respiratory Disease, 141, 466–470PubMedGoogle Scholar
  44. Charest, N.J., Zhou, Z. X., Lubahn, D. B., Olsen, K. L., French, F. S., & Wilson, E. M. (1991). Aframeshift mutation destabilizes androgen receptor messenger RNA in the TFM mouse. Molecular Endocrinology, 5, 573–581PubMedGoogle Scholar
  45. Cherry, J. A., & Baum, M. J. (1990). Effects of lesions of a sexually dimorphic nucleus in the preoptic/ anterior hypothalamic area on the expression of androgen-and estrogen-dependent sexual behaviors in male ferrets. Brain Research,522, 191–203PubMedGoogle Scholar
  46. Clépet, C., &hafer, A. J., Sinclair, A. H., Palmer, M. S., Lovell-Badge, R, & Goodfellow, P. N. (1993). The human SRY tran&ript. Human Molecular Genetics, 2, 2007–2012PubMedGoogle Scholar
  47. Collado, P., Beyer, C., Hutchison, J. B., & Holman, S. D. (1995). Hypothalamic distribution of astrocytes is gender-related in Mongolian gerbils. Neuro&ience Letters, 184, 86–89Google Scholar
  48. Commins, D., & Yahr, P. (1984a). Adult testosterone levels influence the morphology of a sexually dimorphic area in the Mongolian gerbil brain. Journal of Comparative Neurology, 224, 132–140Google Scholar
  49. Commins, D., & Yahr, P. (1984b). Lesions of the sexually dimorphic area disrupt mating and marking in male gerbils. Brain Research Bulletin, 13, 185–193Google Scholar
  50. Crews, D., Wade, J., & Wilczynski, W. (1990). Sexually dimorphic areas in the brain of whiptail lizards. Brain Behavior and Evolution, 36, 262–270Google Scholar
  51. Crews, D., Bergeron, J. M., Bull, J. J., Flores, D., Tousignant, A., Skipper, J. K., & Wibbels, T (1994). Temperature-dependent sex determination in reptiles: Proximate mechanisms, ultimate outcomes, and practical applications. Developmental Genetics, 15, 297–312PubMedGoogle Scholar
  52. Crowley, W. R., O’Donohue, T L., & Jacobowitz, D. M. (1978). Sex differences in catecholamine content in di&rete brain nuclei of the rat: Effects of neonatal castration or testosterone treatment. Acta Endocrínologica, 89, 20–28PubMedGoogle Scholar
  53. Dantzer, R, Koob, G. E, Bluthé, R., & Le Moal, M. (1988). Septal vasopressin modulates social memory in male rats. Brain Research, 457, 143–147PubMedGoogle Scholar
  54. Davies, A. M. (1995). The bcl-2 family of proteins, and the regulation of neuronal survival. Trends in Neuro&iences, 18, 355–358Google Scholar
  55. Davies, A. M. (1996). Paracrine and autocrine actions of neurotrophic factors. Neurochemical Research, 21, 749–753PubMedGoogle Scholar
  56. Davis, E. C., Popper, P., & Gorski, R. A. (1996). The role of apoptosis in sexual differentiation of the rat sexually dimorphic nucleus of the preoptic area. Brain Research,734, 10–18PubMedGoogle Scholar
  57. De Jonee, F. H., Louwerse, A. L., Ooms, M. P., Evers, P., Endert, E., &Van de Poll, N. E. (1989). Lesions of the SDN-POA inhibit sexual behavior of male wistar rats. Brain Research Bulletin, 23, 483–492Google Scholar
  58. del Abril, A., Segovia, S., & Guillamon, A. (1990). Sexual dimorphism in the parastrial nucleus of the rat preoptic area. Developmental Brain Research, 52, 11–15PubMedGoogle Scholar
  59. De Voogd, T. J., & Nottebohm, F. (1981a). Gonadal hormones induce dendritic growth in the adult avian brain. Science, 214, 202–204Google Scholar
  60. De Voogd, T. J., & Nottebohm, F. (1981b). Sex differences in dendritic morphology of a song control nucleus in the canary: A quantitative golgi study. Journal of Comparative Neurology, 196, 309–316Google Scholar
  61. De Voogd, T. J., Nixdorf, B., & Nottebohm, F. (1985). Synaptogenesis and changes in synaptic morphology related to aquisition of a new behavior. Brain Research, 329, 304–308Google Scholar
  62. De Vries, G. J. (1990). Sex differences in neurotransmitter systems. Journal of Neuroendocrinology, 2, 1–13PubMedGoogle Scholar
  63. De Vries, G. J., & Boyle, P. A. (1998). Double duty for sex differences in the brain. Behavior in Brain Research, 92, 205–213Google Scholar
  64. De Vries, G. J., & Villalba, C. (1997). Brain sexual dimorphism and sex differences in parental and other social behaviors. Annals of the New York Academy of &iences, 807, 273–286Google Scholar
  65. De Vries, G. J., Buijs, R. M., &Shifter, A. A. (1984). Gonadal hormone actions on the morphology of the vasopressinergic innervation of the adult rat brain. Brain Research,298, 141–145PubMedGoogle Scholar
  66. De Vries, G. J., Crenshaw, B. J., & Al-Shamma, H. A.. (1992). Gonadal steroid modulation of vasopressin pathways. Annals of the New York Academy of &iences, 652, 387–396Google Scholar
  67. Diamond, M., Binstock, T., & Kohl,J. V. (1996). From fertilization to adult sexual behavior. Hormones and Behavior, 30, 333–353PubMedGoogle Scholar
  68. di Clemente, N., Wilson, C., Faure, E., Boussin, L., Carmillo, P., Tizard, R., Picard, J.-Y., Vigier, B., Josso, N., & Cate, R. (1994). Cloning, expression, and alternative splicing of the receptor for anti-Müllerian hormone. Molecular Endocrinology, 8, 1006–1020PubMedGoogle Scholar
  69. Dohler, K. D., Srivastava, S. S., Shryne, J. E., Jarzab, B., Sipos, A., & Gorski, R. A. (1984). Differentiation of the sexually dimorphic nucleus in the preoptic area of the rat brain is inhibited by postnatal treatment with an estrogen antagonist. Neuroendocrinology, 38, 297–301PubMedGoogle Scholar
  70. Don Carlos, L. L., & Handa, R. J. (1994). Developmental profile of estrogen receptor mRNA in the preoptic area of male and female neonatal rats. Developmental Brain Research, 79, 283–289PubMedGoogle Scholar
  71. Don Carlos, L. L., Mc Abee, M., Ramer-Quinn, D S., & Stancik, D. M. (1995). Estrogen receptor mRNA levels in the preoptic area of neonatal rats are responsive to hormone manipulation. Developmental Brain Research, 84, 253–260PubMedGoogle Scholar
  72. Drea, C. M., Weldele, M. L., Forger, N. G., Co&ia, E. M., Frank, L. G., Licht, P., & Glickman, S. E. (1998), Androgens and ma&ulinization of genitalia in the spotted hyaena (Crocuta crocuta) 2. Effects of prenatal anti-androgens. Journal of Reproduction and Fertility, 113, 117–127PubMedGoogle Scholar
  73. Dubois-Dauphin, M., Frankowski, H., Tsujimoto, Y., & Huarte, J. (1994). Neonatal motoneurons over-expressing the bel-2 protooncogene in transgenic mice are protected from axotomy-induced cell death. Proceedings of the National Academy of &iences of the USA, 91, 3309–3313Google Scholar
  74. Eisenfeld, A. J., & Axelrod, J. (1965), Selectivity of estrogen distribution in tissues. Journal of Pharmacology and Experimental Therapeutics, 150, 469–475PubMedGoogle Scholar
  75. Feder, H. H. (1981). Perinatal hormones and their role in the development of sexually dimorphic behaviors. In N. T. Adler (Ed.), Neuroendocrinology of Reproduction (pp. 158.-228). New York: Plenum PressGoogle Scholar
  76. Fishman, R. B., & Breedlove, S. M. (1985). The androgenic induction of spinal sexual dimorphism is independent of supraspinal afferents. Developmental Brain Research, 23, 255–258Google Scholar
  77. Ford, C. E., Jones, K. W., Polani, P. E., de Almeida, J. C., & Briggs, J. H. (1959). A sex-chromosome anomaly in a case of gonadal dysgenesis (Turner’s Syndrome). Lancet, 1, 711–713Google Scholar
  78. Forger, N. G., & Breedlove, S. M. (1986). Sexual dimorphism in human and canine spinal cord: Role of early androgen. Proceedings of the National Academy of &iences of the USA, 83, 7527–7531Google Scholar
  79. Forger, N. G., & Breedlove, S. M. (1987). Seasonal variation in mammalian striated mu&le mass and motoneuron morphology. Journal of Neurobiology, 18, 155–165PubMedGoogle Scholar
  80. Forger, N. G., & Breedlove, S. M. (1991) Steroid influences on a mammalian neuromu&ular system. Seminars in the Neuro&iences, 3, 459–468Google Scholar
  81. Forger, N. G., Roberts, S. L., Wong, V., & Breedlove, S. M. (1993). Ciliary neurotrophic factor maintains motoneurons and their target mu&les in developing rats. Journal of Neuro&ience, 13, 4720–4726Google Scholar
  82. Forger, N. G., Wong, V., & Breedlove, S. M. (1995). Ciliary neurotrophic factor arrests mu&le and motoneuron degeneration in androgen-insensitive rats. Journal of Neurobiology, 28, 354–362PubMedGoogle Scholar
  83. Forger, N. G., Frank, L. G., Breedlove, S. M., & Glickman, S. E. (1996). Sexual dimorphism of perinea] mu&les and motoneurons in spotted hyenas. Journal of Comparative Neurology, 375, 333–343PubMedGoogle Scholar
  84. Forger, N. G., Howell, M. L., Bengston, L., MacKenzie, L., De Chiara, T. M., & Yancopoulos, G. D. (1997). Sexual dimorphism in the spinal cord is absent in mice lacking the ciliary neurotrophic factor receptor. Journal of Neuro&ience, 17, 9605–9612Google Scholar
  85. Freeman, L. M., Watson, N. V., &Breedlove, S. M. (1996). Androgen spares androgen-insensitive moto-neurons from apoptosis in the spinal nucleus of the bulbocavernosus in rats. Hormones and Behavior, 30, 424–433PubMedGoogle Scholar
  86. Gahr, M., & Konishi, M. (1988). Developmental changes in estrogen-sensitive neurons in the forebrain of the zebra finch. Proceedings of the National Academy of &iences of the USA, 85, 7380–7383Google Scholar
  87. Garcia-Segura, L. M., Chowen, J. A., Duenas, M., Torres-Aleman, I., & Naftolin, F. (1994). Gonadal steroids as promoters of neuroglial plasticity. Psychoneuroendocrinology, 19, 445–453PubMedGoogle Scholar
  88. Garcia-Segura, L. M., Chowen, J. A., & Naftolin, F. (1996). Endocrine glia: roles of glial cells in the brain actions of steroid and thyroid hormones and in the regulation of hormone secretion. Frontiers in Neuroendocrinolagy, 17, 180–211Google Scholar
  89. Garcia-Segura, L. M., Cardona-Gomez, P., Naftolin, F., & Chowen, J. A. (1998). Estradiol upregulates ßc1–2 expression in adult brain neurons. NeuroReport, 9, 593–597PubMedGoogle Scholar
  90. George, F. W., & Ojeda, S. R. (1982). Changes in aromatase activity in the rat brain during embryonic, neonatal, and infantile development. Endocrinology,111, 522–529PubMedGoogle Scholar
  91. George, F. W., & Wilson, J. D. (1994). Sex determination and differentiation. In E. Knobil, & J. D. Neill (Eds.), The physiology of reproduction (2nd ed., pp. 3–28). New York: Raven PressGoogle Scholar
  92. Gibbs, R. B. (1998). Levels of trkA and BDNF mRNA, but not NGF mRNA, fluctuate across the estrous cycle and increase in response to acute hormone replacement. Brain Research,787, 259–268PubMedGoogle Scholar
  93. Giulian, D., Pohorecky, L. A., & McEwen, B. S. (1973). Effects of gonadal steroids upon brain 5-hydroxy-tryptamine levels in the neonatal rat. Endocrinology,93, 1329–1335PubMedGoogle Scholar
  94. Glickman, S. E., Frank, L. G., Licht, P., Yalcinkaya, T., Siiteri, P., & Davidson, J. (1992). Sexual differentiation of the female spotted hyena. Annals of the New York Academy of &iences, 662, 135–159Google Scholar
  95. Goodfellow, P. N., & Lovell-Badge, R. (1993). Sry and sex determination in mammals. Annual Review of Genetics, 27, 71–92PubMedGoogle Scholar
  96. Gorski, R. A., & Wagner, J. W. (1965). Gonadal activity and sexual differentiation of the hypothalamus. Endocrinology, 76, 226–239PubMedGoogle Scholar
  97. Gorski, R. A., Gordon, J. H., Shryne, J. E., & Southam, A. M. (1978). Evidence for a morphological sex difference within the medial preoptic area of the rat brain. Brain Research, 148, 333–346PubMedGoogle Scholar
  98. Goy, R. W., & McEwen, B. S. (1980). Sexual differentiation of the brain Cambridge, MA: MIT PressGoogle Scholar
  99. Graves, J. A. M. (1990). The search for the mammalian testis-determining factor is on again. Reproduction Fertility and Development, 2, 199–204Google Scholar
  100. Griffin, J. E., & Wilson, J. D. (1989). The androgen-resistance syndromes: 5 alpha reductase deficiency, testicular feminization, and related disorders. In C. R. Striver, A. L. Beaudet, W. S. Sly, and D. Valle (Eds.), The metabolic and molecular basis of inherited disease (6th ed., pp. 1919–1944). New York: McGraw-HillGoogle Scholar
  101. Gubbay, J., Collignon, J., Koopman, P., Cape], B., Economou, A., Münsterberg, A., Vivian, N., Goodfellow, P., & Lovell-Badge, R. (1990). A gene mapping to the sex-determining region of the mouse Y chromosome is a member of a novel family of embryonically expressed genes. Nature, 346, 245–250PubMedGoogle Scholar
  102. Gudelsky, G. A., & Porter, J. C. (1981). Sex-related difference in the release of dopamine into hypophysial portal blood. Endocrinology,109, 1394–1398PubMedGoogle Scholar
  103. Guillamon, A., de Blas, M. R., & Segovia, S. (1988). Effects of sex steroids on the development of the locus coeruleus in the rat. Developmental Brain Research, 40, 306–310Google Scholar
  104. Güldner, F. H. (1982). Sexual dimorphisms ofaxo-spine synapses and postsynaptic density material in the suprachiasmatic nucleus of the rat. Neuro&ience Letters, 28, 145–150PubMedGoogle Scholar
  105. Gupta, C., & Jaumotte J. (1993). Epidermal growth factor binding in the developing male reproductive duct and its regulation by testosterone. Endocrinology, 133, 1778–1782PubMedGoogle Scholar
  106. Gurney, M. (1981). Hormonal control of cell form and number in the zebra finch song system. Journal of Neuro&ience, 1, 658–673Google Scholar
  107. Gurney, M. (1982). Behavioral correlates of sexual differentiation in the zebra finch song system. Brain Research, 231, 153–172PubMedGoogle Scholar
  108. Gurney, M., & Konishi, M. (1980). Hormone-induced sexual differentiation of brain and behavior in zebra finches. &ience, 208, 1380–1383Google Scholar
  109. Halachmi, S., Marden, E., Martin, G., Mac Kay, H., Abbondanza, C., & Brown, M. (1994). Estrogen receptor-associated proteins: Possible mediators of hormone-induced tran&ription. &ience, 264, 1455–1458Google Scholar
  110. Honda, R. J., Reid, D. L., & Resko, J. A. (1986). Androgen receptors in brain and pituitary of female rats: Cyclic changes and comparisons with the male. Biology of Reproduction, 34, 293–303Google Scholar
  111. Hogg, C. M., King, C., Ukiyama, E., Falsafi, S., Hogg, T. N., Donahoe, P. K., & Weiss, M. A. (1994). Molecular basis of mammalian sexual differentiation: Activation of Mallerian inhibiting substance gene expression by SRY. &ience,266, 1494–1500Google Scholar
  112. Harris, G. W., & Jacobsohn, D. (1952). Functional grafts of the anterior pituitary gland. Proceedings of the Royal Society of London, Series B. Biological &iences, 130, 263–276Google Scholar
  113. Heid, P., Guttinger, H. R., &Prove, E. (1985). The influence of castration and testosterone replacement on the song architecture of canaries (Serinus canaria). 7zit&hrift far Tierpsychologie, 69, 224–236Google Scholar
  114. Hengarmer, M. O., & Horvitz, H. R. (1994). C. elegans cell survival gene ced-9 encodes a functional homolog of the mammalian proto-oncogene bel-2. Cell,76, 665–676Google Scholar
  115. Herbert, J. (1993). Peptides in the limbic system. Neurochemical codes for coordinated adaptive responses to behavioral and physiological demand. Progress in Neurobiology, 41, 723–791PubMedGoogle Scholar
  116. Hnatczuk, O. C., Lisciotto, C. A., Don Carlos, L. L., Carter, S., & Morrell, J. I. (1994). Estrogen receptor immunoreactivity in specific brain areas of the prairie vole (Microbus ochrogaster) is altered by sexual receptivity and genetic sex. Journal of Endrocrinology, 6, 89–100Google Scholar
  117. Hodgkin, J. (1990). Sex determination compared in Drosophila and Caenorhabditis. Nature, 344, 721–728Google Scholar
  118. Hoffman, P. N., & Cleveland, D. W. (1988). Neurofilament and tubulin expression recapitulates the developmental program during axonal regeneration: Induction of a specific 3-tubulin isotype. Proceedings of the National Academy of &iences of the USA, 85, 4530–4533Google Scholar
  119. Hurst, L. D., & Peck, J. R. (1996). Recent advances in understanding of the evolution and maintenance of sex. TREE, 11, 46–52PubMedGoogle Scholar
  120. Hutchison, J. B., Wingfield, J. C., &Hutchison, R. E. (1984). Sex differences in plasma concentrations of steroids during the sensitive period for brain differentiation in the zebra finch. Journal of Endocrinology, 103, 363–369PubMedGoogle Scholar
  121. Hutton, L. A., Gu, G., & Simerly, R. B. (1998) Development of a sexually dimorphic projection from the bed nucleus of the stria terminalis to the anteroventral periventricular nucleus in the rat. Journal of Neuro&ience, 18, 3003–3013Google Scholar
  122. Imeri, L., Bianchi, S., Angeli, P., & Mancia, M. (1995). Stimulation of cholinergic receptors in the medial preoptic area affects sleep and cortical temperature. American Journal of Physiology, 269, R294–R299PubMedGoogle Scholar
  123. Lmperato-McGinley, J., Guerrero, L., Gautier, T., & Peterson, R. E. (1974). Steroid 5 alpha-reductase deficiency in man: An inherited form of male pseudohermaphroditism. Science,186, 1213–1215Google Scholar
  124. Isgor, C., & Sengelaub, D. R. (1996). Neonatal androgens affect adult spatial behavior and CA3 pyramidal cell morphology in rats: A Golgi study. Society for Neuro&ience Abstracts, 22, 756Google Scholar
  125. Jacobs, P. A., & Strong, J. A. (1959). A case of human intersexuality having a possible XXYsex-determining mechanism. Nature, 183, 302–303PubMedGoogle Scholar
  126. Jacobson, C. D., & Gorski, R. A. (1981). Neurogenesis of the sexually dimorphic nucleus of the preoptic area in the rat. Journal of Comparative Neurology, 196, 519–529Google Scholar
  127. Jacobson, C. D., Davis, F. C., & Gorski, R. A. (1985). Formation of the sexually dimorphic nucleus of the preoptic area: Neuronal growth, migration and changes in cell number. Developmental Brain Research, 21, 7–18Google Scholar
  128. Jordan, C. L., Padgett, B., Hershey, J., Prins, G., & Arnold, A. (1997). Ontogeny of androgen receptor immunoreactivity in lumbar motoneurous and in the sexually dimorphic levator ani mu&le of male rats. Journal of Comparative Neurology, 379, 88–98PubMedGoogle Scholar
  129. Jost, A. (1972). A new look at the mechanisms controlling sex differentiation in mammals. Johns Hopkins Medical Journal, 130, 38–52PubMedGoogle Scholar
  130. Juraska, J. M. (1991). Sex differences in “cognitive” regions of the rat brain. Psychoneuroendocrinology, 16, 105–119PubMedGoogle Scholar
  131. Juraska, J. M., Fitch, J., Henderson, C., & Rivers, N. (1985). Sex differences in the dendritic branching of dentate granule cells following differential experience. Brain Research,333, 73–80PubMedGoogle Scholar
  132. Juraska, J. M., Kopcik, J. R., Washburne, D. L, & Perry, D. L. (1988). Neonatal castration of male rats affects the dendritic response to differential environments in hippocampal dentate granule neurons. Psychobiology, 16, 406–410Google Scholar
  133. Karns, L. R., Shi-Chung, N., Freeman, J. A., & Fishman, M. C. (1987). Cloning of complementary DNA for GAP-43, a neuronal growth-related protein. &ience, 236, 597–600Google Scholar
  134. Kelley, D. B. (1988). Sexually dimorphic behaviors. Annual Review of Neuro&ience, 11, 225–251Google Scholar
  135. Kelley, D. B. (1997). Generating sexually differentiated songs. Current Opinion in Neurobiology, 7, 839–843PubMedGoogle Scholar
  136. Kelley, D. B., & Pfaff, D. W. (1978). Generalizations from comparative studies on neuroanatomical and endocrine mechanisms of sexual behavior. In J. B. Hutchison (Ed.), Biological determinants of sexual behavior (pp. 225–254). Chichester, UK: WileyGoogle Scholar
  137. Kirkpatrick, B., & Bryant, N. L. (1995). Sexual dimorphism in the brain: It’s worse than you thought. Biological Psychiatry, 38, 347–348PubMedGoogle Scholar
  138. Kirn, J. R., & De Voogd, T. J. (1989). Genesis and death of vocal control neurons during sexual differentiation in the zebra finch. Journal of Neuro&ience, 9, 3176–3187PubMedGoogle Scholar
  139. Kondrashov, A. S. (1988). Deleterious mutations and the evolution of sexual reproduction. Nature, 336, 435–440PubMedGoogle Scholar
  140. Konishi, M., & Akutagawa, E. (1985). Neuronal growth, atrophy and death in a sexually dimorphic song nucleus in the zebra finch brain. Nature, 315, 145–147PubMedGoogle Scholar
  141. Korsching, S. (1993). The neurotrophic factor concept: A reexamination. Journal of Neuro&ience, 13, 2739–2748Google Scholar
  142. Krey, L. C., & Mc Ewen, B. S. (1983). Steroid hormone processing in the brains and pituitary glands of nonhuman primates: Mechanisms and physiological significance. In R L. Norman (Ed.), NeuroendoBrine aspects of reproduction (pp. 47–67). New York: Academic PressGoogle Scholar
  143. Kuiper, G. G. L. N., Enmark, E., Pelto-Huikko, M., Nilsson, S., & Gustafsson, J. A. (1996). Cloning of a novel estrogen receptor expressed in rat prostate and ovary. Proceedings of the National Academy of &iences of the USA, 93, 5925–5930Google Scholar
  144. Kurz, E. M., Sengelaub, D. R., &Arnold, A. P. (1986). Androgens regulate the dendritic length of mammalian motoneurons in adulthood. &ience, 232, 395–398Google Scholar
  145. Ladosky, W., & Gaziri, L. C. J. (1970). Brain serotonin and sexual differentiation of the nervous system. Neuroendocrinology, 6, 168–174PubMedGoogle Scholar
  146. Lahr, G., Maxson, S. C., Mayer, A., Just, W., Pilgrim, C., & Reisert, I. (1995). Tran&ription of the Y chromosome gene, Sry, in adult mouse brain. Molecular Brain Research, 33, 179–182PubMedGoogle Scholar
  147. Lauber, A. H., Mobbs, C. V., Muramatsu, M., & Pfaff, D. W. (1991). Estrogen receptor messenger RNA expression in rat hypothalamus as a function of genetic sex and estrogen dose. Endocrinology,129, 3180–3186PubMedGoogle Scholar
  148. Leedy, M. G., Beattie, M. S., & Bresnahan, J. C. (1987). Testosterone-induced plasticity of synaptic inputs to adult mammalian motoneurons. Brain Research, 424, 386–390PubMedGoogle Scholar
  149. Lieberburg, I., & Mc Ewen, B. S. (1977). Brain cell nuclear retention of testosterone metabolites, 5 a-dihydrotestosterone and estradiol-173, in adult rats. Endocrinology,100, 588–597PubMedGoogle Scholar
  150. Lieberburg, I., MacLusky, N., & McEwen, B. S. (1980). Androgen receptors in the perinatal rat brain. Brain Research, 196, 125–138PubMedGoogle Scholar
  151. Lin, L.-F. H., Doherty, D. H., Lile, J. D., Bektesh, S., & Collins, E (1993). GDNF: A glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. &ience, 260, 1130–1132Google Scholar
  152. Lindzey, J., Kumar, M. V., Grossman, M., Young, C., & Tindall, D. J. (1994). Molecular mechanisms of androgen action. Vitamins and Hormones, 49, 383–432PubMedGoogle Scholar
  153. Lonstein, J. S., Simmons, D. A., Swann, J. M., & Stern, J. M. (1997). Forebrain expression of c fos due to active maternal behavior in lactating rats. Neuro&ience, 82, 267–281Google Scholar
  154. Lustig, R. H., Sudol, M., Pfaff, D. W., & Federoff, H. J. (1991). Estrogenic regulation and sex dimorphism of growth-associated protein 43 kDa (GAP-43) messenger RNA in the rat. Molecular Brain Research, 11, 125–132PubMedGoogle Scholar
  155. Lyet, L., Louis, F., Forest, M. G., Josso, N., Behringer, R. R., &Vigier, B. (1995). Ontogeny of reproductive abnormalities induced by deregulation of anti-Müllerian hormone expression in transgenic mice. Biology of Reproduction, 52, 444–454PubMedGoogle Scholar
  156. MacLusky, N. J., & Naftolin, F. (1981). Sexual differentiation of the central nervous system. Science, 211, 1294–1303PubMedGoogle Scholar
  157. MacLusky, N.J., Lieberburg, I., &Mc Ewen, B. S. (1979). The development of estrogen receptor systems in the rat brain: Perinatal development. Brain Research,178, 129–142PubMedGoogle Scholar
  158. MacLusky, N. J., Philip, A., Hurlburt, C., & Naftolin, F. (1985). Estrogen formation in the developing rat brain: Sex differences in aromatase activity during early post-natal life. Psychoneuroendocrinology, 10, 355–361PubMedGoogle Scholar
  159. MacLusky, N. J., Bowlby, D. A., Brown, T J., Peterson, R. E., & Hochberg, R. B. (1997). Sex and the developing brain: Suppression of neuronal estrogen sensitivity by developmental androgen exposure. Neurochemical Research, 22, 1395–1414PubMedGoogle Scholar
  160. Margulis, L., Sagan, D., & Olendzenski, L. (1985). What is sex? In H. O. Halvorson, & A. Monroy, (Eds.), The origin and evolution of sex (Vol. 7, pp. 67–86). New York: LissGoogle Scholar
  161. Martinou, J., Dubois-Dauphin, M., Staole, J. K., Rodriguez, I., Frankowski, H., Missotten, M., Albertini, P., Talabot, D., Catsicas, S., Pietro, C., & Huarte, J. (1994). Overexpression of BCL-2 in transgenic mice protects neurons from naturally occurring cell death and experimental i&hemia. Neuron, 13, 1017–1030PubMedGoogle Scholar
  162. Massagué, J. (1996). TGF signaling: Receptors, transducers, and Mad proteins. Cell, 85, 947–950PubMedGoogle Scholar
  163. Matsumoto, A., & Arai, Y. (1976). Effect of estrogen on early postnatal development of synaptic formation in the hypothalamic arcuate nucleus of female rats. Neuro&ience Letters, 2, 79–82Google Scholar
  164. Matsumoto, A., & Arai, Y. (1980). Sexual dimorphism in “wiring pattern” in the hypothalamic arcuate nucleus and its modification by neonatal hormonal environment. Brain Research, 190, 238–242PubMedGoogle Scholar
  165. Matsumoto, A., Micevych, P. E., &Arnold, A. P. (1988). Androgen regulates synaptic input to moto-neurons of the adult rat spinal cord. Journal of Neuro&ience, 8, 4168–4176Google Scholar
  166. Matsumoto, A., Arai, Y, Urano, A., & Hyodo, S. (1992). Effect of androgen on the expression of gap junction and 13-actin mRNAs in adult rat motoneurons. Neuro&ience Research, 14, 133–144PubMedGoogle Scholar
  167. Matsumoto, A., Arai, Y., & Hyodo, S. (1993). Androgenic regulation of expression of ß-tubulin messenger ribonucleic acid in motoneurons of the spinal nucleus of the bulbocavernosus. Journal of Neuroendocrinology, 5, 357–363PubMedGoogle Scholar
  168. Matthews, G., & Arnold, A. P. (1990). Antiestrogens fail to prevent the ma&uline ontogeny of the zebra finch song system. General and Comparative Endocrinology, 80, 48–58Google Scholar
  169. Maynard-Smith, J. (1978). The evolution of sex Cambridge: Cambridge University PressGoogle Scholar
  170. Mc Carthy, M. M., Schlenker, E. H., & Pfaff, D. W. (1993). Enduring consequences of neonatal treatment with antisense oligodeoxynucleotides to estrogen receptor messenger ribonucleic acid on sexual differentiation of rat brain. Endocrinology,133, 433–439PubMedGoogle Scholar
  171. Mc Ginnis, M. Y., & Katz, S E (1996). Sex differences in cytosolic androgen receptors in gonadectomized male and female rats. Journal of Neuroendocrinology, 8, 193–197PubMedGoogle Scholar
  172. Mc Millan, P. J., Singer, C., & Dorsa, D. M. (1996). The effects of ovariectomy and estrogen replacement on trkA and choline acetyltransferase mRNA expression in the basal forebrain of the adult female Sprague-Dawley rat. Journal of Neuro&ience, 16, 1860–1865Google Scholar
  173. Merry, D. E., & Korsmeyer, S. J. (1997). BCLr2 gene family in the nervous system. Annual Review of Neuro&ience, 20, 245–267Google Scholar
  174. Michael, R. P. (1965). Oestrogens in the central nervous system. British Medical Bulletin, 21, 87–90PubMedGoogle Scholar
  175. Miranda, R. C., Sohrabji, F., & Toran-Allerand, C. D. (1993). Presumptive estrogen target neurons express mRNAs for both the neurotrophins and neurotrophin receptors: A basis for potential developmental interactions of estrogen with the neurotrophins. Molecular and Cellular Neuro&iences, 4, 510–525Google Scholar
  176. Mishina, Y., Rey, R, Finegold, M. J., Matzuk, M. M., Josso, N., Cate, R. L., & Behringer, R R. (1996). Genetic analysis of the Müllerian-inhibiting substance signal transduction pathway in mammalian sexual differentiation. Genes and Development, 10, 2577–2587PubMedGoogle Scholar
  177. Mong, J. A., Kurzweil, R. L., Davis, A. M., Rocca, M. S., & Mc Carthy, M. M. (1996). Evidence for sexual differentiation of glia in rat brain. Hormones and Behavior, 30, 553–562PubMedGoogle Scholar
  178. Mosselman, S., Polman, J., & Dijkema, R. (1996). ER beta: Identification and characterization of a novel human estrogen receptor. l’EBS Letters, 392, 49–53Google Scholar
  179. Müller, H. W., Junghans, U., & Kappler, J. (1995). Astroglial neutrophic and neurite-promoting factors. Pharmacology and Therapeutics, 65, 1–18Google Scholar
  180. Murakami, S., & Arai, Y. (1989). Neuronal death in the developing sexually dimorphic periventricular nucleus of the preoptic area in the female rat: Effect of neonatal androgen treatment. Neuro&ience Letters, 102, 185–190 Google Scholar
  181. Nabekura, J., Oomura, Y., Minami, T., Mizuno, Y., & Fukuda, A. (1986). Mechanism of the rapid effect of 1713-estradiol on medial amygdala neurons. &ience, 233, 226–228Google Scholar
  182. Naftolin, E, Ryan, K. J., Davies, I.J., Reddy, V. V., Flores, F., Petor, Z., Kuhn, M., White, R.J., Takaoka, Y., & Wolin, L. (1975). The formation of estrogens by central neuroendocrine tissues. Recent Progress in Hormone Research, 31, 295–319PubMedGoogle Scholar
  183. Nelson K. G., Takahashi, T, Bossert, N. L, Walmer, D. K,, & McLachlan, J. A. (1991) Epidermal growth factor replaces estrogen in the stimulation of female genital-tract growth and differentiation. Proceedings of the National Academy of &iences of the USA, 88, 21–25Google Scholar
  184. Neri, R, Florance, K., Koziol, P., & Van Cleave, S. (1972). A biological profile of a nonsteroidal antiandrogen, &H 13521 (4’-nitro-3’-trifluoromethylisobutyranilide). Endocrinology, 91, 427–437PubMedGoogle Scholar
  185. Nishizuka, M., & Arai, Y. (1981). Sexual dimorphism in synaptic organization in the amygdala and its dependence on neonatal hormone environment. Brain Research,212, 31–38PubMedGoogle Scholar
  186. Nordeen, E. J., & Nordeen, K. W. (1988). Sex and regional differences in the incorporation of neurons born during song learning in zebra finches. Journal of Neuro&ience, 8, 2869–2874Google Scholar
  187. Nordeen, E. J., & Nordeen, K W. (1996). Sex difference among nonneuronal cells precedes sexually dimorphic neuron growth and survival in an avian song control nucleus. Journal of Neurobiology, 30, 531–542PubMedGoogle Scholar
  188. Nordeen, E. J., Nordeen, K. W., Sengelaub, D. R, & Arnold, A. P. (1985). Androgens prevent normally occurring cell death in a sexually dimorphic spinal nucleus, Science, 229, 671–673PubMedGoogle Scholar
  189. Nordeen, K. W., Nordeen, E. J., & Arnold, A. P. (1987). Estrogen accumulation in zebra finch song control nuclei: Implications for sexual differentiation and adult activation of song behavior. Journal of Neurobiology, 18, 569–582PubMedGoogle Scholar
  190. Nottebohm, F. (1981). A brain for all seasons: Cyclic anatomical changes in song control nuclei of the canary brain. &ience,214, 1368–1370Google Scholar
  191. Nottebohm, F., & Arnold, A. P. (1976). Sexual dimorphism in vocal control areas of the song bird brain. &ience, 194, 211–213Google Scholar
  192. Numan, M., Corodimas, K. P., Numan, M. J., Facotr, E. M., & Piers, W. D. (1988). Axon-sparing lesions of the preoptic region and substantia innominata disrupt maternal behavior in rats. Behavioral Neuro&ience, 102, 381–396Google Scholar
  193. Olmos, G., Naftolin, F., Perez, J., Tranque, P. A., & Garcia-Segura, L. M. (1989). Synaptic remodeling in the rat arcuate nucleus during the estrous cycle. Neuro&ience, 32, 663–667Google Scholar
  194. Oltvai, Z. N., Milliman, C. L., & Korsmeyer, S. J. (1993). Bc1–2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Ce14 74, 609–619Google Scholar
  195. O’Malley, B. W., &hrader, W. T., Mani, S., Smith, C., Weigel, N. L., Conneely, O. M., & Clark, J. H. (1995). An alternative ligand-independent pathway for activation of steroid receptors. Recent Progress in Hormone Research, 50, 333–347PubMedGoogle Scholar
  196. Oppenheim, R. W., Prevette, D., Tytell, M., & Homma, S. (1990). Naturally occurring and induced neuronal death in the chick embryo in vivo requires protein and RNA synthesis: Evidence for the role of cell death genes. Developmental Biology, 138, 104–113PubMedGoogle Scholar
  197. Ovt&haroff, W., Euster&hulte, B., Zienecker, R., Reisert, I., & Pilgrim, C. (1992). Sex differences in densities of dopaminergic fibers and GABAergic neurons in the prenatal rat striatum. Journal of Comparative Neurology, 323, 299–304Google Scholar
  198. Panzica, G. C., Viglietti-Panzica, C., Calacagni, M., Anselmetti, G. C., &humacher, M., & Balthazart, J. (1987). Sexual differentiation and hormonal control of the sexually dimorphic medial preoptic nucleus of the quail. Brain Research,416, 59–68PubMedGoogle Scholar
  199. Parducz, A., Szilagyi, T., Hoyk, S., Naftolin, F., & Garcia-Segura, L.-M. (1996). Neuroplastic changes in the hypothalamic arcuate nucleus: The estradiol effect is accompanied by increased exoendocytotic activity of neuronal membranes. Cellular and Molecular Neurobiology, 16, 259–269PubMedGoogle Scholar
  200. Paredes, R. G., & Baum, M. J. (1995). Altered sexual partner preference in male ferrets given excitotoxic lesions of the preoptic area/anterior hypothalamus. journal of Neuro&ience, 15, 6619–6630Google Scholar
  201. Park, J., Baum, M. J., Paredes, R. G., & Tobet, S. A. (1996). Neurogenesis and cell migration into the sexually dimorphic preoptic area/anterior hypothalamus of the fetal ferret. Journal of Neurobiology, 30, 315–328PubMedGoogle Scholar
  202. Pfaff, D. W. (1966). Morphological changes in the brains of adult male rats after neonatal castration. Journal of Endocrinology, 36, 415–416PubMedGoogle Scholar
  203. Pfaff, D. W., & Keiner, M. (1973). Atlas of estradiol-concentrating cells in the central nervous system of the female rat. Journal of Endocrinology, 151, 121–158Google Scholar
  204. Pfeiffer, C. A. (1936). Sexual differences of the hypophyses and their determination by the gonads. American Journal of Comparative Neurology,58, 195–225Google Scholar
  205. Phoenix, C. H., Goy, R. W., Gerall, A. A., & Young, W. C. (1959). Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology, 65, 369–382PubMedGoogle Scholar
  206. Pietras, R. J., & Szego, C. M. (1977). Specific binding sites for oestrogen at the outer surfaces of isolated endometrial cells. Nature, 205, 69–72Google Scholar
  207. Raisman, G., & Field, P. M. (1971). Sexual dimorphism in the preoptic area of the rat. Science,173, 731–733PubMedGoogle Scholar
  208. Raisman, G., & Field, P. M. (1973). Sexual dimorphism in the neuropil of the preoptic area and its dependence on neonatal androgen. Brain Research,54, 1–29PubMedGoogle Scholar
  209. Rakic, P. (1990). Principles of neural cell migration. Experienlia,46, 882–891Google Scholar
  210. Ramirez, V. D., & Zheng, J. (1996) Membrane sex-steroid receptors in the brain. Frontiers in Neuroendocrinology, 17, 402–439PubMedGoogle Scholar
  211. Rand, M. N., & Breedlove, S. M. (1995). Androgen alters the dendritic arbors of SNB motoneurons by acting upon their target mu&les. Journal of Neuro&ience, 15, 4408–4416Google Scholar
  212. Rasika, S., Nottebohm, F., & Alvarez-Buylla, A. (1994). Testosterone increases the recruitment and/or survival of the new high vocal center neurons in adult female canaries. Proceedings of the National Academy of &iences of the USA, 91, 7854–7858Google Scholar
  213. Reid, S. N. M., & Juraska, J. M. (1995). Sex differences in the number of synaptic junctions in the binocular area of the rat visual cortex. Journal of Comparative Neurology, 352, 560–566PubMedGoogle Scholar
  214. Reisert, I., & Pilgrim, C. (1991). Sexual differentiation of monoaminergic neurons—Genetic or epigenetic? Trends in Neuro&iences, 14, 468–473Google Scholar
  215. Reisert, I., &huster, R., Zienecker, R., & Pilgrim, C. (1990). Prenatal development of mesencephalic and diencephalic dopaminergic systems in the male and female rat. Developmental Brain Research, 53, 222–229PubMedGoogle Scholar
  216. Renfree, M. B., & Short, R. V. (1988). Sex determination in marsupials: Evidence for a marsupialeutherian dichotomy. Philosophical Transactions of the Royal Society of London, B322, 41–53Google Scholar
  217. Resko, J. A., Goy, R. W., & Phoenix, C. H. (1967). Uptake and distribution of exogenous testosterone-12 3H in neural and genital tissues of the castrate guinea pig. Endocrinology, 80, 490–498PubMedGoogle Scholar
  218. Rogers, L. C., Junier, M., Farmer, S. R., & Ojeda, S. R. (1991). A sex-related difference in the developmental expression of class II ß-tubulin messenger RNA in rat hypothalamus. Molecular and Cellular Neuro&iences, 2, 130–138Google Scholar
  219. Roof, R. L., & Havens, M. D. (1992). Testosterone improves maze performance and induces development of a male hippocampus in females. Brain Research,572, 310–313PubMedGoogle Scholar
  220. Roselli, C. E. (1991). Sex differences in androgen receptors and aromatase activity in microdissected regions of the rat brain. Endocrinology,128, 1310–1316PubMedGoogle Scholar
  221. Roselli, C. E., & Resko, J. A. (1993). Aromatase activity in the rat brain: Hormonal regulation and sex differences. Journal of Steroid Biochemistry and Molecular Biology, 44, 499–508PubMedGoogle Scholar
  222. Roselli, C. E., Ellinwood, W. E., & Resko, J. A. (1984). Regulation of brain aromatase activity in rats. Endocrinology,114, 192–200PubMedGoogle Scholar
  223. Rouiller-Fabre, V., Carmona, S., Merhi, R. A., Cate, R, Habert, R., & Vigier, B. (1998) Effect of antiMullerian hormone on Sertoli and Leydig cell functions in fetal and immature rats. Endocrinology,139, 1213–1220PubMedGoogle Scholar
  224. Ruel, T. D., Kelley, D. B., & Tobias, M. L. (1998). Facilitation at the sexually differentiated laryngeal synapse of Xenopus laevis. Journal of Comparative Physiology A, 182, 35–42Google Scholar
  225. Sachs, B. D., & Meisel, R. L. (1988). The physiology of male sexual behavior. In E. Knobil, & J. Neil (Eds.), The physiology of reproduction (pp. 1393–1485). New York: Raven PressGoogle Scholar
  226. Sar, M., & Parikh, I. (1986). Immunohistochemical localization of estrogen receptor in rat brain, pituitary and uterus with monoclonal antibodies. Journal of Steroid Biochemistry, 24, 409–442Google Scholar
  227. Sar, M., & Stumpf, W. E. (1975). Distribution of androgen-concentrating neurons in rat brain. In W. E. Stumpf, & L. D. Grant (Eds.), Anatomical neuroendocránology (pp. 120–133). Basel, Switzerland: KargerGoogle Scholar
  228. &hlinger, B. A., & Arnold, A. P. (1992a). Plasma sex steroids and tissue aromatization in hatchling zebra finches: Implications for the sexual differentiation of singing behavior. Endocrinology, 130, 289–299Google Scholar
  229. &hlinger, B. A., & Arnold, A. P. (1992b). Circulating estrogens in a male songbird originate in the brain. Proceedings of the National Academy of &iences of the USA, 89, 7650–7653Google Scholar
  230. &hlinger, B. A., & Arnold, A. P. (1993). Estrogen synthesis in vivo in the adult zebra finch—Additional evidence that circulating estrogens can originate in brain. Endocrinology, 133, 2610–2616PubMedGoogle Scholar
  231. &hmitt, E., Sane, A. T., Steyaert, A., Cimoli, G., & Bertrand, R. (1997). The Bel-xl and Bax-alpha control points: Modulation of apoptosis induced by cancer chemotherapy and relation to TPCK-protease and caspase activation. Biochemistry and Cell Biology, 75, 301–314PubMedGoogle Scholar
  232. &ott, W. J., & Holson, J. F. (1977). Weight differences in rat embryos prior to sexual differentiation. Journal of Embryology and Experimental Morphology, 40, 259–263PubMedGoogle Scholar
  233. Sellar, M. J., & Perkins-Cole, K. J. (1987). Sex difference in the mouse embryonic development at neurulation, Journal of Reproduction and Fertility, 79, 159–161Google Scholar
  234. Sharman, G. B., Robinson, E. S., Walton, S. M., & Berger, P. J. (1970). Sex chromosomes and reproductive anatomy of some intersex marsupials. Journal of Reproduction and Fertility, 21, 57–68PubMedGoogle Scholar
  235. Shaw, G., Renfree, M. B., Short, R. V., & O, W.-S. (1988). Experimental manipulation of sexual differen-tiation in wallaby pouch young treated with exogenous steroids. Development,104, 689–701PubMedGoogle Scholar
  236. Shaywitz, B. A., Shaywitz, S. E., Pugh, K R., Constable, R. T., Skudlarski, P., Fulbright, R. K, Bronen, R. A., Fletcher, J. M., Shankweller, D. P., Katz, L., & Gore, J. C. (1995). Sex differences in the functional organization of the brain for language. Nature, 373, 607–609PubMedGoogle Scholar
  237. Shea, T. B., Perrone-Bizzozero, N. I., Beermann, M. L., & Benowitz, L. I. (1991) Phospholipid-mediated delivery of anti-GAP-43 antibodies into neuroblastoma cells prevents neuriteogenesis. Journal of Neuro&ience, 11, 1685–1690Google Scholar
  238. Sherry, D. F., Jacobs, L. F., & Gaulin, S. J. C. (1992). Spatial memory and adaptive specialization of the hippocampus. Trends in Neuro&iences, 15, 298–303Google Scholar
  239. Shughrue, P. J., & Dorsa, D. M. (1993a). Gonadal steroids modulate the growth-associated protein CAP-43 (neuromodulin) mRNA in postnatal rat brain. Developmental Brain Research, 73, 123–132Google Scholar
  240. Shughrue, P.J., & Dorsa, D. M. (1993b). Estrogen modulates the growth-associated protein GAP-43 (neuromodulin) mRNA in the rat preoptic area and basal hypothalamus. Neuroendocrinology, 57, 439–447Google Scholar
  241. Siiteri, P. K, & Wilson, J. D. (1974). Testosterone formation and metabolism during male sexual differen-tiation in the human embryo. Journal of Clinical Endocrinology and Metabolism, 38, 113–125PubMedGoogle Scholar
  242. Simerly, R. B., Swanson, L. W., Hanna, R. J., & Gorski, R. A. (1985). Influence of perinatal androgen on the sexually dimorphic distribution of tyrosine hydrorylase-immunoreactive cells and fibers in the anteroventral periventricular nucleus of the rat. Neuroendocrinology, 40, 501–510PubMedGoogle Scholar
  243. Simerly, R. B., Chang, C., Muramatsu, M., & Swanson, L. W. (1990). Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: An in situ hybridization study. Journal of Comparative Neurology, 294, 76–95PubMedGoogle Scholar
  244. Simpson, H. B., & Vicario, D. S. (1991a). Early estrogen treatment alone causes female zebra finches to produce learned, male-like vocalizations. Journal of Neurobiology, 22, 755–776Google Scholar
  245. Simpson, H. B., & Vicario, D. S. (1991b). Early estrogen treatment of female zebra finches ma&ulinizes the brain pathway for learned vocalizations. Journal of Neurobiology, 22, 777–793Google Scholar
  246. Sinclair, A. H., Berta, P., Palmer, M. S., Hawkins, J. R., Griffiths, B. L., Smith, M. J., Foster, J. W., Fri&hauf, A., Lovell-Badge, R., & Goodfellow, P. N. (1990). A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature, 346, 240–244PubMedGoogle Scholar
  247. Sohrabji, F., Greene, L. A., Miranda, R. C., & Toran-Allerand, C. D. (1994). Reciprocal regulation of estrogen and NGF receptors by their ligands in PC12 cells. Journal of Neurobiology, 25, 974–988PubMedGoogle Scholar
  248. Springer, M. L., & Wade, J. (1997). The effects of testicular tissue and prehatching inhibition of estrogen synthesis on the development of courtship and copulatory behavior in zebra finches. Hormones and Behavior, 32, 46–59PubMedGoogle Scholar
  249. Stanley, H. F., & Fink, G. (1986). Synthesis of specific brain proteins is influenced by testosterone at mRNA level in the neonatal rat. Brain Research,370, 223–231PubMedGoogle Scholar
  250. Steimer, T., & Hutchison, J. B. (1990). Is androgen-dependent aromatase activity sexually differentiated in the rat and dove preoptic area? Journal of Neurobiology, 21, 787–795PubMedGoogle Scholar
  251. Stewart, J., Kuhnemann, S., & Rajabi, H. (1991). Neonatal exposure to gonadal hormones affects the development of monoamine systems in rat cortex. Journal of Endocrinology, 3, 85–93Google Scholar
  252. Sumida, H., Nishizuka, M., Kano, Y., & Arai, Y. (1993). Sex differences in the anteroventral periventricular nucleus of the preoptic area and in the related effects of androgen in prenatal rats. Neuro&ience Letters, 151, 41–44Google Scholar
  253. Swaab, D. F., & Fliers, E. (1985). A sexually dimorphic nucleus in the human brain. &ience, 228,1112–1115Google Scholar
  254. Tanapat, P, Hastings, N. B., Reeves, A. J., & Gould, E. (1999). Estrogen stimulates a transient increase in the number of new neurons in the dentate gyros of the adult female rat. Journal of Neuro&ience, 19, 5792–5801Google Scholar
  255. Taylor, B. J., & Truman, J. W. (1992). Commitment of abdominal neuroblasts in Drosophila to a male or female fate is dependent on genes of the sex-determining hierarchy. Development,114, 625–642PubMedGoogle Scholar
  256. Thornhill, J., & Halvorson, I. (1994). Activation of shivering and non-shivering thermogenesis by elec-trical stimulation of the lateral and medial preoptic areas. Brain Research,656, 367–374PubMedGoogle Scholar
  257. Tobet, S. A., & Fox, T. O. (1989). Sex-and hormone-dependent antigen immunoreactivity in developing rat hypothalamus. Proceedings of the National Academy of &iences of the USA, 86, 382–386Google Scholar
  258. Tobet, S. A., & Hanna, I. K. (1997). Ontogeny of sex differences in the mammalian hypothalamus and preoptic area. Cellular and Molecular Neurobiology, 17, 565–601PubMedGoogle Scholar
  259. Tobet, S. A., Baum, M. J., Tang, H. B., Shim, J. H., & Canick, J. A. (1985). Aromatase activity in the perinatal rat forebrain: Effects of age, sex, and intrauterine position. Developmental Brain Research, 23, 171–178Google Scholar
  260. Tobet, S. A., Zahniser, D. J., & Baum, M. J. (1986). Sexual dimorphism in the preoptic/anterior hypo-thalamic area of ferrets: Effects of adult exposure to sex steroids. Brain Research, 364, 249–257PubMedGoogle Scholar
  261. Tobet, S. A., Basham, M. E., & Baum, M. J. (1993). Estrogen receptor immunoreactive neurons in the fetal ferret forebrain. Developmental Brain Research, 72, 167–180PubMedGoogle Scholar
  262. Tobet, S. A., Chickering, T. W., Hanna, L, Crandall, J. E., & &hwarting, G. A. (1994). Can gonadal steroids influence cell position in the developing brain? Hormones and Behavior, 28, 320–327PubMedGoogle Scholar
  263. Tobet, S. A., Paredes, R. G., Chickering, T. W., & Baum, M. J. (1995). Telencephalic and diencephalic origin of radial glial processes in the developing preoptic area/anterior hypothalamus. Journal of Neurobiology, 26, 75–86PubMedGoogle Scholar
  264. Tobet, S. A., Henderson, R. G., Directo, C. O., & Dyer, B. V. (1997). Regional difference in cellular development in the preoptic area and anterior hypothalamus. Society for Neuro&ience Abstracts, 22, 344Google Scholar
  265. Tobias, M. L., Kelley, D. B. (1995). Sexual differentiation and hormonal regulation of the laryngeal synapse in Xenopus laevis. Journal of Neurobiology, 28, 515–526PubMedGoogle Scholar
  266. Tobias, M. L., & Kelley, D. B., & Ellisman, M. (1995). A sex difference in synaptic efficacy at the laryngeal neuromu&ular junction of Xenopus laevis. Journal of Neuro&ience, 15 1660–1668Google Scholar
  267. Toran-Allerand, C. D. (1976). Sex steroids and the development of the newborn mouse hypothalamus and preoptic area in vitro: Implications for sexual differentiation. Brain Research, 106 407–412PubMedGoogle Scholar
  268. Toran-Allerand, C. D. (1980). Sex steroids and the development of the newborn mouse hypothalamus and preoptic area in vitro II. Morphological correlates and hormonal specificity. Brain Research, 189 413–427PubMedGoogle Scholar
  269. Toran-Allerand, C. D., Gerlach, J. L., & McEwen B. S. (1980) Autoradiographic localization of [3H]estradiol related to steroid responsiveness in cultures of the newborn mouse hypothalamus and preoptic area. Brain Research, 184 517–522PubMedGoogle Scholar
  270. Toran-Allerand, C. D., Miranda, R. C., Bentham, W. D. L, Sohrabji, F., Brown, T. J., Hochberg, R. B., & MacLusky, N.J. (1992). Estrogen receptors colocalize with low-affinity nerve growth factor receptors in cholinergic neurons of the basal forebrain. Proceedings of the National Academy of &iences of the USA, 89 4668–4672Google Scholar
  271. Torres-Alemán, I., Rejas, M. T., Pons, S., & Garcia-Segura, L. M. (1992). Estradiol promotes cell shape changes and glial fibrillary acidic protein redistribution in hypothalamic astrocytes in vitro: A neuronal-mediated effect. Gu a, 6 180–187Google Scholar
  272. Towle, A. C., & Sze, R Y. (1983). Steroid binding to synaptic plasma membrane: Differential binding of glucocorticoids and gonadal steroids. Journal of Steroid Biochemistry, 18 135–143PubMedGoogle Scholar
  273. Ueyama, T., Mizuno, N., Takahashi, O., Nomura, S., Arakawa, H., & Matsushima, R. (1985). Central distribution of efferent and afferent components of the pudendal nerve in macaque monkeys. Journal of Comparative Neurology, 232 548–556PubMedGoogle Scholar
  274. Ulibarri, C., & Yahr, P. (1988). Role of neonatal androgens in sexual differentiation of brain structure, &ent marking and gonadotrophin secretion in gerbils. Behavioral and Neural Biology, 49 27–44PubMedGoogle Scholar
  275. Ulibarri, C. M., & Yahr, P. (1993). Ontogeny of the sexually dimorphic area of the gerbil hypothalamus. Developmental Brain Research 74, 14–24PubMedGoogle Scholar
  276. Ulibarri, C. P., Popper, P., & Micevych, P. E. (1995). Motoneurons dorsolateral to the central canal innervate perineal mu&les in the mongolian gerbil. Journal of Comparative Neurology, 356 225–237PubMedGoogle Scholar
  277. Uriel, J., Bouillon, D., & Dupiers, M. (1975). Affinity chromatography of human, rat and mouse alphafetoprotein on estradiol-Sepharose adsorbents. FEBS Letters 53, 305–308PubMedGoogle Scholar
  278. Valdivia, R. P. A., Kuneida, T., Azuma, S., & Toyoda, Y. (1993). PCR sexing and development rate differences in preimplantation mouse embryos fertilized and cultured in vitro. Molecular Reproduction and Development, 35 121–126Google Scholar
  279. Van Leeuwen, F. W., Caffé, A. R., & De Vries, G.J. (1985). Vasopressin cells in the bed nucleus of the stria terminalis of the rat: Sex differences and the influence of androgens. Brain Research, 325 391–394PubMedGoogle Scholar
  280. Vito, G. C., & Fox, T. O. (1979). Embryonic rodent brain contains estrogen receptors. &ience, 204 517–519Google Scholar
  281. Vito, C. C., Wieland, S.J., & Fox, T. O. (1979). Androgen receptors exist throughout the “critical period” of brain sexual differentiation. Nature, 282 308–310PubMedGoogle Scholar
  282. Wade, J., & Arnold, A. P. (1994). Post-hatching inhibition of aromatase activity does not alter sexual differentiation of the zebra finch song system. Brain Research, 693 347–350Google Scholar
  283. Wade, J., & Arnold, A. P. (1996). Functional testicular tissue does not ma&ulinize development of the zebra finch song system. Proceedings of the National Academy of &iences of the USA, 93 5264–5268Google Scholar
  284. Wade, J., &hlinger, B. A., & Arnold, A. P. (1995). Aromatase and 5ß-reductase activity in cultures of developing zebra finch brain: An investigation of sex and regional differences. Journal of Neurobiology, 27 240–251PubMedGoogle Scholar
  285. Wade, J., Springer, M. L., Wingfield, J. C., &Arnold, A. P. (1996). Neither testicular androgens nor embryonic aromatase activity alter morphology of the neural song system in zebra finches. Biology of Reproduction, 55 1126–1132PubMedGoogle Scholar
  286. Wagner, C. K., & Clemens, L. G. (1989). Anatomical organization of the sexually dimorphic perineal neuromu&ular system in the house mouse. Brain Research, 499 93–100PubMedGoogle Scholar
  287. Wagner, C. K., Nakayama, A. Y., & De Vries, G. J. (1998). Potential role of maternal progesterone in the sexual differentiation of the brain. Endocrinology, 139 3658–3661PubMedGoogle Scholar
  288. Wang, Z., Bullock, N. A., & De Vries, G. J. (1993). Sexual differentiation of vasopressin projections of the bed nucleus of the stria terminalis and medial amygdaloid nucleus in rats. Endocrinology 132,2299–2306PubMedGoogle Scholar
  289. Ward, I. (1992). Sexual behavior: The product of perinatal hormonal and prepubertal social factors. In A. Gerall, H. Moltz, & L. L. Ward. (Eds.), Handbook of Behavioral Neurobiology (pp. 157–180). New York: PlenumGoogle Scholar
  290. Watson, J. T., Robertson, J., Sachdev, U., & Kelley, D. B. (1993). Laryngeal mu&le and motor neuron plasticity in Xenopus laevix Testicular ma&ulinization of a developing neuromu&ular system. Journal of Neurobiology, 24 1615–1625PubMedGoogle Scholar
  291. Watson, N., Freeman, L., & Breedlove, S. M. (2001). Neuronal size in the spinal nucleus of the bulbocavernosus: Direct modulation by androgen in rats with mosaic androgen sensitivity. Journal of Neuro&ience, 211062–1066Google Scholar
  292. Weisz, J., & Ward, I. L. (1980). Plasma testosterone and progesterone titers of pregnant rats, their male and female fetuses, and neonatal offspring. Endocrinology, 106 306–316PubMedGoogle Scholar
  293. Welshons, W. J., & Russell, L. B. (1959). The Y-chromosome as the bearer of male determining factors in the mouse. Proceedings of the National Academy of &iences of the USA, 45 560–566Google Scholar
  294. Whalen, R E., & Etgen, A. M. (1978). Ma&ulinization and defeminization induced in female hamsters by neonatal treatment with estradiol benzoate and RU-2858. Hormones and Behavior, 10, 170–177PubMedGoogle Scholar
  295. Williams, C. L., & Meck, W. H. (1991). The organizational effects of gonadal steroids on sexually dimorphic spatial ability. Psychoneuroendocrinology, 16 155–176PubMedGoogle Scholar
  296. Williams, N. (1995). Tracing how the sexes develop. &ience, 269 1822–1827Google Scholar
  297. Wilson, J. D., George, E W., & Griffin, J. E. (1981). The hormonal control of sexual development. &ience, 211 1278–1284Google Scholar
  298. Wimer, R. E., & Wimer, C. (1985). Three sex dimorphisms in the granule cell layer of the hippocampus in house mice. Brain Research, 328 105–109PubMedGoogle Scholar
  299. Wong, M., & Moss, R. L. (1991). Electrophysiological evidence for a rapid membrane action of the gonadal steroid, 171-estradiol, on CAl pyramidal neurons of the rat hippocampus. Brain Research, 543 148–152PubMedGoogle Scholar
  300. Woolley, C. S., Gould, E., Frankfurt, M., & Mc Ewen, B. S. (1990). Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. Journal of Neuro&ience, 10 4035–4039Google Scholar
  301. Xu, J., & Forger, N. G. (1998) Expression and androgen regulation of the ciliary neurotrophic factor receptor (CNTFRa) in mu&les and spinal cord. Journal of Neurobiology, 35 217–225PubMedGoogle Scholar
  302. Yalcinkaya, T. M., Siiteri, P., Vigne, J., Licht, P., Pavgi, S., Frank, L. G., & Glickman, S. E. (1993). A mechanism for virilization of female spotted hyenas in utero. &ience, 260 1929–1931Google Scholar
  303. Zhou, L., Blaustein, J. D., & De Vries, G.J. (1994). Distribution of androgen receptor immunoreactivity in vasopressin-and oxytocin-immunoreactive neurons in the male rat brain. Endocrinology, 134 2622–2627PubMedGoogle Scholar
  304. Zwingman, T., Erickson, R. P., Boyer, T., & Ao, A. (1993). Tran&ription of the sex-determining region genes Sry and Zfy in the mouse preirnplantation embryo. Proceedings of the National Academy of &iences of the USA, 90 814–817Google Scholar

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© Springer Science+Business Media New York 2001

Authors and Affiliations

  • Nancy G. Forger
    • 1
  1. 1.Department of Psychology and Center for Neuroendocrine StudiesUniversity of MassachusettsAmherst

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