Neurobiology pp 180-202 | Cite as

Searching for Neural Correlates of Sexual Differentiation in a Heterogeneous Tissue

Part of the Proceedings in Life Sciences book series (LIFE SCIENCES)


Nearly 20 years have passed since the hypothalamus-preoptic area (HPOA) was identified as a target tissue mediating the effects of gonadal steroids on male and female sexual behaviour (Davidson and Bloch 1969; Eisenfeld and Axelrod 1965; Lisk 1962, 1967; Harris and Michael 1964). Since then our knowledge of how HPOA cells accumulate and metabolize steroids has rapidly progressed. We know, for example, that HPOA cells that respond to testosterone (T) often convert it first to oestradiol (OE2) and/or di- hydrotestosterone (DHT; Luttge 1979, Martini 1982). These metabolites then bind to intracellular receptors. In this regard, T-sensitive cells in the HPOA resemble T-sensitive cells in the male reproductive tract. In females, HPOA cells that respond to progesterone (P) resemble P-sensitive cells in the female reproductive tract in that they synthesize most of their P receptors only after they have been exposed to OE2 (Blaustein and Brown, this Vol.; Moguilewski and Raynaud 1979a,b; MacLusky and McEwen 1978, 1980). The receptors themselves are similar in the HPOA and peripheral targets (Barley et al. 1975; Feder et al. 1979; Moguilewsky and Raynaud 1979a), and in both tissues, the steroid eventually binds to acceptor sites on the chromatin (Fox and Johnston 1974; Whalen and Olsen 1978). Moreover, these processes are similar in adults and neonates (MacLusky and Naftolin 1981). These observations have encouraged the view that steroids activate mating behaviour in adulthood, and sexually differentiate the HPOA during early development, in the same way that they modify cellular functions in other parts of the body, i.e., by modifying synthesis of messenger RNA and protein.


Sexual Differentiation Neural Correlate Gonadal Steroid Heterogeneous Tissue Corpus Luteum 
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  1. Adkins-Regan E (1981) Early organizational effects of hormones: an evolutionary perspective. In: Adler NT (ed) Neuroendocrinology of reproduction physiology and behavior. Plenum, New York London, p 159Google Scholar
  2. Alberts B, Bray D, Lewis J, Roff M, Roberts K, Watson JD (1983) Molecular biology of the cell. Garland, New YorkGoogle Scholar
  3. Arendash GW, Gorski RA (1983) Effects of discrete lesions of the sexually dimorphic nucleus of the preoptic area or other medial preoptic regions on the sexual behavior of male rats. Brain Res Bull 10:147–154PubMedGoogle Scholar
  4. Atz JW (1964) Intersexuality in fishes. In: Armstrong CN, Marshall AJ (eds) Intersexuality in vertebrates including man. Academic, New York, p 145Google Scholar
  5. Ayoub DM, Greenough WT, Juraska JM (1983) Sex differences in dendritic structure in the preoptic area of the juvenile macaque monkey brain. Science (Wash DC) 219:197–198Google Scholar
  6. Barley J, Ginsburg M, Greenstein BD, MacLusky NJ, Thomas PJ (1975) An androgen receptor in rat brain and pituitary. Brain Res 100:383–393PubMedGoogle Scholar
  7. Baum MJ (1979) Differentiation of coital behavior in mammals: a comparative analysis. Neurosci Biobehav Rev 3:265–284PubMedGoogle Scholar
  8. Baum MJ, Gallagher CA (1981) Increasing dosages of estradiol benzoate activate equivalent degrees of sexual receptivity in gonadectomized male and female ferrets. Physiol Behav 26:751–753PubMedGoogle Scholar
  9. Beach FA (1976) Sexual attractivity, proceptivity, and receptivity in female mammals. Horm Behav 7:105–138PubMedGoogle Scholar
  10. Beach FA, Buehler MG (1977) Male rats with inherited insensitivity to androgen show reduced sexual behavior. Endocrinology 100:197–200PubMedGoogle Scholar
  11. Bishop W, Kalra PS, Fawcett CP, Krulich L, McCann SM (1972) The effects of hypothalamic lesions on the release of gonadotropins and prolactin in response to estrogen and progesterone treatment in female rats. Endocrinology 91:1404–1410PubMedGoogle Scholar
  12. 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. J Comp Neurol 212: 118–130PubMedGoogle Scholar
  13. Breedlove SM, Arnold AP (1981) Sexually dimorphic motor nucleus in the rat lumbar spinal cord: response to adult hormone manipulation, absence in androgen-insensitive rats. Brain Res 225: 297–307PubMedGoogle Scholar
  14. Brown RE (1977) Odor preference and urine-marking scales in male and female rats: effects of gonadectomy and sexual experience on responses to conspecific odors. J Comp Physiol Psychol 91:1190–1206Google Scholar
  15. Brown RE (1978) Hormonal control of odor preferences and urine-marking in male and female rats. Physiol Behav 20:21–24PubMedGoogle Scholar
  16. Christensen LW, Gorski RA (1978) Independent masculinization of neuroendocrine systems by intracerebral implants of testosterone or estradiol in the neonatal female rat. Brain Res 146: 325–340PubMedGoogle Scholar
  17. Gemens LG, Gladue BA, Coniglio LP (1978) Prenatal endogenous androgenic influences on masculine sexual behavior and genital morphology in male and female rats. Horm Behav 10:40–53Google Scholar
  18. Cohen RS, Pfaff DW (1981) Ultrastructure of neurons in the ventromedial nucleus of the hypothalamus in ovariectomized rats with or without estrogen treatment. Cell Tissue Res 217:451–470PubMedGoogle Scholar
  19. Commins D, Yahr P (1984a) Adult testosterone levels influence to the morphology of a sexually dimorphic area in the Mongolian gerbil brain. J Comp Neurol 224:132–140PubMedGoogle Scholar
  20. Commins D, Yahr P (1984b) Acetylcholinesterase activity in the sexually dimorphic area of the gerbil brain: sex differences and influences of adult gonadal steroids. J Comp Neurol 224:123–131PubMedGoogle Scholar
  21. Commins D, Yahr P (1984c) Lesions of the sexually dimorphic area disrupt mating and marking in male gerbils. Brain Res Bull 13:185–193PubMedGoogle Scholar
  22. Commins D, Yahr P (1985) Autoradiographic localization of estrogen and androgen receptors in the sexually dimorphic area and other regions of the gerbil brain. J Comp Neurol 231:473–489PubMedGoogle Scholar
  23. Corballis MC, Morgan JJ (1978) On the biological basis of human laterality I. Evidence for a maturational left-right gradient Behav Brain Sci 2:261–336Google Scholar
  24. Davidson JM, Bloch GJ(1969) Neuroendocrine aspects of male reproduction. Biol Reprod 1:67–92Google Scholar
  25. Davis PG, Barfield RJ (1979a) Activation of masculine sexual behavior by intracranial estradiol benzoate implants in male rats. Neuroendocrinology 28:217–227PubMedGoogle Scholar
  26. Davis PG, Barfield RJ (1979b) Activation of feminine sexual behavior in castrated male rats by intrahypothalamic implants of estradiol benzoate. Neuroendocrinology 28:228–233PubMedGoogle Scholar
  27. Davis PG, Chaptal CV, McEwen BS (1979a) Independence of the differentiation of masculine and feminine sexual behavior in rats. Horm Behav 12:12–19PubMedGoogle Scholar
  28. Davis PG, McEwen BS, Pfaff DW (1979b) Localized behavioral effects of tritiated estradiol implants in the ventromedial hypothalamus of female rats. Endocrinology 104:898–903PubMedGoogle Scholar
  29. DeBold JF (1978) Modification of nuclear retention of [H] estradiol by cells of the hypothalamus as a function of early hormone experience. Brain Res 159:416–420PubMedGoogle Scholar
  30. DeBold JF, Whalen RE (1975) Differential sensitivity of mounting and lordosis control systems to early androgen treatment in male and female hamsters. Horm Behav 6:197–209PubMedGoogle Scholar
  31. DeVoogd T, Nottebohm F (1981) Gonadal hormones induce dendritic growth in the adult avian brain. Science (Wash DC) 214:202–204Google Scholar
  32. Dohler KD, Coquelin A, Davis F, Hines M, Shryne JE, Gorski RA (1982) Differentiation of the sexually-dimorphic nucleus in the preoptic area of the rat brain is determined by the perinatal hormone environment. Neurosci Lett 33:295–298PubMedGoogle Scholar
  33. Eisenfeld AJ, Axelrod J (1965) Selectivity of estrogen distribution in tissues. J Pharmacol Exp Ther 150:469–475PubMedGoogle Scholar
  34. Feder HH (1981) Hormonal actions on the sexual differentiation of the genitalia and gonadotropin- regulating systems. In: Adler NT (ed) Neuroendocrinology of reproduction: physiology and behavior. Plenum, New York, p 89Google Scholar
  35. Feder HH, Landau IT, Walker WA (1979) Anatomical and biochemical substrates of the actions of estrogens and antiestrogens on brain tissues that regulate female sex behavior of rodents. In: Beyer C (ed) Endocrine control of sexual behavior. Raven, New York, p 317Google Scholar
  36. Fox TO (1975) Androgen- and estrogen-binding macromolecules in developing mouse brain: biochemical and genetic evidence. Proc Nat Acad Sci USA 72:4303–4307PubMedGoogle Scholar
  37. Fox TO, Johnston C (1974) Estradiol receptors from mouse brain and uterus: binding to DNA. Brain Res 77:330–336PubMedGoogle Scholar
  38. Gentry RT, Wade GN (1976) Sex differences in sensitivity of food intake, body weight, and running- wheel activity to ovarian steroids in rats. J Comp Physiol Psychol 90:747–754PubMedGoogle Scholar
  39. Gerendai I, Rotsztejn W, Marchetti B, Kordon C, Scapagini U (1978) Unilateral ovariectomy-induced luteinizing hormone-releasing hormone content changes in the two halves of the mediobasal hypothalamus. Neurosci Lett 9:333–336PubMedGoogle Scholar
  40. Goldfoot DA, Feder HH, Goy RW (1969) Development of bisexuality in the male rat treated neonatally with androstenedione. J Comp Physiol Psychol 67:41–45PubMedGoogle Scholar
  41. Goldman SA, Nottebohm F (1983) Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. Proc Nat Acad Sei USA 80:2390–2394Google Scholar
  42. Goodman RL (1978) The site of the positive feedback action of estradiol in the rat. Endocrinology 102:151–159PubMedGoogle Scholar
  43. Gorski RA, Gordon JH, Shryne JE, Southam AM (1978) Evidence for a morphological sex difference within the medial preoptic area of the rat. Brain Res 148:333–346PubMedGoogle Scholar
  44. Gorski RA, Harlan RE, Jacobson CD, Shryne JE, Southam M (1980) Evidence for the existence of a sexually dimorphic nucleus in the preoptic area of the rat. J Comp Neurol 193:529–539PubMedGoogle Scholar
  45. Goy RW, Goldfoot DA (1975) Neuroendocrinology: animal models and problems of human sexuality. Arch Sex Behav 4:405–420PubMedGoogle Scholar
  46. Goy RW, McEwen BS (1980) Sexual differentiation of the brain. MIT Press, CambridgeGoogle Scholar
  47. Grant LD, Bissette G, Nemeroff CB (1984) Distribution of peptides in the central nervous system. In: Nemeroff CB, Dunn AJ (eds) Peptides, hormones, and behavior. Spectrum, Jamaica, p 37Google Scholar
  48. Greenough WT, Carter CS, Steerman C, DeVoogd TJ (1977) Sex differences in dendritic patterns in hamster preoptic area. Brain Res 126:63–72PubMedGoogle Scholar
  49. Griffiths EC, Hooper KC, Jeffcoate SL, Holland DT (1975) The effects of gonadectomy and gonadal steroids on the activity of hypothalamic peptidases inactivating luteinizing hormone-releasing hormone (LH-RH). Brain Res 88:384–388PubMedGoogle Scholar
  50. Harris GW, Michael RP (1964) The activation of sexual behaviour by hypothalamic implants of oestrogen. J Physiol (Lond) 17:275–301Google Scholar
  51. Hart BL (1974) Medial preoptic-anterior hypothalamic area and the sociosexual behavior of male dogs: a comparative neuropsychological analysis. J Comp Physiol Psychol 86:328–349PubMedGoogle Scholar
  52. Hart BL, Voith VL (1978) Changes in urine spraying, feeding, and sleep behavior of cats following medial pre optic-anterior hypothalamic lesions. Brain Res 145:406–409PubMedGoogle Scholar
  53. Hayashi S (1976) Sterilization of female rats by neonatal placement of estradiol micropellets in anterior hypothalamus. Endocrinol J 23:55–60Google Scholar
  54. Heimer L, Larsson K (1966/67) Impairment of mating behavior in male rats following lesions in the pre optic-anterior hypothalamic continuum. Brain Res 3:248–263Google Scholar
  55. Hlinak Z, Madlafousek J, Mohapelova A (1979) Initiation of copulatory behavior in castrated male rats injected with critically adjusted doses of testosterone. Horm Behav 13:9–20PubMedGoogle Scholar
  56. Kalra PS, McCann SM (1975) The stimulatory effect on gonadotropin release of implants of estradiol or progesterone in certain sites in the central nervous system. Neuroendocrinology 19: 289–302PubMedGoogle Scholar
  57. Kelley DB, Pfaff DW (1978) Generalizations from comparative studies on neuroanatomical and endocrine mechanisms of sexual behaviour. In: Hutchison JB (ed) Biological determinants of sexual behaviour. Wiley, Chichester, p 225Google Scholar
  58. King WJ, Green GL (1984) Monoclonal antibodies localize oestrogen receptor in the nuclei of target cells. Nature (Lond) 307:745–747Google Scholar
  59. LaVelle A (1951) Nucleolar changes and development of Nissl substance in the cerebral cortex of fetal guinea pigs. J Comp Neurol 94:453–467PubMedGoogle Scholar
  60. LaVelle A (1956) Nucleolar and Nissl substance development in nerve cells. J Comp Neurol 104: 175–201PubMedGoogle Scholar
  61. Lieberburg I, McEwen BS (1977) Brain cell nuclear retention of testosterone metabolites, 5a-di-hydrotestoster one and estradiol-17/3, in adult male rats. Endocrinology 100:588–597PubMedGoogle Scholar
  62. Lieberburg I, MacLusky N, McEwen BS (1980) Cytoplasmic and nuclear estradiol-l7/3 binding in male and female rat brain: regional distribution, temporal aspects and metabolism. Brain Res 193:487–503PubMedGoogle Scholar
  63. Lisk RD (1962) Diencephalic placement of estradiol and sexual receptivity in the female rat. Am J Physiol 203:493–496PubMedGoogle Scholar
  64. Lisk RD (1967) Neural localization for androgen activation of copulatory behavior in the male rat. Endocrinology 80:754–761PubMedGoogle Scholar
  65. Luine VN, McEwen BS (1983) Sex differences in cholinergic enzymes of diagonal band nuclei in the rat preoptic area. Neuroendocrinology 36:475–482PubMedGoogle Scholar
  66. Luine VN, Rhodes JC (1983) Gonadal hormone regulation of MAO and other enzymes in hypothalamic areas. Neuroendocrinology 36:235–241PubMedGoogle Scholar
  67. Luine VN, Khylchevskaya RI, McEwen BS (1974) Oestrogen effects on brain and pituitary enzyme activities. J Neurochem 23:925–934PubMedGoogle Scholar
  68. Luine VN, McEwen BS, Black IB (1977) Effect of 17/3-estradiol on hypothalamic tyrosine hydroxylase activity. Brain Res 120:188–192PubMedGoogle Scholar
  69. Luttge WG (1979) Endocrine control of mammalian male sexual behavior: an analysis of the potential role of testosterone metabolites. In: Beyer C (ed) Endocrine control of sexual behavior. Raven, New York, p 341Google Scholar
  70. MacLusky NJ, McEwen BS (1978) Oestrogen modulates progestin receptor concentrations in some brain regions and not others. Nature (Lond) 274:276–277Google Scholar
  71. MacLusky NJ, McEwen BS (1980) Progestin receptors in rat brain: distribution and properties of cytoplasmic progestin binding sites. Endocrinology 106:192–202PubMedGoogle Scholar
  72. MacLusky NJ, Naftolin F (1981) Sexual differentiation of the central nervous system. Science (Wash DC) 211:1294–1303Google Scholar
  73. Madlafousek J, Hlinak Z, Beran J (1976) Decline of sexual behavior in castrated male rats: effects of female precopulatory behavior. Horm Behav 7:245–252PubMedGoogle Scholar
  74. Marrone BL, Feder HH (1977) Characteristics of (H)estrogen and H)progestin uptake and effects of progesterone on (H)estrogen uptake in brain, anterior pituitary and peripheral tissues of male and female guinea pigs. Biol Reprod 17:42–57PubMedGoogle Scholar
  75. Martini L (1982) The 5a-reduction of testosterone in the neuroendocrine structures. Biochemical and physiological implications. Endocr Rev 3:1–15PubMedGoogle Scholar
  76. Mathews D, Edwards DA (1977) Involvement of the ventromedial and anterior hypothalamic nuclei in the hormonal induction of receptivity in the female rat. Physiol Behav 19:319–326PubMedGoogle Scholar
  77. Matsumoto A, Arai Y (1983) Sex difference in volume of the ventromedial nucleus of the hypothalamus in the rat. Endocrinol Jpn 30:277–280PubMedGoogle Scholar
  78. Maurer RA, Woolley DE (1974) Demonstration of nuclear H-estradiol binding in hypothalamus and amygdala of female, androgenized-female and male rats. Neuroendocrinology 16:137–147PubMedGoogle Scholar
  79. McEwen BS (1981) Neural gonadal steroid actions. Science (Wash DC) 211:1303–1311Google Scholar
  80. Meisel RL, Ward IL (1981) Fetal female rats are masculinized by male httermates located caudally in the uterus. Science (Wash DC) 213:239–242Google Scholar
  81. Moguilewsky M, Raynaud JP (1979a) Estrogen-sensitive progestin-binding sites in the female rat brain and pituitary. Brain Res 164:165–175PubMedGoogle Scholar
  82. Moguilewsky M, Raynaud JP (1979b) The relevance of hypothalamic and hypophyseal progestin receptor regulation in the induction and inhibition of sexual behavior in the female rat. Endocrinology 105:516–522PubMedGoogle Scholar
  83. Morrell JI, Pfaff DW (1982) Characterization of estrogen-concentrating hypothalamic neurons by their anoxal projections. Science (Wash DC) 217:1273–1276Google Scholar
  84. Nance DM, Moger WH (1982) Ipsilateral hypothalamic deafferentiation blocks the increase in serum FSH foUowing hemicastration. Brain Res Bull 8:299–302PubMedGoogle Scholar
  85. Nance DM, Christensen LW, Shryne JE, Gorski RA (1977) Modifications in gonadotropin control and reproductive behavior in the female rat by hypothalamic and preoptic lesions. Brain Res Bull 2:307–312PubMedGoogle Scholar
  86. Nance DM, White JP, Moger WH (1983) Neural regulation of the ovary: evidence for hypothalamic asymmetry in endocrine control. Brain Res Bull 10:353–355PubMedGoogle Scholar
  87. Neill JD (1972) Sexual differences in the hypothalamic regulation of prolactin secretion. Endocrinology 90:1154–1159PubMedGoogle Scholar
  88. Nordeen EJ, Yahr P (1982) Hemispheric asymmetries in the behavioral and hormonal effects of sexually differentiating mammalian brain. Science (Wash DC) 218:391–394Google Scholar
  89. Nordeen EJ, Yahr P (1983) A regional analysis of estrogen binding to hypothalamic cell neclei in relation to masculinization and defeminization. J Neurose 3:933–941Google Scholar
  90. Nottebohm F (1980) Testosterone triggers growth of brain vocal control nuclei in adult female canaries. Brain Res 189:429–436PubMedGoogle Scholar
  91. Nottebohm F (1981) A brain for all seasons: cyclical anatomical changes in song control neclei of the canary brain. Science (Wash DC) 214:1368–1370Google Scholar
  92. Nottebohm F, Arnold AP (1976) Sexual dimorphism in vocal control areas of the songbird brain. Science (Wash DC) 194:211–213Google Scholar
  93. Numan M, Rosenblatt JS, Komisaruk BR (1977) Medial preoptic area and onset of maternal behavior in the rat. J Comp Physiol Psychol 91:146–164PubMedGoogle Scholar
  94. Ogren L, Vertes M, Woolley D (1976) In vivo nuclear H-estradiol binding in brain areas of the rat: reduction by endogenous and exogenous androgens. Neuroendocrinology 21:350–365PubMedGoogle Scholar
  95. Olsen KL (1979) Androgen-sensitive rats are defeminized by their testes. Nature (Lond) 279:238–239Google Scholar
  96. Olsen KL, Whalen RE (1980) Sexual differentiation of the brain: effects on mating behavior and [H] estradiol binding by hypothalamic chromatin in rats. Biol Reprod 22:1068–1072PubMedGoogle Scholar
  97. Olsen KL, Whalen RE (1981) Hormonal control of the development of sexual behavior in androgen- insensitive (tfm) rats. Physiol Behav 27:883–886PubMedGoogle Scholar
  98. Palay SL, Palade GE (1955) The fine structure of neurons. J Biochem Biophys Cytol 1:69–88Google Scholar
  99. Palkovits M (1973) Isolated removal of hypothalamic or other brain nuclei of the rat. Brain Res 59:449–450PubMedGoogle Scholar
  100. Pfaff DW (1970) Nature of sex hormone effects on rat sex behavior: specificity of effects and individual patterns of response. J Comp Physiol Psychol 73:349–358PubMedGoogle Scholar
  101. Pfaff DW, Zigmond RE (1971) Neonatal androgen effects on sexual and non-sexual behavior of adult rats tested under various hormone regimes. Neuroendocrinology 7:129–145PubMedGoogle Scholar
  102. Price EO (1975) Hormonal control of urine-marking in wild and domestic Norway rats. Horm Behav 6:393–397PubMedGoogle Scholar
  103. Rainbow TC, Davis PG, McEwen BS (1980a) Anisomycin inhibits the activation of sexual behavior by estradiol and progesterone. Brain Res 194:548–555PubMedGoogle Scholar
  104. Rainbow TC, Degroff V, Luine VN, McEwen BS (1980b) Estradiol11 ß increases the number of muscarinic receptors in hypothalamic nuclei. Brain Res 198:239–243PubMedGoogle Scholar
  105. Rainbow TC, Parsons B, McEwen BS (1982) Sex differences in rat brain oestrogen and progestin receptors. Nature (Lond) 300:648–649Google Scholar
  106. Raisman G, Field PM (1971) Sexual dimorphism in the preoptic area of the rat. Science (Wash DC) 173:731–733Google Scholar
  107. Raisman G, Field PM (1973) Sexual dimorphism in the neuropil of the preoptic area and its dependence on neonatal androgen. Brain Res 54:1–29PubMedGoogle Scholar
  108. Rubin BS, Barfield RJ (1980) Priming of estrous responsiveness by implants of H/J-estradiol in the ventromedial hypothalamic nucleus of female rats. Endocrinology 106:504–509PubMedGoogle Scholar
  109. Rubin BS, Barfield RJ (1983a) Progesterone in the ventromedial hypothalamus facilitates estrous behavior in ovariectomized, estrogen-primed rats. Endocrinology 113:797–804PubMedGoogle Scholar
  110. Rubin BS, Barfield RJ (1983b) Induction of estrous behavior in ovariectomized rats by sequential replacement of estrogen and progesterone to the ventromedial hypothalamus. Neuroendocrinology 37:218–224PubMedGoogle Scholar
  111. Sawchenko PE, Swanson LW (1982) Immunohistochemical identification of neurons in the paraventricular nucleus of the hypothalamus that project to the medulla or to the spinal cord in the rat. J Comp Neurol 205:260–272PubMedGoogle Scholar
  112. Scouten CW, Burrell L, Palmer T, Cegavske CE (1980) Lateral projections of the medial preoptic area are necessary for androgenic influence on urine marking and copulation in rats. Physiol Behav 25:237–241PubMedGoogle Scholar
  113. Stern JJ (1969) Neonatal castration, androstenedione, and the mating behavior of the male rat. J Comp Physiol Psychol 64:608–612Google Scholar
  114. Swanson LW (1977) Immunohistochemical evidence for a neurophysin-containing autonomic pathway arising in the paraventricular nucleus of the hypothalamus. Brain Res 128:346–353PubMedGoogle Scholar
  115. Swanson LW, Kuypers HGJM (1980) The paraventricular nucleus of the hypothalamus: cytoarchi- tectonic subdivisions and the organization of projections to the pituitary, dorsal vagal complex and spinal cord as demonstrated by retrograde fluorescence double-labelling methods. J Comp Neurol 194:555–570PubMedGoogle Scholar
  116. Swanson LW, McKellar S (1979) The distribution of oxytocin- and neurophysin-stained fibers in the spinal cord of the rat and monkey. J Comp Neurol 188:87–106PubMedGoogle Scholar
  117. Swanson LW, Sawchenko PE (1983) Hypothalamic integration: organization of the paraventricular and supraoptic nuclei. Annu Rev Neurosci 6:269–324PubMedGoogle Scholar
  118. Wade GN, Zucker I (1970) Modulation of food intake and locomotor activity in female rats by diencephalic hormone implants. J Comp Physiol Psychol 72:328–336PubMedGoogle Scholar
  119. Wallis CJ, Luttge WG (1980) Influence of estrogen and progesterone on glutamic acid decarboxylase activity in discrete regions of rat brain. J Neurochem 34:609–613PubMedGoogle Scholar
  120. Welshons WV, Lieberman ME, Gorski J (1984) Nuclear localization of unoccuppied oestrogen receptors. Nature (Lond) 307:747–749Google Scholar
  121. Whalen RE (1974) Sexual differentiation: models, methods, and mechanisms. In: Friedman RC, Richart RM, Vande Wiele RL (eds) Sex differences in behavior. Wiley, New York, p 467Google Scholar
  122. Whalen RE, Massicci J (1975) Subcellular analysis of the accumulation of estrogen by the brain of male and female rats. Brain Res 89:255–264PubMedGoogle Scholar
  123. Whalen RE, Olsen KL (1978) Chromatin binding of estradiol in the hypothalamus and cortex of male and female rats. Brain Res 152:121–131PubMedGoogle Scholar
  124. Whalen RE, Luttge WG, Gorzalka BB (1971) Neonatal androgenization and the development of estrogen responsivity in male and female rats. Horm Behav 2:83–90Google Scholar
  125. Wüson JD, George FW, Griffin JE (1981) The hormonal control of sexual development. Science (Wash DC) 211:1278–1284Google Scholar
  126. Yahr P (1977) Central control of scent marking. In: Muller-Schwarze D, Mozell MM (eds) Chemical signals in vertebrates. Plenum, New York, p 547Google Scholar
  127. Yahr P (1983) Hormonal influences on territorial marking behavior. In: Svare BB (ed) Hormones and aggressive behavior. Plenum, New York, p 145Google Scholar

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© Springer-Verlag Berlin Heidelberg 1985

Authors and Affiliations

  • P. Yahr
    • 1
  1. 1.Department of PsychobiologyUniversity of CaliforniaIrvineUSA

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