Archives of Sexual Behavior

, Volume 3, Issue 1, pp 51–90 | Cite as

Fetal hormones, the Brain, and human sex differences: A heuristic, integrative review of the recent literature

  • June M. Reinisch


Many investigators of sex differences have suggested that underlying physiological-biological factors probably account, at least in part, for some of the sexually dimorphic behaviors identified in humans. Although few have conjectured as to the specific nature of the mechanism mediating these differential tendencies, the evidence reported here from animal behavior experiments, brain studies, and human clinical syndromes strongly suggests that it is the presence or absence of androgen during the period critical for the organization and differentiation of the human brain that is the operative agent. Further, it is necessary to qualify the hypothesis by placing it in proper perspective in terms of the many influential postnatal factors. Psychosexual differentiation must be understood as an end result or complex of various component factors and not as a single or global entity (Money and Ehrhardt, 1968). The data presented clearly compel the conclusion that a fetal hormonal effect is influential in the subsequent development of sex differences, but in most cases its effect must be seen as limited in scope and of a diffuse quality rather than directly related to specific behaviors. In view of the evidence from the animal experiments that the nature of the mammalian genetic constitution is a “plastic, pluripotential matrix, highly susceptible to shaping and selection by environmental influences such as hormones” (Goy, 1970) and considering the dependence of the human species on experience and learning processes for the expression of complex patterns of behavior, the influence of the prenatal hormones is best understood as setting a bias on the neural substratrum, which in turn predisposes the individual to the acquisition and expression of sexually dimorphic patterns of response and behavior (Goy, 1970; Hamburg and Lunde, 1966). It is not possible at this point in research to identify the response patterns and behavior styles which are directly or indirectly the result of prenatal hormonal influences, but it appears evident that at least some of those mentioned in this discussion are related to hormonally mediated brain differences.


Androgen Integrative Review Diffuse Quality Proper Perspective Brain Difference 
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.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Anastasi, A. (1958).Differential Psychology: Individual and Group Differences in Behavior 3rd ed., Macmillan, New York.Google Scholar
  2. Barraclough, C. A. (1961). Production of anovulatory, sterile rats by single injections of testosterone propionate.Endocrinology 6862–67.PubMedGoogle Scholar
  3. Barraclough, C. A. (1966). Modification in the CNS regulation of reproduction after exposure of prepubertal rats to steroid hormones. In Pincus, G. (ed.),Recent Progress in Hormone Research, Vol. 22, Academic Press, New York.Google Scholar
  4. Barraclough, C. A., and Gorski, R. A. (1961). Evidence that the hypothalamus is responsible for androgen-induced sterility in the female rat.Endocrinology 6868–79.PubMedGoogle Scholar
  5. Barraclough, C. A., and Gorski, R. A. (1962). Studies on mating behavior in the androgen-sterilized female rat in relation to hypothalamic regulation of sexual behavior.J. Endocrinol. 25175–182.PubMedGoogle Scholar
  6. Beach, F. A. (1971). Hormonal factors controlling the differentiation, development, and display of copulatory behavior in the ramstergig and related species. In Tobach, E., Aaronson, L. R., and Shaw, E. (eds.),Biopsychology of Behavior Academic Press, New York, pp. 249–296.Google Scholar
  7. Beach, F. A., and Westbrook, W. H. (1968). Dissociation of androgenic effects on sexual morphology and behavior in male rats.Endrocrinology 83395–398.Google Scholar
  8. Beach, F. A., Noble, G., and Orndoff, K. (1969). Effects of perinatal androgen treatment on responses of male rats to gonadal hormones in adulthood.J. Comp. Physiol. Psychol. 68490–497.PubMedGoogle Scholar
  9. Beeman, E. A. (1947). The effect of male hormone on aggressive behavior in mice.Physiol. Zool. 20373–405.Google Scholar
  10. Birch, G., and Clark, G. (1950). Hormonal modification of social behavior. IV. The mechanism of estrogen-induced dominance in chimpanzees.J. Comp. Physiol. Psychol. 43181–193.PubMedGoogle Scholar
  11. Boersma, F. J., Muir, W., Wilton, K., and Barham, P. (1969). Eye movements during embedded figure tasks.Percept. Motor Skills 28271–274.PubMedGoogle Scholar
  12. Bronson, G. W. (1969). Sex differences in the development of fearfulness: A replication.Psychon. Sci. 17367–368.Google Scholar
  13. Broverman, D. M., Klaiber, E. L., Kobayashi, Y., and Vogel, W. (1968). Roles of activation and inhibition in sex differences in cognitive abilities.Psychol. Rev. 7523–50.Google Scholar
  14. Buchsbaum, M., and Silverman, J. (1968). Stimulus intensity control and the cortical evoked response.Psychosom. Med. 3012–22.PubMedGoogle Scholar
  15. Burns, R. K. (1961). Role of hormones in the differentiation of sex. In Young, W. C., (ed.),Sex and Internal Secretions 3rd ed. Williams and Wilkins, Baltimore, Vol. I, pp. 76–158.Google Scholar
  16. Clark, H. M. (1935). Sex differences in change in potency of anterior hypophysis following bilateral castration in newborn rats.Anat. Rec. 61193–205.Google Scholar
  17. Clayton, R. B., Kogura, J., and Kraemer, H. C. (1970). Sexual differentiation of the brain: Effects of testosterone on brain RNA metabolism in newborn female rats.Nature 226810–812.PubMedGoogle Scholar
  18. Diamond, M., and Young, W. C. (1963). Differential responsiveness of pregnant and nonpregnant guinea pigs to the masculinizing action of testosterone propionate.Endocrinology 72429–438.PubMedGoogle Scholar
  19. Donev, S. (1970). Occurrence of the neurosecretory substance during the embryonic development of the guinea pig.Z. Zellforsch. 104517–529.PubMedGoogle Scholar
  20. Dörner, G. (1968). Hormonal induction and prevention of female homosexuality.J. Endocrinol. 42163–164.Google Scholar
  21. Dörner, G. (1970). The influence of sex hormones during the hypothalamic differentiation and maturation phases on gonadal function and sexual behavior during the hypothalamic functional phase.Endokrinologie 56280–291.PubMedGoogle Scholar
  22. Dörner, G., and Staudt, J. (1968). Structural changes in the preoptic anterior hypothalamic area of the male rat, following neonatal castration and androgen substitution.Neuroendocrinology 3136–140.PubMedGoogle Scholar
  23. Dörner, G., and Staudt, J. (1969a). Structural changes in the hypothalamic ventromedial nucleus of the male rat, following neonatal castration and androgen treatment.Neuroendocrinology 4278–281.PubMedGoogle Scholar
  24. Dörner, G., and Staudt, J. (1969b). Perinatal structural sex differentiation of the hypothalamus in rats.Neuroendocrinology 5103–106.PubMedGoogle Scholar
  25. Dörner, G., Döcke, F., and Moustafa, S. (1968). Differential localization of a male and a female hypothalamic mating centre.J. Reprod. Fertil. 17583–586.PubMedGoogle Scholar
  26. Edwards, D. A. (1969). Early androgen stimulation and aggressive behavior in male and female mice.Physiol. Behav. 4333–338.Google Scholar
  27. Edwards, D. A. (1970). Post-natal androgenization and adult aggressive behavior in female mice.Physiol. Behav. 5465–467.PubMedGoogle Scholar
  28. Edwards, D. A., and Herndon, J. (1970). Neonatal estrogen stimulation and aggressive behavior in female mice.Physiol. Behav. 5993–995.PubMedGoogle Scholar
  29. Ehrhardt, A. A., and Money, J. (1967). Progestin-induced hermaphroditism: I.Q. and psychosexual identity in a study of ten girls.J. Sex Res. 383–100.Google Scholar
  30. Ehrhardt, A. A., Epstein, R., and Money, J. (1968a). Fetal androgens and female gender identity in the early-treated adrenogenital syndrome.Johns Hopkins Med. J. 122 160–167.PubMedGoogle Scholar
  31. Ehrhardt, A. A., Evers, K., and Money, J. (1968b). Influence of androgen and some aspects of sexually dimorphic behavior in women with the late-treated adrenogenital syndrome.Johns Hopkins Med. J. 123115–122.PubMedGoogle Scholar
  32. Ehrhardt, A. A., Greenberg, N., and Money, J. (1970). Female gender identity and absence of fetal gonadal hormones: Turner's syndrome.Johns Hopkins Med. J. 126237–248.PubMedGoogle Scholar
  33. Gill, N. T., Herdtner, T. J., and Lough, L. (1968). Perceptual and socio-economic variables, instruction in body-orientation, and predicted academic success in young children.Percept. Motor Skills 261175–1184.PubMedGoogle Scholar
  34. Gorski, R. A., and Barraclough, A. (1963). Effects of low dosages of androgen on the differentiation of hypothalamic regulatory control of ovulation in the rat.Endocrinology 73210–216.PubMedGoogle Scholar
  35. Gorski, R. A., and Wagner, J. W. (1965). Gonadal activity and sexual differentiation of the hypothalamus.Endocrinology 76226–239.PubMedGoogle Scholar
  36. Goy, R. W. (1968). Organizing effects of androgen on the behavior of rhesus monkeys. In Michael, R. P. (ed.),Endocrinology and Human Behavior Oxford University Press, London, pp. 12–31.Google Scholar
  37. Goy, R. W. (1970). Early hormonal influence on the development of sexual and sex-related behavior. In Quarton, G. C., Melanchuk, T., and Schmitt, F. O. (eds.),Neuro-Sciences: A Study Program Rockefeller University Press, New York, pp. 196–207.Google Scholar
  38. Grady, K. L., Phoenix, C. H., and Young, W. C. (1965). Role of the developing rat testis in differentiation of the neural tissues mediating mating behavior.J. Comp. Physiol. Psychol. 59176–182.PubMedGoogle Scholar
  39. Hamburg, D. A., and Lunde, D. T. (1966). Sex hormones in the development of differences in human behavior. In Maccoby, E. E. (ed.),The Development of Sex Differences Stanford University Press, Stanford, Calif., pp. 1–24.Google Scholar
  40. Hamm, N., and Hoving, K. (1969). Age and sex differences in the perception of autokinesis in children.Percept. Motor Skills 28317–318.PubMedGoogle Scholar
  41. Harris, G. W. (1964). Sex hormones, brain development and brain function.Endocrinology 75627–648.PubMedGoogle Scholar
  42. Harris, G. W., and Jacobsohn, D. (1952). Functional grafts of the anterior pituitary gland.Proc. Roy. Soc. Lond. Ser. B B139263–276.Google Scholar
  43. Harris, G. W., and Levine, S. (1965). Sexual differentiation of the brain and its experimental control.J. Physiol. 181379–400.PubMedGoogle Scholar
  44. Harris, G. W., and Naftolin, F. (1970). The hypothalamus and control of ovulation.Brit. Med. Bull. 263–9.PubMedGoogle Scholar
  45. Immergluck, L., and Mearini, M. C. (1969). Age and sex differences in responses to embedded figures and reversible figures.J. Exptl. Child Psychol. 8210–221.Google Scholar
  46. Jost, A. (1953). Problems of fetal endocrinology: The gonadal and hypophyseal hormones.Recent Prog. Horm. Res. 8 379–418.Google Scholar
  47. Jost, A. (1972). A new look at the mechanisms controlling sex differentiation in mammals.Johns Hopkins Med. J. 130 38–53.PubMedGoogle Scholar
  48. Kagan, J. (1969). On the meaning of behavior: Illustrations from the infant.Child Develop. 401121–1134.PubMedGoogle Scholar
  49. Korner, A. F. (1969). Neonatal startles, smiles, erections, and reflex sucks as related to state, sex, and individuality.Child Develop. 401039–1053.PubMedGoogle Scholar
  50. Ladosky, W., and Gaziri, L. C. J. (1970). Brain serotonin and sexual differentiation of the nervous system.Neuroendocrinology 6168–174.PubMedGoogle Scholar
  51. Levine, S. (1966). Sex differences in the brain.Sci. Am. 21484–90.Google Scholar
  52. Lewis, V. G., Money, J., and Epstein, R. (1968). Concordance of verbal and nonverbal ability in the adrenogenital syndrome.Johns Hopkins Med. J. 122192–195.PubMedGoogle Scholar
  53. Luttge, W. G., and Whalen, R. E. (1970). Regional localization of estrogenic metabolites in the brain of male and female rats.Steroids 15605–612.PubMedGoogle Scholar
  54. Maccoby, E. E. (1966).The Development of Sex Differences Stanford University Press, Stanford, Calif.Google Scholar
  55. Martinez, C., and Bittner, J. J. (1956). Non-hypophyseal sex differences in estrous behavior of mice bearing pituitary grafts.Proc. Soc. Exptl. Biol. Med. 91506–509.Google Scholar
  56. Masica, D. N., Money, J., Erhardt, A. A., and Lewis, V. G. (1969). I.Q., fetal sex hormones and cognitive patterns: Studies in the testicular feminizing syndrome of androgen insensitivity.Johns Hopkins Med. J. 12434–43.PubMedGoogle Scholar
  57. Moguilevsky, J. A. (1966). Effect of testosterone “in vitro” on the oxygen uptake of different hypothalamic areas.Acta Physiol. Lat. Am. 16353–356.PubMedGoogle Scholar
  58. Moguilevsky, J. A., and Malinow, M. R. (1964). Endogenous oxygen uptake of the hypothalamus in female rats.Am. J. Physiol. 206855–857.PubMedGoogle Scholar
  59. Moguilevsky, J. A., and Rubinstein, L. (1967). Glycolytic and oxidative metabolism of hypothalamic areas in prepubertal and androgenized rats.Neuroendocrinology 2 213–221.Google Scholar
  60. Moguilevsky, J. A., Timiras, P. S., and Geel, S. (1964). Oxygen consumption and carbon dioxide production in the hypothalamus and cerebral cortex. Influence of sexual maturation in male rats.Acta Physiol. Lat. Am. 14207–210.PubMedGoogle Scholar
  61. Moguilevsky, J. A., Schiaffini, O., and Foglia, V. (1966). Effect of castration on the oxygen uptake of different parts of hypothalamus.Life Sci. 5447–452.PubMedGoogle Scholar
  62. Moguilevsky, J. A., Libertun, C., Schiaffini, O., and Szwarcfarb, B. (1968). Sexual differences in hypothalamic metabolism.Neuroendocrinology 3193–199.PubMedGoogle Scholar
  63. Moguilevsky, J. A., Libertun, C., Schiaffini, O., and Scacchi, P. (1969). Metabolic evidence of the sexual differentiation of hypothalamus.Neuroendocrinology 4264–269.PubMedGoogle Scholar
  64. Money, J. (1960). Components of eroticism in man: Cognitional rehearsals. InRecent Advances in Biological Psychology Grune and Stratton, New York.Google Scholar
  65. Money, J. (1965a). Psychosexual differentiation. In Money, J. (ed.),Sex Research: New Developments Holt, New York.Google Scholar
  66. Money, J. (1965b). Influence of hormones on sexual behavior.Ann. Rev. Med. 1667–82.PubMedGoogle Scholar
  67. Money, J. (1972). Determinants of human sexual identity and behavior. In Sagar, C. J., and Kaplan, H. S. (eds.),Progress in Group and Family Therapy Brunner/Mazel, New York.Google Scholar
  68. Money, J., and Ehrhardt, A. A. (1968). Prenatal hormonal exposure: Possible effects on behavior in man. In Michall, R. P. (ed.),Endocrinology and Human Behavior Oxford University Press, London, pp. 32–48.Google Scholar
  69. Money, J., and Lewis, V. (1966). I.Q., genetics and accelerated growth: Adrenogenital syndrome.Bull. Johns Hopkins Hosp. 118365–373.Google Scholar
  70. Money, J., and Meredith, T. (1967). Elevated verbal IQ and idiopathic precocious sexual maturation.Pediat. Res. 159–65.Google Scholar
  71. Money, J., Lewis, V., Ehrhardt, A. A., and Drash, P. W. (1967). I.Q. impairment and elevation in endocrine and related cytogenetic disorders. InPsychopathology of Mental Development Grune and Stratton, New York.Google Scholar
  72. Money, J., Ehrhardt, A. A., and Masica, D. N. (1968). Fetal feminization induced by androgen insensitivity in the testicular feminization syndrome: Effect on marriage and maternalism.Johns Hopkins Med. J. 123105–114.PubMedGoogle Scholar
  73. Nadler, R. D. (1969). Differentiation of the capacity for male sexual behavior in the rat.Hormones Behav. 153–56.Google Scholar
  74. Neumann, F., Elger, W., and Steinbeck, H. (1970). Antiandrogens and reproductive development.Phil. Trans. Roy. Soc. Lond. Ser. B. 259179–184.Google Scholar
  75. Nucci, L. P., and Beach, F. A. (1971). Effects of prenatal androgen treatment on mating behavior in female hamsters.Endocinology 881514–1515.Google Scholar
  76. Pfaff, D. W., and Zigmond, R. E. (1971). Neonatal androgen effects on sexual and non-sexual behavior of adult rats tested under various hormone regimes.Neuroendocrinology 7129–145.PubMedGoogle Scholar
  77. Pfeiffer, C. A. (1936). Sexual differences of the hypophyses and their determination by the gonads.Am. J. Anat. 58195–225.Google Scholar
  78. Phoenix, C. H., Goy, R. W., Gerall, A. A., and Young, W. C. (1959). Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig.Endocrinology 65369–382.PubMedGoogle Scholar
  79. Phoenix, G. H., Goy, R. W., and Resko, J. A. (1968). Psychosexual differentiation as a function of androgenic stimulation. In Diamond, M. (ed.),Perspectives in Reproduction and Sexual Behavior Indiana University Press, Bloomington, Ind., pp. 33–49.Google Scholar
  80. Scacchi, P., Moguilevsky, J. A., Libertun, C., and Christot, J. (1970). Sexual differences in protein content of the hypothalamus in rats.Proc. Soc. Exptl. Biol. Med. 133845–848.Google Scholar
  81. Schally, A. V., and Kastin, A. J. (1969). The present concept of the nature of hypothalamic hormones stimulating and inhibiting the release of pituitary hormones.Triangle 9 19–25.PubMedGoogle Scholar
  82. Segal, S. J., and Johnson, D. C. (1959). Absence of steroid hormones on the neural system: Ovulation controlling mechanisms.Arch. Anat. Suppl. 48261–273.Google Scholar
  83. Silverman, J. (1971). Attentional styles and the study of sex differences. In Mostofsky, D. (ed.),Attention: Contemporary Studies and Analysis Appleton-Century-Crofts, New York.Google Scholar
  84. Silverman, J., and King, C. (1970). Pseudo perceptual differentiation.J. Consult. Clin. Psychol. 34119–123.PubMedGoogle Scholar
  85. Swanson, H. H. (1967). Alteration of sex-typical behavior of hamsters in open field and emergence tests by neo-natal administration of androgen or oestrogen.Anim. Behav. 15209–216.PubMedGoogle Scholar
  86. Swanson, H. H., and Crossley, D. A. (1971). Sexual behavior in the golden hamster and its modification by neonatal administration of testosterone propionate. In Hamburgh, M., and Barrington, E. J. (eds.),Hormones in Behavior, Appleton-Century-Crofts, New York, pp. 677–687.Google Scholar
  87. Ward, I. L. (1969). Differential effect of pre- and postnatal androgen on the sexual behavior of intact and spayed female rats.Hormones Behav. 125–36.Google Scholar
  88. Ward, I. L. (1972). Female sexual behavior in male rats treated prenatally with an anti-androgen.Physiol. Behav. 853–56.PubMedGoogle Scholar
  89. Watson, J. S. (1969). Operant conditioning of visual fixation in infants under visual and auditory reinforcement.Develop. Psychol. 1508–516.Google Scholar
  90. Whalen, R. E. (1968). Differentiation of the neural mechanisms which control gonadotropin secretion and sexual behavior. In Diamond, M. (ed.),Perspectives in Reproduction and Sexual Behavior Indiana University Press, Bloomington, Ind., pp. 303–340.Google Scholar
  91. Whalen, R. E., and Edwards, D. A. (1967). Hormonal determinants of the development of masculine and feminine behavior in male and female rats.Anat. Rec. 157173–180.PubMedGoogle Scholar
  92. Whalen, R. E., and Luttge, W. G. (1971). Testosterone, androstenedione, and dihydrotestosterone: Effects on mating behavior of male rats.Hormones Behav. 2117–125.Google Scholar
  93. Whalen, R. E., and Robertson, R. T. (1968). Sexual exhaustion and recovery of masculine copulatory behavior in virilized female rats.Psychon. Sci. 11319–320.Google Scholar
  94. Whalen, R. E., Edwards, D. A., Luttage, W. C., and Robertson, T. (1969). Early androgen treatment and male sexual behavior in female rats.Physiol. Behav. 433–39.Google Scholar
  95. Witkin, H. A. (1962).Psychological Differentiation Wiley, New York.Google Scholar
  96. Young, W. C., Goy, R. W., and Phoenix, C. H. (1964). Hormones and sexual behavior.Science 143212–218.PubMedGoogle Scholar

Copyright information

© Plenum Publishing Corporation 1974

Authors and Affiliations

  • June M. Reinisch
    • 1
  1. 1.Developmental PsychologyTeacher's College, Columbia UniversityNew YorkUSA

Personalised recommendations