Archives of Sexual Behavior

, Volume 41, Issue 3, pp 571–581

Effects of Fetal Testosterone on Visuospatial Ability

  • Bonnie Auyeung
  • Rebecca Knickmeyer
  • Emma Ashwin
  • Kevin Taylor
  • Gerald Hackett
  • Simon Baron-Cohen
Original Paper

Abstract

This study investigated whether fetal testosterone (FT) measured from second trimester amniotic fluid was related to specific aspects of visuospatial ability, in children aged 7–10 years (35 boys, 29 girls). A series of tasks were used: the children’s Embedded Figures Test (EFT) (a test of attention to detail), a ball targeting task (measuring hand-eye coordination), and a computerized mental rotation task (measuring rotational ability). FT was a significant predictor for EFT scores in both boys and girls, with boys also showing a clear advantage for this task. No significant sex differences were observed in targeting. Boys scored higher than girls on mental rotation. However, no significant relationships were observed between FT and targeting or mental rotation. Girls’ performance on the mental rotation and targeting tasks was significantly related to age, indicating that these tasks may have been too difficult for the younger children. These results indicate that FT has a significant role in some aspects of cognitive development but that further work is needed to understand its effect on the different aspects of visuospatial ability.

Keywords

Spatial ability Mental rotation Sex differences Fetal testosterone 

References

  1. Altman, D. G. (1991). Practical statistics for medical research. London: Chapman and Hall.Google Scholar
  2. Auyeung, B., Baron-Cohen, S., Ashwin, E., Knickmeyer, R., Taylor, K., Hackett, G., et al. (2009a). Fetal testosterone predicts sexually differentiated childhood behavior in girls and in boys. Psychological Science, 20, 144–148.PubMedCrossRefGoogle Scholar
  3. Auyeung, B., Baron-Cohen, S., Chapman, E., Knickmeyer, R., Taylor, K., & Hackett, G. (2006). Foetal testosterone and the child systemizing quotient. European Journal of Endocrinology, 155, S123–S130.CrossRefGoogle Scholar
  4. Auyeung, B., Baron-Cohen, S., Chapman, E., Knickmeyer, R., Taylor, K., & Hackett, G. (2009b). Fetal testosterone and autistic traits. British Journal of Psychology, 100, 1–22.PubMedCrossRefGoogle Scholar
  5. Baker, S. W., & Ehrhardt, A. A. (1974). Prenatal androgen, intelligence and cognitive sex differences. In R. C. Friedman, R. M. Richart, & R. L. Van de Wiele (Eds.), Sex differences in behavior (pp. 53–76). New York: Wiley.Google Scholar
  6. Baron-Cohen, S. (2002). The extreme male brain theory of autism. Trends in Cognitive Science, 6, 248–254.CrossRefGoogle Scholar
  7. Baron-Cohen, S., Knickmeyer, R., & Belmonte, M. K. (2005). Sex differences in the brain: Implications for explaining autism. Science, 310, 819–823.PubMedCrossRefGoogle Scholar
  8. Baron-Cohen, S., Lutchmaya, S., & Knickmeyer, R. (2004). Prenatal testosterone in mind. Cambridge, MA: The MIT Press.Google Scholar
  9. Beck-Peccoz, P., Padmanabhan, V., Baggiani, A. M., Cortelazzi, D., Buscaglia, M., Medri, G., et al. (1991). Maturation of hypothalamic-pituitary-gonadal function in normal human fetuses: Circulating levels of gonadotropins, their common alpha-subunit and free testosterone, and discrepancy between immunological and biological activities of circulating follicle-stimulating hormone. Journal of Clinical Endocrinology and Metabolism, 73, 525–532.PubMedCrossRefGoogle Scholar
  10. Bergman, K., Glover, V., Sarkar, P., Abbott, D. H., & O’Connor, T. G. (2010). In utero cortisol and testosterone exposure and fear reactivity in infancy. Hormones and Behavior, 57, 306–312.PubMedCrossRefGoogle Scholar
  11. Bigelow, G. (1971). Field dependence-field independence. Journal of Educational Research, 64, 397–400.Google Scholar
  12. Brosnan, M., Daggar, R., & Collomosse, J. (2010). The relationship between systemising and mental rotation and the implications for the extreme male brain theory of autism. Journal of Autism and Developmental Disorders, 40, 1–7.PubMedCrossRefGoogle Scholar
  13. Chakrabarti, B., Dudbridge, F., Kent, L., Wheelwright, S., Hill-Cawthorne, G., Allison, C., et al. (2009). Genes related to sex steroids, neural growth, and social-emotional behavior are associated with autistic traits, empathy, and Asperger syndrome. Autism Research, 2, 157–177.PubMedCrossRefGoogle Scholar
  14. Cohen, J. (1988). Statistical power analysis for the behavioral sciences (2nd ed.). Hillsdale, NJ: Lawrence Erlbaum Associates.Google Scholar
  15. Cohen-Bendahan, C. C., van de Beek, C., & Berenbaum, S. A. (2005). Prenatal sex hormone effects on child and adult sex-typed behavior: Methods and findings. Neuroscience and Biobehavioral Reviews, 29, 353–384.PubMedCrossRefGoogle Scholar
  16. Collaer, M. L., & Hines, M. (1995). Human behavioural sex differences: A role for gonadal hormones during early development? Psychological Bulletin, 118, 55–107.PubMedCrossRefGoogle Scholar
  17. d’Ercole, C., Shojai, R., Desbriere, R., Chau, C., Bretelle, F., Piechon, L., et al. (2003). Prenatal screening: Invasive diagnostic approaches. Child’s Nervous System, 19, 444–447.PubMedCrossRefGoogle Scholar
  18. Falter, C. M., Arroyo, M., & Davis, G. J. (2006). Testosterone: Activation or organization of spatial cognition? Biological Psychology, 73, 132–140.PubMedCrossRefGoogle Scholar
  19. Falter, C. M., Plaisted, K. C., & Davis, G. (2008). Visuo-spatial processing in autism—testing the predictions of extreme male brain theory. Journal of Autism and Developmental Disorders, 38, 507–515.PubMedCrossRefGoogle Scholar
  20. Fausto-Sterling, A. (1992). Myths of gender. New York: Basic Books.Google Scholar
  21. Feng, J., Spence, I., & Pratt, J. (2007). Playing an action video game reduces gender differences in spatial cognition. Psychological Science, 18, 850–855.PubMedCrossRefGoogle Scholar
  22. Finegan, J., Bartleman, B., & Wong, P. Y. (1989). A window for the study of prenatal sex hormone influences on postnatal development. Journal of Genetic Psychology, 150, 101–112.PubMedCrossRefGoogle Scholar
  23. Finegan, J. K., Niccols, G. A., & Sitarenios, G. (1992). Relations between prenatal testosterone levels and cognitive abilities at 4 years. Developmental Psychology, 28, 1075–1089.CrossRefGoogle Scholar
  24. Galis, F., Ten Broek, C. M., Van Dongen, S., & Wijnaendts, L. C. (2010). Sexual dimorphism in the prenatal digit ratio (2D:4D). Archives of Sexual Behavior, 39, 57–62.PubMedCrossRefGoogle Scholar
  25. Goy, R. W., Bercovitch, F. B., & McBrair, M. C. (1988). Behavioral masculinization is independent of genital masculinization in prenatally androgenized female rhesus macaques. Hormones and Behavior, 22, 552–571.PubMedCrossRefGoogle Scholar
  26. Grimshaw, G. M., Sitarenios, G., & Finegan, J. K. (1995). Mental rotation at 7 years: Relations with prenatal testosterone levels and spatial play experiences. Brain and Cognition, 29, 85–100.PubMedCrossRefGoogle Scholar
  27. Halpern, D. F. (2000). Sex differences in cognitive abilities (3rd ed.). Mahwah, NJ: Erlbaum.Google Scholar
  28. Hampson, E., Ellis, C. L., & Tenk, C. M. (2008). On the relation between 2D:4D and sex- dimorphic personality traits. Archives of Sexual Behavior, 37, 133–144.PubMedCrossRefGoogle Scholar
  29. Hampson, E., Rovet, J. F., & Altmann, D. (1998). Spatial reasoning in children with congenital adrenal hyperplasia due to 21-hydroxylase deficiency. Developmental Neuropsychology, 14, 299–320.CrossRefGoogle Scholar
  30. Hines, M. (2004). Brain gender. New York: Oxford University Press.Google Scholar
  31. Hines, M., Fane, B. A., Pasterski, V. L., Matthews, G. A., Conway, G. S., & Brook, C. (2003). Spatial abilities following prenatal androgen abnormality: Targeting and mental rotations performance in individuals with congenital adrenal hyperplasia. Psychoneuroendocrinology, 28, 1010–1026.PubMedCrossRefGoogle Scholar
  32. Hooven, C. K., Chabris, C. F., Ellison, P. T., & Kosslyn, S. M. (2004). The relationship of male testosterone to components of mental rotation. Neuropsychologia, 42, 782–790.PubMedCrossRefGoogle Scholar
  33. Johnson, E. S., & Meade, A. C. (1987). Developmental patterns of spatial ability: An early sex difference. Child Development, 58, 725–740.PubMedCrossRefGoogle Scholar
  34. Karp, S. A., & Konstadt, N. L. (1963). Manual for the Children’s Embedded Figures Test. Brookland, NY: Cognitive Tests.Google Scholar
  35. Kerns, K. A., & Berenbaum, S. A. (1991). Sex differences in spatial ability in children. Behavior Genetics, 21, 383–396.PubMedCrossRefGoogle Scholar
  36. Kimura, D. (1999). Sex and cognition. Cambridge, MA: The MIT Press.Google Scholar
  37. Knickmeyer, R., Baron-Cohen, S., Fane, B. A., Wheelwright, S., Mathews, G. A., Conway, G. S., et al. (2006). Androgens and autistic traits: A study of individuals with congenital adrenal hyperplasia. Hormones and Behavior, 50, 148–153.PubMedCrossRefGoogle Scholar
  38. Levine, S. C., Huttenlocher, J., Taylor, A., & Langrock, A. (1999). Early sex differences in spatial skill. Developmental Psychology, 35, 940–949.PubMedCrossRefGoogle Scholar
  39. Linn, M. C., & Petersen, A. C. (1986). Gender differences in spatial ability: Implications for mathematics and science achievement. In J. S. Hyde & M. C. Linn (Eds.), The psychology of gender: Advances through meta-analysis (pp. 67–101). Baltimore: Johns Hopkins University Press.Google Scholar
  40. Lutchmaya, S., Baron-Cohen, S., Raggatt, P., Knickmeyer, R., & Manning, J. T. (2004). 2nd to 4th digit ratios, fetal testosterone and estradiol. Early Human Development, 77, 23–28.PubMedCrossRefGoogle Scholar
  41. Malas, M. A., Dogan, S., Evcil, E. H., & Desdicioglu, K. (2006). Fetal development of the hand, digits and digit ratio (2D:4D). Early Human Development, 82, 469–475.PubMedCrossRefGoogle Scholar
  42. Malouf, M. A., Migeon, C. J., Carson, K. A., Petrucci, L., & Wisniewski, A. B. (2006). Cognitive outcome in adult women affected by congenital adrenal hyperplasia due to 21-hydroxylase deficiency. Hormone Research, 65, 142–150.PubMedCrossRefGoogle Scholar
  43. Manning, J. T. (2002). Digit ratio: A pointer to fertility, behavior and health. New Brunswick, NJ: Rutgers University Press.Google Scholar
  44. Manning, J. T., & Taylor, R. P. (2001). Second to fourth digit ratio and male ability in sport: Implications for sexual selection in humans. Evolution and Human Behavior, 22, 61–69.PubMedCrossRefGoogle Scholar
  45. Nebot, T. K. (1988). Sex differences among children on embedded tasks. Perceptual and Motor Skills, 67, 972–974.PubMedCrossRefGoogle Scholar
  46. New, M. I. (1998). Diagnosis and management of congenital adrenal hyperplasia. Annual Review of Medicine, 49, 311–328.PubMedCrossRefGoogle Scholar
  47. Nordenstrom, A., Servin, A., Bohlin, G., Larsson, A., & Wedell, A. (2002). Sex-typed toy play behavior correlates with the degree of prenatal androgen exposure assessed by the CYP21 genotype in girls with congenital adrenal hyperplasia. Journal of Clinical Endocrinology & Metabolism, 87, 5119–5124.CrossRefGoogle Scholar
  48. Parlee, M. B., & Rajagopal, J. (1974). Sex differences on the Embedded-Figures Test: A cross-cultural comparison of college students in India and in the United States. Perceptual and Motor Skills, 39, 1311–1314.CrossRefGoogle Scholar
  49. Pasterski, V. L., Geffner, M. E., Brain, C., Hindmarsh, P., Brook, C., & Hines, M. (2005). Prenatal hormones and postnatal socialization by parents as determinants of male-typical toy play in girls with congenital adrenal hyperplasia. Child Development, 76, 264–278.PubMedCrossRefGoogle Scholar
  50. Perlman, S. M. (1973). Cognitive abilities of children with hormone abnormalities: Screening by psychoeducational tests. Journal of Learning Disabilities, 6, 26–34.CrossRefGoogle Scholar
  51. Puts, D. A., McDaniel, M. A., Jordan, C. L., & Breedlove, S. M. (2008). Spatial ability and prenatal androgens: meta-analyses of congenital adrenal hyperplasia and digit ratio (2D:4D) studies. Archives of Sexual Behavior, 37, 100–111.PubMedCrossRefGoogle Scholar
  52. Quadagno, D. M., Briscoe, R., & Quadagno, J. S. (1977). Effects of perinatal gonadal hormones on selected nonsexual behavior patterns: A critical assessment of the nonhuman and human literature. Psychological Bulletin, 84, 62–80.PubMedCrossRefGoogle Scholar
  53. Resnick, S. M., Berenbaum, S. A., Gottesman, I. I., & Bouchard, T. J. (1986). Early hormonal influences on cognitive functioning in congenital adrenal hyperplasia. Developmental Psychology, 22, 191–198.CrossRefGoogle Scholar
  54. Sangalli, M., Langdana, F., & Thurlow, C. (2004). Pregnancy loss rate following routine genetic amniocentesis at Wellington Hospital. New Zealand Medical Journal, 117, U818.PubMedGoogle Scholar
  55. Sarkar, P., Bergman, K., Fisk, N. M., O’Connor, T. G., & Glover, V. (2007). Amniotic fluid testosterone: Relationship with cortisol and gestational age. Clinical Endocrinology, 67, 743–747.PubMedCrossRefGoogle Scholar
  56. Shah, A., & Frith, C. (1993). Why do autistic individuals show superior performance on the block design task? Journal of Child Psychology and Psychiatry, 34, 1351–1364.PubMedCrossRefGoogle Scholar
  57. Shah, A., & Frith, U. (1983). An islet of ability in autistic children: A research note. Journal of Child Psychology and Psychiatry, 24, 613–620.PubMedCrossRefGoogle Scholar
  58. Smail, P. J., Reyes, F. I., Winter, J. S. D., & Faiman, C. (1981). The fetal hormonal environment and its effect on the morphogenesis of the genital system. In S. J. Kogan & E. S. E. Hafez (Eds.), Pediatric andrology (pp. 9–19). Boston: Martinus Nijhoff.CrossRefGoogle Scholar
  59. Terlecki, M. S., Newcombe, N. S., & Little, M. (2008). Durable and generalized effects of spatial experience on mental rotation: Gender differences in growth patterns. Applied Cognitive Psychology, 22, 996–1013.CrossRefGoogle Scholar
  60. Thomas, J. R., & French, K. E. (1985). Gender differences across age in motor performance a meta-analysis. Psychological Bulletin, 98, 260–282.PubMedCrossRefGoogle Scholar
  61. van de Beek, C., Thijssen, J. H. H., Cohen-Kettenis, P. T., van Goozen, S. H., & Buitelaar, J. K. (2004). Relationships between sex hormones assessed in amniotic fluid, and maternal and umbilical cord blood: What is the best source of information to investigate the effects of fetal hormonal exposure? Hormones and Behavior, 46, 663–669.PubMedCrossRefGoogle Scholar
  62. van de Beek, C., van Goozen, S. H. M., Buitelaar, J. K., & Cohen-Kettenis, P. T. (2008). Prenatal sex hormones (maternal and amniotic fluid) and gender-related play behavior in 13-month-old infants. Archives of Sexual Behavior, 38, 6–15.CrossRefGoogle Scholar
  63. Voyer, D., Voyer, S., & Bryden, M. P. (1995). Magnitude of sex differences in spatial abilities: A meta-analysis and consideration of critical variables. Psychological Bulletin, 117, 250–270.PubMedCrossRefGoogle Scholar
  64. Watson, N. V., & Kimura, D. (1991). Nontrivial sex differences in throwing and intercepting: Relation to psychometrically-defined spatial functions. Personality and Individual Differences, 12, 375–385.CrossRefGoogle Scholar
  65. Williams, C. L., Barnett, A. M., & Meck, W. H. (1990). Organizational effects of early gonadal secretions on sexual differentiation in spatial memory. Behavioral Neuroscience, 104, 84–97.PubMedCrossRefGoogle Scholar
  66. Williams, C. L., & Meck, W. H. (1991). The organizational effects of gonadal steroids on sexually dimorphic spatial ability. Psychoneuroendocrinology, 16, 155–176.PubMedCrossRefGoogle Scholar
  67. Witkin, H. A., Oltman, P. K., Raskin, E., & Karp, S. (1971). A Manual for the Embedded Figures Test. Palo Alto, CA: Consulting Psychology Press.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Bonnie Auyeung
    • 1
  • Rebecca Knickmeyer
    • 1
    • 2
  • Emma Ashwin
    • 1
  • Kevin Taylor
    • 3
  • Gerald Hackett
    • 4
  • Simon Baron-Cohen
    • 1
  1. 1.Department of PsychiatryUniversity of CambridgeCambridgeUK
  2. 2.Department of PsychiatryUniversity of North Carolina at Chapel HillChapel HillUSA
  3. 3.Department of Clinical BiochemistryAddenbrooke’s HospitalCambridgeUK
  4. 4.Department of Foetal MedicineRosie Maternity HospitalCambridgeUK

Personalised recommendations