Abstract
Hormonal manipulations indicate that early androgens organize sex differences in spatial ability in laboratory rats. In humans, spatial ability is also sexually dimorphic, and information about the effects of prenatal androgens on spatial ability can be obtained from studies of congenital adrenal hyperplasia (CAH) and the ratio of the second and fourth finger lengths (2D:4D). CAH is characterized by prenatal overproduction of adrenal androgens and several lines of evidence suggest that 2D:4D reflects prenatal androgen exposure. Some studies have found that these proxy measures of prenatal androgens predict spatial ability, others have found no significant relationship, and yet others have obtained results in the opposite direction. In light of these mixed findings, we conducted meta-analyses of published literature and unpublished results to determine if, across studies, either of these indicators of prenatal androgens predicts performance on spatial tasks that show a male advantage. In addition, we applied a trim and fill analysis to the data in search of asymmetry that might be an indication of publication bias. Results indicated that females with CAH perform better on these spatial tasks, and CAH males perform worse, than do controls. Little or no relationship exists between 2D:4D and spatial ability. Implications for possible hormonal contributions and the developmental timing of sex differences in spatial cognition are discussed.
Similar content being viewed by others
References
Astur, R. S., Ortiz, M. L., & Sutherland, R. J. (1998). A characterization of performance by men and women in a virtual Morris water task: A large and reliable sex difference. Behavioural Brain Research, 93, 185–190.
Austin, E. J., Manning, J. T., McInroy, K., & Mathews, E. (2002). A preliminary investigation of the associations between personality, cognitive ability and digit ratio. Personality and Individual Differences, 33, 1115–1124.
Baker, S. W., & Ehrhardt, A. A. (1974). Prenatal androgen, intelligence, and cognitive sex differences. In R. C. Friedman, R. M. Richart, & R. L. Vande Wiele (Eds.), Sex differences in behavior (pp. 53–76). New York: Wiley.
Berenbaum, S. A. (1999). Effects of early androgens on sex-typed activities and interests in adolescents with congenital adrenal hyperplasia. Hormones and Behavior, 35, 102–110.
Berenbaum, S. A. (2001). Cognitive function in congenital adrenal hyperplasia. Endocrinology and Metabolism Clinics of North America, 30, 173–192.
Bodner, G. M., & Guay, R. B. (1997). The Purdue visualization of rotations test. The Chemical Educator, 2, 1–18.
Borenstein, M., Hedges, L., Higgins, J., & Rothstein, H. (2005). Comprehensive meta-analysis Version 2. Englewood, NJ: Biostat.
Bowman, R. E., MacLusky, N. J., Sarmiento, Y., Frankfurt, M., Gordon, M., & Luine, V. N. (2004). Sexually dimorphic effects of prenatal stress on cognition, hormonal responses, and central neurotransmitters. Endocrinology, 145, 3778–3787.
Brown, W. M., Hines, M., Fane, B. A., & Breedlove, S. M. (2002). Masculinized finger length patterns in human males and females with congenital adrenal hyperplasia. Hormones and Behavior, 42, 380–386.
Buck, J. J., Williams, R. M., Hughes, I. A., & Acerini, C. L. (2003). In-utero androgen exposure and 2nd to 4th digit length ratio-comparisons between healthy control and females with classical congenital adrenal hyperplasia. Human Reproduction, 18, 976–979.
Cohen, J. (1988). Statistical power for the behavioral sciences (2nd ed.). Hillsdale, NJ: Erlbaum.
Cole-Harding, S., Morstad, A. L., & Wilson, J. R. (1988). Spatial ability in members of opposite-sex twin pairs. Behavior Genetics, 18, 710.
Coolican, J., & Peters, M. (2003). Sexual dimorphism in the 2D/4D ratio and its relation to mental rotation performance. Evolution and Human Behavior, 24, 179–183.
Cooper, L. A., & Shepard, R. N. (1973). Chronometric studies of the rotation of mental images. In W. G. Chase (Ed.), Visual information processing (pp. 75–176). Oxford: Academic Press.
Csatho, A., Osvath, A., Karadi, K., Bicsak, E., Manning, J. T., & Kallai, J. (2003). Spatial navigation related to the ratio of second to fourth digit length in women. Learning and Individual Differences, 13, 239–249.
Dawson, J. L., Cheung, Y. M., & Lau, R. T. (1975). Developmental effects of neonatal sex hormones on spatial and activity skills in the white rat. Biological Psychology, 3, 213–229.
Dorr, H. G., & Sippell, W. G. (1993). Prenatal dexamethasone treatment in pregnancies at risk for congenital adrenal hyperplasia due to 21-hydroxylase deficiency: Effect on midgestational amniotic fluid steroid levels. Journal of Clinical Endocrinology and Metabolism, 76, 117–120.
Driscoll, I., Hamilton, D. A., Petropoulos, H., Yeo, R. A., Brooks, W. M., Baumgartner, R. N., et al. (2003). The aging hippocampus: Cognitive, biochemical and structural findings. Cerebral Cortex, 13, 1344–1351.
Driscoll, I., Hamilton, D. A., Yeo, R. A., Brooks, W. M., & Sutherland, R. J. (2005). Virtual navigation in humans: The impact of age, sex, and hormones on place learning. Hormones and Behavior, 47, 326–335.
Dureman, I., Kebbon, L., & Osterberg, E. (1971). Manual till DS-batteriet. Stockholm: Psykologiforlaget.
Duval, S. J., & Tweedie, R. L. (2000). A non-parametric “trim and fill” method of accounting for publication bias in meta-analysis. Journal of the American Statistical Association, 95, 89–98.
Ekstrom, R. B., French, J. W., Harman, H. H., & Dermen, D. (1976). Manual for kit of factor-referenced cognitive tests. Princeton, NJ: Educational Testing Service.
Grimshaw, G. M., Sitarenios, G., & Finegan, J. A. (1995). Mental rotation at 7 years: Relations with prenatal testosterone levels and spatial play experiences. Brain and Cognition, 29, 85–100.
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.
Healy, W. (1914). A pictorial completion test. Psychological Review, 21, 189–203.
Helleday, J., Bartfai, A., Ritzen, E. M., & Forsman, M. (1994). General intelligence and cognitive profile in women with congenital adrenal hyperplasia (CAH). Psychoneuroendocrinology, 19, 343–356.
Hines, M. (2004). Brain gender. New York: Oxford University Press.
Hines, M., Fane, B. A., Pasterski, V. L., Mathews, 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.
Hojbjerg Gravholt, C., Svenstrup, B., Bennett, P., & Sandahl Christiansen, J. (1999). Reduced androgen levels in adult turner syndrome: Influence of female sex steroids and growth hormone status. Clinical Endocrinology, 50, 791–800.
Imperato-McGinley, J., Peterson, R. E., Gautier, T., Cooper, G., Danner, R., Arthur, A., et al. (1982). Hormonal evaluation of a large kindred with complete androgen insensitivity: Evidence for secondary 5 alpha-reductase deficiency. Journal of Clinical Endocrinology and Metabolism, 54, 931–941.
Imperato-McGinley, J., Pichardo, M., Gautier, T., Voyer, D., & Bryden, M. P. (1991). Cognitive abilities in androgen-insensitive subjects: Comparison with control males and females from the same kindred. Clinical Endocrinology, 34, 341–347.
Isgor, C., & Sengelaub, D. R. (1998). Prenatal gonadal steroids affect adult spatial behavior, CA1 and CA3 pyramidal cell morphology in rats. Hormones and Behavior, 34, 183–198.
Isgor, C., & Sengelaub, D. R. (2003). Effects of neonatal gonadal steroids on adult CA3 pyramidal neuron dendritic morphology and spatial memory in rats. Journal of Neurobiology, 55, 179–190.
Jackson, D. N. I., Vernon, P. A., & Jackson, D. N. (1993). Dynamic spatial performance and general intelligence. Intelligence, 17, 451–460.
Jager, A. O., & Althoff, K. (1983). WILDE-intelligenz-test. Gottingen: Hogrefe.
Jonasson, Z. (2005). Meta-analysis of sex differences in rodent models of learning and memory: A review of behavioral and biological data. Neuroscience and Biobehavioral Reviews, 28, 811–825.
Joseph, R., Hess, S., & Birecree, E. (1978). Effects of hormone manipulations and exploration on sex differences in maze learning. Behavioral Biology, 24, 364–377.
Kempel, P., Gohlke, B., Klempau, J., Zinsberger, P., Reuter, M., & Hennig, J. (2005). Second-to-fourth digit lengths, testosterone and spatial ability. Intelligence, 33, 215–230.
Kitraki, E., Kremmyda, O., Youlatos, D., Alexis, M. N., & Kittas, C. (2004). Gender-dependent alterations in corticosteroid receptor status and spatial performance following 21 days of restraint stress. Neuroscience, 125, 47–55.
Maccoby, E. E., & Jacklin, C. N. (1974). The psychology of sex differences. Stanford, CA: Stanford University Press.
Malas, M. A., Dogan, S., Hilal Evcil, E., & Desdicioglu, K. (2006). Fetal development of the hand, digits and digit ratio (2D:4D). Early Human Development, 82, 469–475.
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.
Mann, V. A., Sasanuma, S., Sakuma, N., & Masaki, S. (1990). Sex differences in cognitive abilities: A cross-cultural perspective. Neuropsychologia, 28, 1063–1077.
Manning, J. T. (2002). Digit ratio: A pointer to fertility, behavior, and health. New Brunswick, NJ: Rutgers University Press.
Manning, J. T., Bundred, P. E., Newton, D. J., & Flanagan, B. F. (2003). The second to fourth digit ratio and variation in the androgen receptor gene. Evolution and Human Behavior, 24, 399–405.
Manning, J. T., Scutt, D., Wilson, J., & Lewis-Jones, D. I. (1998). The ratio of the 2nd and 4th digit length: A predictor of sperm numbers and concentrations of testosterone, luteinizing hormone and oestrogen. Human Reproduction, 13, 3000–3004.
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.
Mayes, J. T., & Jahoda, G. (1988). Patterns of visual-spatial performance and ‘spatial ability’: Dissociation of ethnic and sex differences. British Journal of Psychology, 79, 105–119.
McBurney, D. H., Gaulin, S. J. C., Devineni, T., & Adams, C. (1997). Superior spatial ability of women: Stronger evidence for the gathering hypothesis. Evolution and Human Behavior, 18, 167–174.
McFadden, D., Loehlin, J. C., Breedlove, S. M., Lippa, R. A., Manning, J. T., & Rahman, Q. (2005). A reanalysis of five studies on sexual orientation and the relative length of the 2nd and 4th fingers (the 2D:4D ratio). Archives of Sexual Behavior, 34, 341–356.
McFadden, D., & Schubel, E. (2003). The relationships between otoacoustic emissions and relative lengths of fingers and toes in humans. Hormones and Behavior, 43, 421–429.
McGuire, L. S., Ryan, K. O., & Omenn, G. S. (1975). Congenital adrenal hyperplasia. II. Cognitive and behavioral studies. Behavior Genetics, 5, 175–188.
Morris, R. G. M. (1981). Spatial localization does not require the presence of local cues. Learning and Motivation, 12, 239–260.
Nijhuis-van der Sanden, M. W., Eling, P. A., & Otten, B. J. (2003). A review of neuropsychological and motor studies in Turner Syndrome. Neuroscience and Biobehavioral Reviews, 27, 329–338.
Nunez, J. L., & McCarthy, M. M. (2003). Estradiol exacerbates hippocampal damage in a model of preterm infant brain injury. Endocrinology, 144, 2350–2359.
Okten, A., Kalyoncu, M., & Yaris, N. (2002). The ratio of second- and fourth-digit lengths and congenital adrenal hyperplasia due to 21-hydroxylase deficiency. Early Human Development, 70, 47–54.
O’Shaughnessy, P. J., Baker, P. J., & Johnston, H. (2006). The foetal Leydig cell—Differentiation, function and regulation. International Journal of Andrology, 29, 90–95.
Owen, K., & Lynn, R. (1993). Sex differences in primary cognitive abilities among blacks, Indians and whites in South Africa. Journal of Biosocial Science, 25, 557–560.
Pang, S., Levine, L. S., Cederqvist, L. L., Fuentes, M., Riccardi, V. M., Holcombe, J. H., et al. (1980). Amniotic fluid concentrations of delta 5 and delta 4 steroids in fetuses with congenital adrenal hyperplasia due to 21 hydroxylase deficiency and in anencephalic fetuses. Journal of Clinical Endocrinology and Metabolism, 51, 223–229.
Perlman, S. M. (1973). Cognitive abilities of children with hormone abnormalities: Screening by psychoeducational tests. Journal of Learning Disabilities, 6, 26–34.
Peters, M., Manning, J. T., & Reimers, S. (2007). The effects of sex, sexual orientation, and digit ratio (2D:4D) on mental rotation performance. Archives of Sexual Behavior, 36, 251–260.
Poulin, M., O’Connell, R. L., & Freeman, L. M. (2004). Picture recall skills correlate with 2D:4D ratio in women but not in men. Evolution and Human Behavior, 25, 174–181.
Puts, D. A., Gaulin, S. J., & Breedlove, S. M. (2007). Sex differences in spatial ability: Evolution, hormones and the brain. In S. M. Platek, J. P. Keenan, & T. K. Shackelford (Eds.), Evolutionary cognitive neuroscience (pp. 329–379). Cambridge, MA: MIT Press.
Putz, D. A., Gaulin, S. J., Sporter, R. J., & McBurney, D. H. (2004). Sex hormones and finger length: What does 2D:4D indicate? Evolution and Human Behavior, 25, 182–199.
Rahman, Q., Wilson, G. D., & Abrahams, S. (2004). Biosocial factors, sexual orientation and neurocognitive functioning. Psychoneuroendocrinology, 29, 867–881.
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.
Ripa, C. P. L., Johannsen, T. H., Mortensen, E. L., & Muller, J. (2003). General cognitive functions, mental rotations ability, and handedness in adult females with congenital adrenal hyperplasia [Abstract]. Hormones and Behavior, 44, 72.
Roof, R. L. (1993). Neonatal exogenous testosterone modifies sex difference in radial arm and Morris water maze performance in prepubescent and adult rats. Behavioural Brain Research, 53, 1–10.
Roof, R. L., & Havens, M. D. (1992). Testosterone improves maze performance and induces development of a male hippocampus in females. Brain Research, 572, 310–313.
Ross, J. L., Stefanatos, G. A., Kushner, H., Zinn, A., Bondy, C., & Roeltgen, D. (2002). Persistent cognitive deficits in adult women with Turner syndrome. Neurology, 58, 218–225.
Rothstein, H., Sutton, A. J., & Borenstein, M. (2005). Publication bias in meta analysis: Prevention, assessment and adjustments. Chichester, UK: Wiley.
Sanders, G., Bereckzei, T., Csatho, A., & Manning, J. T. (2005). The ratio of the 2nd to 4th finger length predicts spatial ability in men but not women. Cortex, 41, 789–795.
Scarbrough, P. S., & Johnston, V. S. (2005). Individual differences in women’s facial preferences as a function of digit ratio and mental rotation ability. Evolution and Human Behavior, 26, 509–526.
Shepard, R. N., & Metzler, J. (1971). Mental rotation of three dimensional objects. Science, 171, 701–703.
Silverman, I., & Eals, M. (1992). Sex differences in spatial abilities: Evolutionary theory and data. In J. Barkow, L. Cosmides, & J. Tooby (Eds.), The adapted mind: Evolutionary psychology and the generation of culture (pp. 533–549). New York: Oxford University Press.
Stewart, J., Skvarenina, A., & Pottier, J. (1975). Effects of neonatal androgens on open-field behavior and maze learning in the prepubescent and adult rat. Physiology and Behavior, 14, 291–295.
Thurstone, L. L., & Thurstone, T. G. (1963). Primary mental abilities. Chicago: Science Research Associates.
van Anders, S. M., & Hampson, E. (2005). Testing the prenatal androgen hypothesis: Measuring digit ratios, sexual orientation, and spatial abilities in adults. Hormones and Behavior, 47, 92–98.
Vandenberg, S. G., & Kuse, A. R. (1978). Mental rotations: A group test of three-dimensional spatial visualization. Perceptual and Motor Skills, 47, 599–604.
Vicedomini, J. P., Nonneman, A. J., DeKosky, S. T., & Scheff, S. W. (1986). Perinatal glucocorticoids disrupt learning: A sexually dimorphic response. Physiology and Behavior, 36, 145–149.
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.
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.
Williams, T. J., Pepitone, M. E., Christensen, S. E., Cooke, B. M., Huberman, A. D., Breedlove, N. J., et al. (2000). Finger-length ratios and sexual orientation. Nature, 404, 455–456.
Wudy, S. A., Dorr, H. G., Solleder, C., Djalali, M., & Homoki, J. (1999). Profiling steroid hormones in amniotic fluid of midpregnancy by routine stable isotope dilution/gas chromatography-mass spectrometry: Reference values and concentrations in fetuses at risk for 21-hydroxylase deficiency. Journal of Clinical Endocrinology and Metabolism, 84, 2724–2728.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Puts, D.A., McDaniel, M.A., Jordan, C.L. et al. Spatial Ability and Prenatal Androgens: Meta-Analyses of Congenital Adrenal Hyperplasia and Digit Ratio (2D:4D) Studies. Arch Sex Behav 37, 100–111 (2008). https://doi.org/10.1007/s10508-007-9271-3
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10508-007-9271-3