Skip to main content Accesibility Help

Association between a marker for prenatal testosterone exposure and externalizing behavior problems in children

  • Jianghong Liu (a1), Jill Portnoy (a1) and Adrian Raine (a1)

Prenatal androgen exposure has been associated with aggressive behavior in adults. It is less clear whether this association holds for childhood externalizing behavior. This study tests the hypothesis that increased prenatal androgen exposure is associated with aggressive behavior and attention problems in childhood. The ratio of the length of the second finger digit relative to the fourth digit, which is a marker for prenatal testosterone exposure, was assessed in 239 male and female fifth grade schoolchildren from Jintan, China, together with parent and teacher ratings of aggression and attention problems. Increased aggression and attention problems were both significantly associated with a lower ratio of the length of the second finger digit relative to the fourth digit ratios in boys but not girls. The effects remained significant after controlling for early adversity. These findings are the first to establish a relationship between an indirect indicator of fetal androgen exposure and any child psychopathology in Chinese children, and the observed effect size in boys was stronger than in male adults in Western studies. The results provide limited cross-cultural support for the importance of prenatal androgen exposure in contributing to the development of externalizing behavior problems in children, and they suggest that such effects may be specific to boys who may be relatively more vulnerable to early prenatal influences.

Corresponding author
Address correspondence and reprint requests to: Adrian Raine, Departments of Criminology, Psychiatry, and Psychology, University of Pennsylvania, 3809 Walnut Street, Philadelphia, PA 19104; E-mail:
Hide All
Achenbach, T. M. (1991). Manual for the Child Behavior Checklist/4–18 and 1991 profile. Burlington, VT: University of Vermont, Department of Psychiatry.
Achenbach, T. M., & Rescorla, L. (2000). Manual for the ASEBA Preschool Forms, & Profiles. Burlington, VT: University of Vermont, Department of Psychiatry.
Archer, J. (2004). Sex differences in aggression in real-world settings: A meta-analytic review. Review of General Psychology, 8, 291322.
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, 11151124.
Bailey, A. A., & Hurd, P. L. (2005). Finger length ratio (2D:4D) correlates with physical aggression in men but not in women. Biological Psychology, 68, 215222.
Benderlioglu, Z., & Nelson, R. J. (2004). Digit length ratios predict reactive aggression in women, but not in men. Hormones and Behavior, 46, 558564.
Berenbaum, S. A. (1999). Effects of early androgens on sex-typed activities and interests in adolescents with congenital adrenal hyperplasia. Hormones and Behavior, 35, 102110.
Berenbaum, S. A., & Resnick, S. M. (1997). Early androgen effects on aggression in children and adults with congenital adrenal hyperplasia. Psychoneuroendocrinology, 22, 505515.
Breedlove, S. M. (1994). Sexual differentiation of the human nervous system. Annual Review of Psychology, 45, 389418.
Brennan, P. A., Grekin, E. R., Mortensen, E. L., & Mednick, S. A. (2002). Relationship of maternal smoking during pregnancy with criminal arrest and hospitalization for substance abuse in male and female adult offspring. American Journal of Psychiatry, 159, 4854.
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, 380386.
Burriss, R. P., Little, A. C., & Nelson, E. C. (2007). 2D : 4D and sexually dimorphic facial characteristics. Archives of Sexual Behavior, 36, 377384.
Butovskaya, M. L., Burkova, V., & Mabulla, A. (2010). Sex differences in 2D : 4D ratio, aggression and conflict resolution in African children and adolescents: A cross-cultural study. Journal of Aggression, Conflict and Peace Research, 2, 1731.
Cicchetti, D. (2010). Resilience under conditions of extreme stress: A multilevel perspective. World Psychiatry, 9, 145154.
Cousins, A. J., Fugere, M. A., & Franklin, M. (2009). Digit ratio (2D:4D), mate guarding, and physical aggression in dating couples. Personality and Individual Differences, 46, 709713.
Coyne, S. M., Manning, J. T., Ringer, L., & Bailey, L. (2007). Directional asymmetry (right–left differences) in digit ratio (2D:4D) predict indirect aggression in women. Personality and Individual Differences, 43, 865872.
Csathó, Á., Osváth, A., Karádi, K., Bicsák, É., Manning, J., & Kállai, J. (2001). Spatial navigation related to the ratio of second to fourth digit length in women. Learning and Individual Differences, 13, 239249.
Dietrich, K. N., Ris, M. D., Succop, P. A., Berger, O. G., & Bornschein, R. L. (2001). Early exposure to lead and juvenile delinquency. Neurotoxicology and Teratology, 23, 511518.
Dogan, A., Barut, C., Konuk, N., & Bilge, Y. (2008). Relation of 2D : 4D ratio to aggression and anger. Neurology Psychiatry and Brain Research, 14, 151158.
Ekblad, S. (1990). The Children's Behaviour Questionnaire for completion by parents and teachers in a Chinese sample. Journal of Child Psychology and Psychiatry, 31, 775791.
Fairchild, G., Passamonti, L., Hurford, G., Hagan, C. C., von dem Hagen, E. A., van Goozen, S. H., et al. (2011). Brain structure abnormalities in early-onset and adolescent-onset conduct disorder. American Journal of Psychiatry, 168, 624633.
Fink, B., Manning, J. T., Williams, J. H. G., & Podmore-Nappin, C. (2007). The 2nd to 4th digit ratio and developmental psychopathology in school-aged children. Personality and Individual Differences, 42, 369379.
Finkelstein, J. W., Susman, E. J., Chinchilli, V., Schwab, J., Demers, L., Liben, L., et al. (1995). Testosterone (T) or conjugated estrogen (E) cause increases in aggressive behavior in hypogonadal boys or girls. Pediatric Research, 37, A88.
Gao, Y., Raine, A., Venables, P. H., Dawson, M. E., & Mednick, S. A. (2010). Association of poor childhood fear conditioning and adult crime. American Journal of Psychiatry, 167, 5660.
George, R. (1930). Human finger types. Anatomical Record, 46, 199204.
Geschwind, N., & Galaburda, A. M. (1985). Cerebral lateralization: Biological mechanisms, associations, and pathology: I. A hypothesis and a program for research. Archives of Neurology, 42, 428459.
Giedd, J. N., Clasen, L. S., Lenroot, R., Greenstein, D., Wallace, G. L., Ordaz, S., et al. (2006). Puberty-related influences on brain development. Molecular and Cellular Endocrinology, 254, 154162.
Gobrogge, K. L., Breedlove, S. M., & Klump, K. L. (2008). Genetic and environmental influences on 2D : 4D finger length ratios: A study of monozygotic and dizygotic male and female twins. Archives of Sexual Behavior, 37, 112118.
Goodman, R. (1991). Developmental disorders and structural brain development. In Rutter, M. & Caesar, P. (Eds.), Biological risk factors for psychosocial disorders (pp. 2049). Cambridge: Cambridge University Press.
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, 133144.
Harris, J. A., Rushton, J. P., Hampson, E., & Jackson, D. N. (1996). Salivary testosterone and self-report aggressive and pro-social personality characteristics in men and women. Aggressive Behavior, 22, 321331.
Honekopp, J., & Watson, S. (2011). Meta-analysis of the relationship between digit-ratio 2D:4D and aggression. Personality and Individual Differences, 51, 381386.
Hyde, J. S. (1986). Gender differences in aggression. In Hyde, J. S. & Linn, M. C. (Eds.), The psychology of gender: Advances through meta-analysis (pp. 5166). Baltimore, MD: Johns Hopkins University Press.
James, W. H. (2008). Further evidence that some male-based neurodevelopmental disorders are associated with high intrauterine testosterone concentrations. Developmental Medicine and Child Neurology, 50, 1518.
Knickmeyer, R. C., Woolson, S., Hamer, R. M., Konneker, T., & Gilmore, J. H. (2011). 2D:4D ratios in the first 2 years of life: Stability and relation to testosterone exposure and sensitivity. Hormones and Behavior, 60, 256263.
Kondo, T., Zakany, J., Innis, J. W., & Duboule, D. (1997). Of fingers, toes and penises. Nature, 390(6655), 29.
Lemiere, J., Boets, B., & Danckaerts, M. (2010). No association between the 2D : 4D fetal testosterone marker and multidimensional attentional abilities in children with ADHD. Developmental Medicine & Child Neurology, 52, e202e208.
Levy, J., & Heller, W. (1992). Gender differences in human neuropsychological function. In Arnold, A., Moltz, H. & Ward, I. (Eds.), Sexual differentiation (pp. 245274). New York: Plenum Press.
Liu, J., Cheng, H., & Leung, P. W. (2011). The application of the preschool Child Behavior Checklist and the Caregiver–Teacher Report Form to mainland Chinese children: Syndrome structure, gender differences, country effects, and inter-informant agreement. Journal of Abnormal Child Psychology, 39, 251264.
Liu, J., McCauley, L. A., Zhao, Y., Zhang, H., & Pinto-Martin, J. (2010). Cohort profile: The China Jintan Child Cohort Study. International Journal of Epidemiology, 39, 668674.
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, 2328.
Lyon, G., & Gadisseux, J. F. (1991). Structural abnormalities of the brain in developmental disorders. In Rutter, M. & Caesar, P. (Eds.), Biological risk factors for psychosocial disorders (pp. 119). Cambridge: Cambridge University Press.
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, 469475.
Manning, J. (2002). Digit ratio: A pointer to fertility, behavior and health. New Brunswick, NJ: Rutgers University Press.
Manning, J. T., Baron-Cohen, S., Wheelwright, S., & Sanders, G. (2001). The 2nd to 4th digit ratio and autism. Developmental Medicine and Child Neurology, 43, 160164.
Manning, J. T., Fink, B., Neave, N., & Caswell, N. (2005). Photocopies yield lower digit ratios (2D : 4D) than direct finger measurements. Archives of Sexual Behavior, 34, 329333.
Manning, J. T., Scutt, D., Wilson, J., & Lewis-Jones, D. I. (1998). The ratio of 2nd to 4th digit length: A predictor of sperm numbers and concentrations of testosterone, luteinizing hormone and oestrogen. Human Reproduction, 13, 30003004.
Manning, J. T., Stewart, A., Bundred, P. E., & Trivers, R. L. (2004). Sex and ethnic differences in 2nd to 4th digit ratio of children. Early Human Development, 80, 161168.
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, 6169.
Manning, J. T., Trivers, R. L., Singh, D., & Thornhill, R. (1999). The mystery of female beauty. Nature, 399(6733), 214215.
Martel, M. M. (2009). Conscientiousness as a mediator of the association between masculinized finger-length ratios and attention-deficit/hyperactivity disorder (ADHD). Journal of Child Psychology and Psychiatry, 50, 790798.
Martel, M. M., Gobrogge, K. L., Breedlove, S. M., & Nigg, J. T. (2008). Masculinized finger-length ratios of boys, but not girls, are associated with attention-deficit/hyperactivity disorder. Behavioral Neuroscience, 122, 273281.
Martel, M. M., Klump, K., Nigg, J. T., Breedlove, S. M., & Sisk, C. L. (2009). Potential hormonal mechanisms of attention-deficit/hyperactivity disorder and major depressive disorder: A new perspective. Hormones and Behavior, 55, 465479.
McIntyre, M. H., Barrett, E. S., McDermott, R., Johnson, D. D. P., Cowden, J., & Rosen, S. P. (2007). Finger length ratio (2D : 4D) and sex differences in aggression during a simulated war game. Personality and Individual Differences, 42, 755764.
McIntyre, M. H., Ellison, P. T., Lieberman, D. E., Demerath, E., & Towne, B. (2005). The development of sex differences in digital formula from infancy in the Fels Longitudinal Study. Proceedings of the Royal Society B: Biological Sciences, 272(1571), 1473.
McManus, I., & Bryden, M. (1991). Geschwind's theory of cerebral lateralization: Developing a formal, causal model. Psychological Bulletin, 110, 237.
Moffitt, T. E. (1990). Juvenile delinquency and attention deficit disorder: Boys' developmental trajectories from age 3 to age 15. Child Development, 61, 893910.
Neugebauer, R., Hoek, H. W., & Susser, E. (1999). Prenatal exposure to wartime famine and development of antisocial personality disorder in early adulthood. Journal of the American Medical Association, 282, 455462.
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, 4754.
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, 369382.
PopeH. G., Jr. H. G., Jr., Kouri, E. M., & Hudson, J. I. (2000). Effects of supraphysiologic doses of testosterone on mood and aggression in normal men: A randomized controlled trial. Archives of General Psychiatry, 57, 133140.
Raine, A. (2008). From genes to brain to antisocial behavior. Current Directions in Psychological Science, 17, 323328.
Raine, A. (2011). An amygdala structural abnormality common to two subtypes of conduct disorder: A neurodevelopmental conundrum. American Journal of Psychiatry, 168, 569571.
Raine, A., Venables, P. H., & Williams, M. (1996). Better autonomic conditioning and faster electrodermal half-recovery time at age 15 years as possible protective factors against crime at age 29 years. Developmental Psychology, 32, 624630.
Rubia, K. (2011). “Cool” inferior frontostriatal dysfunction in attention-deficit/hyperactivity disorder versus “hot” ventromedial orbitofrontal–limbic dysfunction in conduct disorder: A review. Biological Psychiatry, 69(12), e6987.
Rutter, M., Hersov, L. A., & Shaffer, D. (1978). Aggression and anti-social behavior in childhood and adolescence. In Rutter, M., Hersov, L. A. & Shaffer, D. (Eds.), Family, area, and school influences in the genesis of conduct disorder (pp. 95113). New York: Wiley.
Tomaszycki, M. L., Gouzoules, H., & Wallen, K. (2005). Sex differences in juvenile rhesus macaque (Macaca mulatta) agonistic screams: Life history differences and effects of prenatal androgens. Devlopmental Psychobiology, 47, 318327.
Trivers, R., Manning, J., & Jacobson, A. (2006). A longitudinal study of digit ratio (2D:4D) and other finger ratios in Jamaican children. Hormones and Behavior, 49, 150156.
Van Goozen, S. H. M., Cohen-Kettenis, P. T., Gooren, L. J. G., Frijda, N. H., & Van De Poll, N. E. (1995). Gender differences in behaviour: Activating effects of cross-sex hormones. Psychoneuroendocrinology, 20, 343363.
Vermeersch, H., T'Sjoen, G., Kaufman, J. M., & Vincke, J. (2008). 2D:4D, sex steroid hormones and human psychological sex differences. Hormones and Behavior, 54, 340346.
Voracek, M., Manning, J. T., & Ponocny, I. (2005). Digit ratio (2D : 4D) in homosexual and heterosexual men from Austria. Archives of Sexual Behavior, 34, 335340.
Weine, A. M., Phillips, J. S., & Achenbach, T. M. (1995). Behavioral and emotional problems among Chinese American children: Parent and teacher reports for ages 6 to 13. Journal of Abnormal Child Psychology, 23, 619639.
Williams, J. H. G., Greenhalgh, K. D., & Manning, J. T. (2003). Second to fourth finger ratio and possible precursors of developmental psychopathology in preschool children. Early Human Development, 72, 5765.
Yang, C. F. J., Gray, P. B., Zhang, J. X., & Pope, H. G. (2009). Second to fourth digit ratios, sex differences, and behavior in Chinese men and women. Social Neuroscience, 4, 4959.
Yu, L., & Winter, S. (2011). Gender atypical behavior in Chinese school-aged children: Its prevalence and relation to sex, age, and only-child status. Journal of Sex Research, 48, 334348.
Zheng, Z. G., & Cohn, M. J. (2011). Developmental basis of sexually dimorphic digit ratios. Proceedings of the National Academy of Sciences of the United States of America, 108, 1628916294.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Development and Psychopathology
  • ISSN: 0954-5794
  • EISSN: 1469-2198
  • URL: /core/journals/development-and-psychopathology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *


Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed