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Social stress and the oxytocin receptor gene interact to predict antisocial behavior in an at-risk cohort

Published online by Cambridge University Press:  08 July 2014

Erica L. Smearman ,
D. Anne Winiarski ,
Patricia A. Brennan ,
Jake Najman  and
Katrina C. Johnson
Erica L. Smearman
Affiliation:
Emory University Rollins School of Public Health Emory University School of Medicine
D. Anne Winiarski
Affiliation:
Emory University
Patricia A. Brennan
Affiliation:
Emory University
Jake Najman
Affiliation:
University of Queensland
Katrina C. Johnson*
Affiliation:
Emory University School of Medicine
*
Address correspondence and reprint requests to: Katrina C. Johnson, Emory University School of Medicine, Psychology and Interdisciplinary Sciences Building, 36 Eagle Row Atlanta, GA 30322; E-mail: kcederb@emory.edu.
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Abstract

Polymorphisms in the oxytocin receptor gene are commonly associated with prosocial behaviors in the extant literature, yet their role in antisocial behaviors has rarely been explored, particularly during the transition from adolescence to early adulthood. We examined a prospective cohort (N = 404), collecting youth, mother, and clinician reports of conduct-disordered and antisocial behavior at ages 15 and 20. The oxytocin receptor gene rs53576 polymorphism was hypothesized to interact with social stress to predict antisocial outcomes. Structural equation modeling results revealed a significant main effect at age 15 (p = .025); those with the G allele exhibited higher levels of conduct problems. Structural equation modeling revealed a significant Gene × Environment interaction at age 20 (p = .029); those with the G allele who experienced high social stress exhibited higher levels of antisocial behavior. Heterozygous (AG) grouping models were compared, and parameter estimations supported G dominant groupings. These novel findings suggest that rs53576 polymorphisms may influence social salience and contribute to risk for antisocial outcomes, particularly under conditions of high social stress.

Type
Special Section Articles
Information
Development and Psychopathology , Volume 27 , Issue 1: What Works for Whom? Genetic Moderation of Intervention Efficacy , February 2015 , pp. 309 - 318
Copyright
Copyright © Cambridge University Press 2014 

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References

Achenbach, T. M. (1991). Integrative guide for the 1991 CBCL/4–18, YSR, and TRF profiles. Burlington, VT: University of Vermont, Department of Psychiatry.Google Scholar
Achenbach, T. M., & Edelbrock, C. S. (1983). Manual for the Child Behavior Checklist and Revised Child Behavior Profile. Burlington, VT: University of Vermont, Research Center for Children, Youth, & Families.Google Scholar
Achenbach, T. M., & Rescorla, L. A. (2003). Manual for the ASEBA adult forms & profiles. Burlington, VT: University of Vermont, Research Center for Children, Youth, & Families.Google Scholar
Adrian, C., & Hammen, C. (1993). Stress exposure and stress generation in children of depressed mothers. Journal of Consulting and Clinical Psychology: Journal of Consulting and Clinical Psychology, 61, 354.Google Scholar
Arbuckle, J. K. (2011). IBM® SPSS® AmosTM 20 User's Guide. http://www.amosdevelopment.com. AMOS Development Corporation.Google Scholar
Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2013). A sociability gene? Meta-analysis of oxytocin receptor genotype effects in humans. Psychiatric Genetics. Advance online publication.Google Scholar
Barraza, J. A., & Zak, P. J. (2009). Empathy toward strangers triggers oxytocin release and subsequent generosity. Annals of the New York Academy of Sciences, 1167, 182–189. doi:10.1111/j.1749-6632.2009.04504.xCrossRefGoogle ScholarPubMed
Bartz, J. A., Simeon, D., Hamilton, H., Kim, S., Crystal, S., Braun, A., et al. (2011). Oxytocin can hinder trust and cooperation in borderline personality disorder. Social Cognitive and Affective Neuroscience, 6, 556–563. doi:10.1093/scan/nsq085Google Scholar
Bartz, J. A., Zaki, J., Bolger, N., & Ochsner, K. N. (2011). Social effects of oxytocin in humans: Context and person matter. Trends in Cognitive Sciences, 15, 301–309. doi:10.1016/j.tics.2011.05.002Google Scholar
Beitchman, J. H., Zai, C. C., Muir, K., Berall, L., Nowrouzi, B., Choi, E., et al. (2012). Childhood aggression, callous–unemotional traits and oxytocin genes. European Child & Adolescent Psychiatry, 21, 125. doi:10.1007/s00787-012-0240-6Google Scholar
Bradley, B., Westen, D., Mercer, K. B., Binder, E. B., Jovanovic, T., Crain, D., et al. (2011). Association between childhood maltreatment and adult emotional dysregulation in a low-income, urban, African American sample: Moderation by oxytocin receptor gene. Development and Psychopathology, 23, 439–452. doi:doi:10.1017/S0954579411000162Google Scholar
Brennan, P. A., Hammen, C., Sylvers, P., Bor, W., Najman, J., Lind, P., et al. (2011). Interactions between the COMT Val108/158Met polymorphism and maternal prenatal smoking predict aggressive behavior outcomes. Biological Psychology, 87, 99–105. doi:10.1016/j.biopsycho.2011.02.013Google Scholar
Browne, M. W., Cudeck, R., Bollen, K. A., & Long, J. S. (1993). Alternative ways of assessing model fit. Sage Focus Editions, 154, 136.Google Scholar
Caspi, A., McClay, J., Moffitt, T. E., Mill, J., Martin, J., Craig, I. W., et al. (2002). Role of genotype in the cycle of violence in maltreated children. Science, 297, 851–854. doi:10.1126/science.1072290CrossRefGoogle ScholarPubMed
Chen, F. S., Kumsta, R., von Dawans, B., Monakhov, M., Ebstein, R. P., & Heinrichs, M. (2011). Common oxytocin receptor gene (OXTR) polymorphism and social support interact to reduce stress in humans. Proceedings of the National Academy of Sciences, 108, 19937–19942. doi:10.1073/pnas.1113079108Google Scholar
Chronis, A. M., Lahey, B. B., Pelham, W. E. Jr., Williams, S. H., Baumann, B. L., Kipp, H., et al. (2007). Maternal depression and early positive parenting predict future conduct problems in young children with attention-deficit/hyperactivity disorder. Developmental Psychology, 43, 70–82. doi:10.1037/0012-1649.43.1.70Google Scholar
De Dreu, C. K. W., Greer, L. L., Handgraaf, M. J. J., Shalvi, S., Van Kleef, G. A., Baas, M., et al. (2010). The neuropeptide oxytocin regulates parochial altruism in intergroup conflict among humans. Science, 328, 1408–1411. doi:10.1126/science.1189047CrossRefGoogle ScholarPubMed
Dodge, K. A., & Crick, N. R. (1990). Social information-processing bases of aggressive behavior in children. Personality and Social Psychology Bulletin, 16, 8–22. doi:10.1177/0146167290161002Google Scholar
Dodge, K. A., & Pettit, G. S. (2003). A biopsychosocial model of the development of chronic conduct problems in adolescence. Developmental Psychology, 39, 349–371. doi:10.1037/0012-1649.39.2.349Google Scholar
Duncan, L. E., & Keller, M. C. (2011). A critical review of the first 10 years of candidate gene-by-environment interaction research in psychiatry. American Journal of Psychiatry, 168, 1041–1049.Google Scholar
Fergusson, D. M., Horwood, L. J., & Lynskey, M. (1994). The Childhoods of Multiple Problem Adolescents: A 15-year longitudinal study. Journal of Child Psychology and Psychiatry, 35, 1123–1140. doi:10.1111/j.1469-7610.1994.tb01813.xGoogle Scholar
First, M. B., Gibbon, M., Spitzer, R. L., Williams, J. B. W., & Benjamin, L. S. (1997). Structured Clinical Interview for DSM-IV Axis II Personality Disorders (SCID-II). Washington, DC: American Psychiatric Press.Google Scholar
Gonzaga, G. C., Turner, R. A., Keltner, D., Campos, B., & Altemus, M. (2006). Romantic love and sexual desire in close relationships. Emotion, 6, 163–179. doi:10.1037/1528-3542.6.2.163Google Scholar
Gordon, I., Zagoory-Sharon, O., Schneiderman, I., Leckman, J. F., Weller, A., & Feldman, R. (2008). Oxytocin and cortisol in romantically unattached young adults: Associations with bonding and psychological distress. Psychophysiology, 45, 349–352.CrossRefGoogle ScholarPubMed
Greenberg, M. T., Speltz, M. L., Deklyen, M., & Jones, K. (2001). Correlates of clinic referral for early conduct problems: Variable- and person-oriented approaches. Development and Psychopathology, 13, 255–276.CrossRefGoogle ScholarPubMed
Groppe, S. E., Gossen, A., Rademacher, L., Hahn, A., Westphal, L., Gründer, G., et al. (2013). Oxytocin influences processing of socially relevant cues in the ventral tegmental area of the human brain. Biological Psychiatry, 74, 172–179. doi:10.1016/j.biopsych.2012.12.023Google Scholar
Hammen, C. (1991). Generation of stress in the course of unipolar depression. Journal of Abnormal Psychology, 100, 555–561. doi:10.1037/0021-843x.100.4.555Google Scholar
Hammen, C., & Brennan, P. A. (2001). Depressed adolescents of depressed and nondepressed mothers: Tests of an interpersonal impairment hypothesis. Journal of Consulting and Clinical Psychology, 69, 284–294. doi:10.1037/0022-006x.69.2.284Google Scholar
Hammen, C., Hazel, N. A., Brennan, P. A., & Najman, J. (2012). Intergenerational transmission and continuity of stress and depression: Depressed women and their offspring in 20 years of follow-up. Psychological Medicine, 42, 931–942. doi:10.1017/S0033291711001978Google Scholar
Hazel, N. Â A., Hammen, C., Brennan, P. Â A., & Najman, J. (2008). Early childhood adversity and adolescent depression: The mediating role of continued stress. Psychological Medicine, 38, 581–589. doi:10.1017/S0033291708002857CrossRefGoogle ScholarPubMed
Hooper, D., Coughlan, J., & Mullen, M. R. (2008). Structural equation modelling: Guidelines for determining model fit. Electronic Journal of Business Research Methods, 6, 53–59.Google Scholar
Hu, L. t., & Bentler, P. M. (1999). Cutoff criteria for fit indexes in covariance structure analysis: Conventional criteria versus new alternatives. Structural Equation Modeling, 6, 1–55. doi:10.1080/10705519909540118Google Scholar
Kim, H. S., Sherman, D. K., Sasaki, J. Y., Xu, J., Chu, T. Q., Ryu, C., et al. (2010). Culture, distress, and oxytocin receptor polymorphism (OXTR) interact to influence emotional support seeking. Proceedings of the National Academy of Sciences, 107, 15717–15721. doi:10.1073/pnas.1010830107CrossRefGoogle ScholarPubMed
Kline, R. B. (2010). Principles and practice of structural equation modeling (3rd ed.). New York: Guilford Press.Google Scholar
Kogan, A., Saslow, L. R., Impett, E. A., Oveis, C., Keltner, D., & Rodrigues Saturn, S. (2011). Thin-slicing study of the oxytocin receptor (OXTR) gene and the evaluation and expression of the prosocial disposition. Proceedings of the National Academy of Sciences, 108, 19189–19192. doi:10.1073/pnas.1112658108Google Scholar
Krueger, F., Parasuraman, R., Iyengar, V., Thornburg, M., Weel, J., Lin, M., et al. (2012). Oxytocin receptor genetic variation promotes human trust behavior. Frontiers in Human Neuroscience, 6, 4. doi:10.3389/fnhum.2012.00004Google Scholar
Kumsta, R., & Heinrichs, M. (2013). Oxytocin, stress and social behavior: Neurogenetics of the human oxytocin system. Current Opinion in Neurobiology, 23, 11–16. doi:10.1016/j.conb.2012.09.004Google Scholar
Lim, M. M., & Young, L. J. (2006). Neuropeptidergic regulation of affiliative behavior and social bonding in animals. Hormones and Behavior, 50, 506–517. doi:10.1016/j.yhbeh.2006.06.028CrossRefGoogle ScholarPubMed
Malik, A. I., Zai, C. C., Abu, Z., Nowrouzi, B., & Beitchman, J. H. (2012). The role of oxytocin and oxytocin receptor gene variants in childhood-onset aggression. Genes, Brain and Behavior, 11, 545–551. doi:10.1111/j.1601-183X.2012.00776.xGoogle Scholar
Manolio, T. A., Collins, F. S., Cox, N. J., Goldstein, D. B., Hindorff, L. A., Hunter, D. J., et al. (2009). Finding the missing heritability of complex diseases. Nature, 461, 747–753. doi:10.1038/nature08494Google Scholar
Moffitt, T. E. (1993). Adolescence-limited and life-course-persistent antisocial behavior: A developmental taxonomy. Psychological Review, 100, 674–701. doi:10.1037/0033-295x.100.4.674Google Scholar
Moffitt, T. E., Caspi, A., Harrington, H., & Milne, B. J. (2002). Males on the life-course-persistent and adolescence-limited antisocial pathways: Follow-up at age 26 years. Development and Psychopathology, 14, 179–207.Google Scholar
Najman, J., Bor, W., O'Callaghan, M., Williams, G., Aird, R., & Shuttlewood, G. (2005). Cohort profile: The Mater–University of Queensland Study of Pregnancy (MUSP). International Journal of Epidemiology, 34, 992–997. doi:10.1093/ije/dyi119Google Scholar
Orvaschel, H. (1995). The Schedule for Affective Disorders and Schizophrenia for School-Age Children—Epidemiologic version 5 (K-SADS-E-5). Ft. Lauderdale, FL: Author.Google Scholar
Raine, A. (2002). Biosocial studies of antisocial and violent behavior in children and adults: A review. Journal of Abnormal Child Psychology, 30, 311–326. doi:10.1023/a:1015754122318Google Scholar
Rao, U. M. A., Hammen, C., & Daley, S. E. (1999). Continuity of depression during the transition to adulthood: A 5-year longitudinal study of young women. Journal of the American Academy of Child & Adolescent Psychiatry, 38, 908–915. doi:10.1097/00004583-199907000-00022Google Scholar
Rhee, S. H., & Waldman, I. D. (2002). Genetic and environmental influences on antisocial behavior: A meta-analysis of twin and adoption studies. Psychological Bulletin, 128, 490–529. doi:10.1037/0033-2909.128.3.490Google Scholar
Riem, M. M., Pieper, S., Out, D., Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2011). Oxytocin receptor gene and depressive symptoms associated with physhiological reactivity to infant crying. Social Cognitive and Affective Neuroscience, 6, 294–300.Google Scholar
Rodrigues, S. M., Saslow, L. R., Garcia, N., John, O. P., & Keltner, D. (2009). Oxytocin receptor genetic variation relates to empathy and stress reactivity in humans. Proceedings of the National Academy of Sciences, 106, 21437–21441. doi:10.1073/pnas.0909579106Google Scholar
Saphire-Bernstein, S., Way, B. M., Kim, H. S., Sherman, D. K., & Taylor, S. E. (2011). Oxytocin receptor gene (OXTR) is related to psychological resources. Proceedings of the National Academy of Sciences, 108, 15118–15122. doi:10.1073/pnas.1113137108CrossRefGoogle ScholarPubMed
Shamay-Tsoory, S. G., Fischer, M., Dvash, J., Harari, H., Perach-Bloom, N., & Levkovitz, Y. (2009). Intranasal administration of oxytocin increases envy and schadenfreude (gloating). Biological Psychiatry, 66, 864–870. doi:10.1016/j.biopsych.2009.06.009Google Scholar
Slatkin, M. (2009). Epigenetic inheritance and the missing heritability problem. Genetics, 182, 845–850Google Scholar
Sturge-Apple, M. L., Cicchetti, D., Davies, P. T., & Suor, J. H. (2012). Differential susceptibility in spillover between interparental conflict and maternal parenting practices: Evidence for OXTR and 5-HTT genes. Journal of Family Psychology, 26, 431–442. doi:10.1037/a0028302Google Scholar
Yong, E. (2012). Dark side of the love hormone. New Scientist, 213, 39–41. doi:10.1016/S0262-4079(12)60377-7Google Scholar