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Youth temperament, harsh parenting, and variation in the oxytocin receptor gene forecast allostatic load during emerging adulthood

Published online by Cambridge University Press:  13 June 2016

Gene H. Brody ,
Tianyi Yu ,
Allen W. Barton ,
Gregory E. Miller  and
Edith Chen
Gene H. Brody*
Affiliation:
University ofGeorgia
Tianyi Yu
Affiliation:
University ofGeorgia
Allen W. Barton
Affiliation:
University ofGeorgia
Gregory E. Miller
Affiliation:
Northwestern University
Edith Chen
Affiliation:
Northwestern University
*
Address correspondence and reprint requests to: Gene H. Brody, University of Georgia, Center for Family Research, 1095 College Station Road, Athens, GA 30602-4527; E-mail: gbrody@uga.edu.
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Abstract

An association has been found between receipt of harsh parenting in childhood and adult health problems. However, this research has been principally retrospective, has treated children as passive recipients of parental behavior, and has overlooked individual differences in youth responsivity to harsh parenting. In a 10-year multiple-wave prospective study of African American families, we addressed these issues by focusing on the influence of polymorphisms in the oxytocin receptor gene (OXTR), variants of which appear to buffer or amplify responses to environmental stress. The participants were 303 youths, with a mean age of 11.2 at the first assessment, and their parents, all of whom were genotyped for variations in the rs53576 (A/G) polymorphism. Teachers rated preadolescent (ages 11 to 13) emotionally intense and distractible temperaments, and adolescents (ages 15 and 16) reported receipt of harsh parenting. Allostatic load was assessed during young adulthood (ages 20 and 21). Difficult preadolescent temperament forecast elevated receipt of harsh parenting in adolescence, and adolescents who experienced harsh parenting evinced high allostatic load during young adulthood. However, these associations emerged only among children and parents who carried A alleles of the OXTR genotype. The results suggest the oxytocin system operates along with temperament and parenting to forecast young adults’ allostatic load.

Type
Regular Articles
Information
Development and Psychopathology , Volume 29 , Issue 3 , August 2017 , pp. 791 - 803
Copyright
Copyright © Cambridge University Press 2016 

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Footnotes

The research reported in this article was supported by Grant P30 DA027827 from the National Institute on Drug Abuse and Grant R01 HD030588 from the National Institute of Child Health and Human Development.

References

Aiken, L. S., & West, S. G. (1991). Multiple regression: Testing and interpreting interactions. Thousand Oaks, CA: Sage.Google Scholar
Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2008). Oxytocin receptor (OXTR) and serotonin transporter (5-HTT) genes associated with observed parenting. Social Cognitive and Affective Neuroscience, 3, 128–134.CrossRefGoogle ScholarPubMed
Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2014). A sociability gene? Meta-analysis of oxytocin receptor genotype effects in humans. Psychiatric Genetics, 24, 45–51.CrossRefGoogle ScholarPubMed
Beach, S. R. H., Lei, M. K., Brody, G. H., Yu, T., & Philibert, R. A. (2014). Nonsupportive parenting affects telomere length in young adulthood among African Americans: Mediation through substance use. Journal of Family Psychology, 28, 967–972.CrossRefGoogle ScholarPubMed
Belsky, J. (1997). Variation in susceptibility to environmental influence: An evolutionary argument. Psychological Inquiry, 8, 182–186.CrossRefGoogle Scholar
Belsky, J., & Pluess, M. (2009). Beyond diathesis stress: Differential susceptibility to environmental influences. Psychological Bulletin, 135, 885–908.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Brody, G. H., Chen, Y.-F., Kogan, S. M., Yu, T., Molgaard, V. K., DiClemente, R. J., et al. (2012). Family-centered program to prevent substance use, conduct problems, and depressive symptoms in Black adolescents. Pediatrics, 129, 108–115.CrossRefGoogle ScholarPubMed
Brody, G. H., Ge, X., Conger, R. D., Gibbons, F. X., Murry, V. M., Gerrard, M., et al. (2001). The influence of neighborhood disadvantage, collective socialization, and parenting on African American children's affiliation with deviant peers. Child Development, 72, 1231–1246.CrossRefGoogle ScholarPubMed
Brody, G. H., Murry, V. M., Gerrard, M., Gibbons, F. X., Molgaard, V., McNair, L., et al. (2004). The Strong African American Families program: Translating research into prevention programming. Child Development, 75, 900–917.CrossRefGoogle ScholarPubMed
Brody, G. H., Yu, T., Chen, Y.-F., Kogan, S. M., Evans, G. W., Beach, S. R. H., et al. (2013). Cumulative socioeconomic status risk, allostatic load, and adjustment: A prospective latent profile analysis with contextual and genetic protective factors. Developmental Psychology, 49, 913–927.CrossRefGoogle ScholarPubMed
Campbell, A. (2010). Oxytocin and human social behavior. Personality and Social Psychology Review, 14, 281–295.CrossRefGoogle ScholarPubMed
Capaldi, D. M., & Rothbart, M. K. (1992). Development and validation of an early adolescent temperament measure. Journal of Early Adolescence, 12, 153–173.CrossRefGoogle Scholar
Caspi, A., Hariri, A. R., Holmes, A., Uher, R., & Moffitt, T. E. (2010). Genetic sensitivity to the environment: The case of the serotonin transporter gene and its implications for studying complex diseases and traits. FOCUS, 8, 398–416.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Cicchetti, D., & Rogosch, F. A. (2012). Gene × Environment interaction and resilience: Effects of child maltreatment and serotonin, corticotropin releasing hormone, dopamine, and oxytocin genes. Development and Psychopathology, 24, 411–427.CrossRefGoogle ScholarPubMed
Cicchetti, D., & Toth, S. L. (2005). Child maltreatment. Annual Review of Clinical Psychology, 1, 409–438.CrossRefGoogle ScholarPubMed
Contreras, L. N., Hane, S., & Tyrrell, J. B. (1986). Urinary cortisol in the assessment of pituitary-adrenal function: Utility of 24-hour and spot determinations. Journal of Clinical Endocrinology and Metabolism, 62, 965–969.CrossRefGoogle ScholarPubMed
Costa, B., Pini, S., Gabelloni, P., Abelli, M., Lari, L., Cardini, A., et al. (2009). Oxytocin receptor polymorphisms and adult attachment style in patients with depression. Psychoneuroendocrinology, 34, 1506–1514.CrossRefGoogle ScholarPubMed
Creswell, K. G., Wright, A. C., Troxel, W. M., Ferrell, R. E., Flory, J. D., & Manuck, S. B. (2015). OXTR polymorphism predicts social relationships through its effects on social temperament. Social Cognitive and Affective Neuroscience, 10, 869–876.CrossRefGoogle ScholarPubMed
Danese, A., & McEwen, B. S. (2012). Adverse childhood experiences, allostasis, allostatic load, and age-related disease. Physiology & Behavior, 106, 29–39.CrossRefGoogle ScholarPubMed
Danese, A., Moffitt, T. E., Harrington, H., Milne, B. J., Polanczyk, G., Pariante, C. M., et al. (2009). Adverse childhood experiences and adult risk factors for age-related disease: Depression, inflammation, and clustering of metabolic risk markers. Archives of Pediatrics and Adolescent Medicine, 163, 1135–1143.CrossRefGoogle ScholarPubMed
Davenport, E., Yap, M. B. H., Simmons, J. G., Sheeber, L. B., & Allen, N. B. (2011). Maternal and adolescent temperament as predictors of maternal affective behavior during mother-adolescent interactions. Journal of Adolescence, 34, 829–839.CrossRefGoogle ScholarPubMed
Dube, S. R., Fairweather, D., Pearson, W. S., Felitti, V. J., Anda, R. F., & Croft, J. B. (2009). Cumulative childhood stress and autoimmune diseases in adults. Psychosomatic Medicine, 71, 243–250.CrossRefGoogle ScholarPubMed
Else-Quest, N. M., Hyde, J. S., Goldsmith, H. H., & Van Hulle, C. A. (2006). Gender differences in temperament: A meta-analysis. Psychological Bulletin, 132, 33–72.CrossRefGoogle ScholarPubMed
Evans, G. W. (2003). A multimethodological analysis of cumulative risk and allostatic load among rural children. Developmental Psychology, 39, 924–933.CrossRefGoogle ScholarPubMed
Hammen, C., Bower, J. E., & Cole, S. W. (2015). Oxytocin receptor gene variation and differential susceptibility to family environment in predicting youth borderline symptoms. Journal of Personality Disorders, 29, 177–192.CrossRefGoogle ScholarPubMed
Israel, S., Lerer, E., Shalev, I., Uzefovsky, F., Riebold, M., Laiba, E., et al. (2009). The oxytocin receptor (OXTR) contributes to prosocial fund allocations in the Dictator Game and the Social Value Orientations task. PLOS ONE, 4, e5535.CrossRefGoogle ScholarPubMed
Kamarck, T. W., Jennings, J. R., Debski, T. T., Glickman-Weiss, E., Johnson, P. S., Eddy, M. J., et al. (1992). Reliable measures of behaviorally-evoked cardiovascular reactivity from a PC-based test battery: Results from student and community samples. Psychophysiology, 29, 17–28.CrossRefGoogle ScholarPubMed
Karlamangla, A. S., Singer, B. H., & Seeman, T. E. (2006). Reduction in allostatic load in older adults is associated with lower all-cause mortality risk: MacArthur studies of successful aging. Psychosomatic Medicine, 68, 500–507.CrossRefGoogle ScholarPubMed
Keltikangas-Järvinen, L., Pulkki-Råback, L., Puttonen, S., Viikari, J., & Raitakari, O. T. (2006). Childhood hyperactivity as a predictor of carotid artery intima media thickness over a period of 21 years: The Cardiovascular Risk in Young Finns Study. Psychosomatic Medicine, 68, 509–516.CrossRefGoogle Scholar
Kim, K. J., Conger, R. D., Lorenz, F. O., & Elder, G. H. Jr. (2001). Parent-adolescent reciprocity in negative affect and its relation to early adult social development. Developmental Psychology, 37, 775–790.CrossRefGoogle ScholarPubMed
Kim-Cohen, J., Caspi, A., Taylor, A., Williams, B., Newcombe, R., Craig, I. W., et al. (2006). MAOA, maltreatment, and gene-environment interaction predicting children's mental health: New evidence and a meta-analysis. Molecular Psychiatry, 11, 903–913.CrossRefGoogle ScholarPubMed
Klahr, A. M., Klump, K., & Burt, S. A. (2015). A constructive replication of the association between the oxytocin receptor genotype and parenting. Journal of Family Psychology, 29, 91–99.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Kovacs, M. (1979). Treating depressive disorders: The efficacy of behavior and cognitive therapies. Behavior Modification, 3, 496–517.CrossRefGoogle Scholar
Laukkanen, J., Ojansuu, U., Tolvanen, A., Alatupa, S., & Aunola, K. (2014). Child's difficult temperament and mothers’ parenting styles. Journal of Child and Family Studies, 23, 312–323.CrossRefGoogle Scholar
Laursen, B., & Collins, W. A. (2009). Parent-child relationships during adolescence. In Lerner, R. M. & Steinberg, L. (Eds.), Handbook of adolescent psychology (3rd ed., Vol. 2, pp. 3–42). Hoboken, NJ: Wiley.Google Scholar
Lengua, L. J., & Kovacs, E. A. (2005). Bidirectional associations between temperament and parenting and the prediction of adjustment problems in middle childhood. Journal of Applied Developmental Psychology, 26, 21–38.CrossRefGoogle Scholar
Lucht, M. J., Barnow, S., Sonnenfeld, C., Rosenberger, A., Grabe, H. J., Schroeder, W., et al. (2009). Associations between the oxytocin receptor gene (OXTR) and affect, loneliness and intelligence in normal subjects. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 35, 860–866.CrossRefGoogle Scholar
McEwen, B. S. (2000). Allostasis and allostatic load: Implications for neuropsychopharmacology. Neuropsychopharmacology, 22, 108–124.CrossRefGoogle ScholarPubMed
Michalska, K. J., Decety, J., Liu, C., Chen, Q., Martz, M. E., Jacob, S., et al. (2014). Genetic imaging of the association of oxytocin receptor gene (OXTR) polymorphisms with positive maternal parenting. Frontiers in Behavioral Neuroscience, 8, 21.CrossRefGoogle Scholar
Miller, G. E., Chen, E., & Parker, K. J. (2011). Psychological stress in childhood and susceptibility to the chronic diseases of aging: Moving toward a model of behavioral and biological mechanisms. Psychological Bulletin, 137, 959–997.CrossRefGoogle Scholar
Miller, G. E., & Cole, S. W. (2012). Clustering of depression and inflammation in adolescents previously exposed to childhood adversity. Biological Psychiatry, 72, 34–40.CrossRefGoogle ScholarPubMed
Monroe, S. M., & Simons, A. D. (1991). Diathesis-stress theories in the context of life stress research: Implications for the depressive disorders. Psychological Bulletin, 110, 406–425.CrossRefGoogle ScholarPubMed
Patrick, D. L., Cheadle, A., Thompson, D. C., Diehr, P., Koepsell, T., & Kinne, S. (1994). The validity of self-reported smoking: A review and meta-analysis. American Journal of Public Health, 84, 1086–1093.CrossRefGoogle ScholarPubMed
Paulussen-Hoogeboom, M. C., Stams, G. J. J. M., Hermanns, J. M. A., & Peetsma, T. T. D. (2007). Child negative emotionality and parenting from infancy to preschool: A meta-analytic review. Developmental Psychology, 43, 438–453.CrossRefGoogle ScholarPubMed
Posner, M. I., & Rothbart, M. K. (2007). Educating the human brain. Washington, DC: American Psychological Association.CrossRefGoogle Scholar
Poulin, M. J., Holman, E. A., & Buffone, A. (2012). The neurogenetics of nice: Receptor genes for oxytocin and vasopressin interact with threat to predict prosocial behavior. Psychological Science, 23, 446–452.CrossRefGoogle ScholarPubMed
Preacher, K. J., Rucker, D. D., & Hayes, A. F. (2007). Addressing moderated mediation hypotheses: Theory, methods, and prescriptions. Multivariate Behavioral Research, 42, 185–227.CrossRefGoogle ScholarPubMed
Proctor, B. D., & Dalaker, J. (2003). Poverty in the United States: 2002 (Current Population Reports, P60-222). Washington, DC: US Census Bureau.Google Scholar
Pulkki-Råback, L., Elovainio, M., Kivimäki, M., Raitakari, O. T., & Keltikangas-Järvinen, L. (2005). Temperament in childhood predicts body mass in adulthood: The Cardiovascular Risk in Young Finns Study. Health Psychology, 24, 307–315.CrossRefGoogle ScholarPubMed
Putnam, S. P., Ellis, L. K., & Rothbart, M. K. (2001). The structure of temperament from infancy through adolescence. In Eliasz, A. & Angleitner, A. (Eds.), Advances in research on temperament (pp. 165–182). Lengerich, Germany: Pabst Science.Google Scholar
Puttonen, S., Elovainio, M., Kivimäki, M., Koskinen, T., Pulkki-Råback, L., Viikari, J. S. A., et al. (2008). Temperament, health-related behaviors, and autonomic cardiac regulation: The Cardiovascular Risk in Young Finns Study. Biological Psychology, 78, 204–210.CrossRefGoogle ScholarPubMed
Radloff, L. S. (1977). The CES-D Scale: A self-report depression scale for research in the general population. Applied Psychological Measurement, 1, 385–401.CrossRefGoogle Scholar
Repetti, R. L., Taylor, S. E., & Seeman, T. E. (2002). Risky families: Family social environments and the mental and physical health of offspring. Psychological Bulletin, 128, 330–366.CrossRefGoogle ScholarPubMed
Riggin, R. M., & Kissinger, P. T. (1977). Determination of catecholamines in urine by reverse-phase liquid chromatography with electrochemical detection. Analytical Chemistry, 49, 2109–2111.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Roisman, G. I., Newman, D. A., Fraley, R. C., Haltigan, J. D., Groh, A. M., & Haydon, K. C. (2012). Distinguishing differential susceptibility from diathesis–stress: Recommendations for evaluating interaction effects. Development and Psychopathology, 24, 389–409.CrossRefGoogle ScholarPubMed
Rothbart, M. K., & Bates, J. E. (1998). Temperament. In Damon, W. (Ed.), Handbook of child psychology: Vol. 3. Social, emotional and personality development (5th ed., pp. 105–176). New York: Wiley.Google Scholar
Rutter, M. L. (2012). Resilience as a dynamic concept. Development and Psychopathology, 24, 335–344.CrossRefGoogle ScholarPubMed
Sanson, A. V., & Rothbart, M. K. (1995). Child temperament and parenting. In Bornstein, M. H. (Ed.), Handbook of parenting: Vol. 4. Applied and practical parenting (pp. 299–321). Hillsdale, NJ: Erlbaum.Google 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.CrossRefGoogle ScholarPubMed
Seeman, T. E., Singer, B. H., Ryff, C. D., Dienberg Love, G., & Levy-Storms, L. (2002). Social relationships, gender, and allostatic load across two age cohorts. Psychosomatic Medicine, 64, 395–406.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Thompson, S. M., Hammen, C., Starr, L. R., & Najman, J. M. (2014). Oxytocin receptor gene polymorphism (rs53576) moderates the intergenerational transmission of depression. Psychoneuroendocrinology, 43, 11–19.CrossRefGoogle ScholarPubMed
Tost, H., Kolachana, B. S., Hakimi, S., Lemaitre, H., Verchinski, B. A., Mattay, V. S., et al. (2010). A common allele in the oxytocin receptor gene (OXTR) impacts prosocial temperament and human hypothalamic-limbic structure and function. Proceedings of the National Academy of Sciences, 107, 13936–13941.CrossRefGoogle ScholarPubMed
Way, B. M., & Taylor, S. E. (2010). The serotonin transporter promoter polymorphism is associated with cortisol response to psychosocial stress. Biological Psychiatry, 67, 487–492.CrossRefGoogle ScholarPubMed