Hostname: page-component-8448b6f56d-xtgtn Total loading time: 0 Render date: 2024-04-18T12:43:09.761Z Has data issue: false hasContentIssue false

Intergenerational transmission of risk for social inhibition: The interplay between parental responsiveness and genetic influences

Published online by Cambridge University Press:  11 February 2013

Misaki N. Natsuaki*
Affiliation:
University of California, Riverside
Leslie D. Leve
Affiliation:
Oregon Social Learning Center
Jenae M. Neiderhiser
Affiliation:
Pennsylvania State University
Daniel S. Shaw
Affiliation:
University of Pittsburgh
Laura V. Scaramella
Affiliation:
University of New Orleans
Xiaojia Ge
Affiliation:
University of Minnesota, Twin Cities
David Reiss
Affiliation:
Yale Child Study Center
*
Address correspondence and reprint requests to: Misaki N. Natsuaki, Department of Psychology, University of California, Riverside, 900 University Avenue, Riverside, CA 92521; E-mail: misaki.natsuaki@ucr.edu.

Abstract

To better understand mechanisms underlying the intergenerational transmission of social anxiety, we used a prospective adoption design to examine the roles of genetic influences (inferred from birth mothers' social phobia) and rearing environment (adoptive mothers' and fathers' responsiveness) on the development of socially inhibited, anxious behaviors in children between 18 and 27 months of age. The sample consisted of 275 adoption-linked families, each including an adopted child, adoptive parents, and a birth mother. Results indicated that children whose birth mothers met criteria for the diagnosis of social phobia showed elevated levels of observed behavioral inhibition in a social situation at 27 months of age if their adoptive mothers provided less emotionally and verbally responsive rearing environments at 18 months of age. Conversely, in the context of higher levels of maternal responsiveness, children of birth mothers with a history of social phobia did not show elevated levels of behavioral inhibition. These findings on maternal responsiveness were replicated in a model predicting parent reports of child social anxiety. The findings are discussed in terms of gene–environment interactions in the intergenerational transmission of social anxiety.

Type
Regular Articles
Copyright
Copyright © Cambridge University Press 2013

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Achenbach, T. M. (1992). Manual for the Child Behavior Checklist 2/3 and 1992 profile. Burlington, VT: University of Vermont, Department Psychiatry.Google Scholar
Ahadi, S., & Diener, E. (1989). Multiple determinants and effect size. Journal of Personality and Social Psychology, 56, 398406.Google Scholar
Aiken, L. S., & West, S. G. (1996). Multiple regression: Testing and interpreting interactions. Thousand Oaks, CA: Sage.Google Scholar
American Psychiatric Association. (1994). Diagnostic and statistical manual of mental disorders (4th ed.). Washington, DC: Author.Google Scholar
Andrews, G., & Peters, L. (1998). The psychometric properties of the Composite International Diagnostic Interview. Social Psychiatry Psychiatric Epidemiology, 33, 8088.Google Scholar
Askey, C., & Field, A. P. (2008). The vicarious learning pathways to fear 40 years on. Clinical Psychology Review, 28, 12491265.CrossRefGoogle Scholar
Bandura, A. (1969). Principles of behavioral modification. New York: Holt, Rinehart & Winston.Google Scholar
Bank, L., Dishion, T. J., Skinner, M., & Patterson, G. R. (1990). Method variance in structural equation modeling: Living with “glop.” In Patterson, G. R. (Ed.), Aggression and depression in family interactions (pp. 247280). Hillsdale, NJ: Erlbaum.Google Scholar
Barry, R. A., Kochanska, G., & Philibert, R. A. (2008). GxE interaction in the organization of attachment: Mothers' responsiveness as a moderator of children's genotypes. Journal of Child Psychology and Psychiatry, 49, 13131320.Google Scholar
Beck, A. T., & Steer, R. A. (1993a). Beck Anxiety Inventory manual. San Antonio, TX: Psychological Corporation.Google Scholar
Beck, A. T., & Steer, R. A. (1993b). Beck Depression Inventory manual. San Antonio, TX: Psychological Corporation.Google Scholar
Beidel, D., & Turner, S. M. (1997). At risk for anxiety: I. Psychopathology in the offspring of anxious parents. Journal of American Academy of Child & Adolescent Psychiatry, 36, 918924.Google Scholar
Belsky, J., Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2007). For better and for worse: Differential susceptilibility to environmental influences. Current Directions in Psychological Science, 16, 300304.CrossRefGoogle Scholar
Biederman, J., Hirshfeld-Becker, D. R., Rosenbaum, J. F., Friedman, D., Snidman, N., Kagan, J., et al. (2001). Further evidence of association between behavioral inhibition and social anxiety in children. American Journal of Psychiatry, 158, 16731679.Google Scholar
Biederman, J., Rosenbaum, J. F., Hirshfeld, D. R., Faraone, S. V., Bolduc, E. A., Gersten, M., et al. (1990). Psychiatric correlates of behavioral inhibition in young children of parents with and without psychiatric disorders. Archives of General Psychiatry, 47, 2126.Google Scholar
Bornstein, M. H., & Tamis-LeMonda, C. S. (1989). Maternal responsiveness and cognitive development in children. In Bornstein, M. H. (Ed.), Maternal responsiveness: Characteristics and consequences (pp. 4961). San Francisco, CA: Jossey–Bass.Google Scholar
Boyce, W. T., & Ellis, B. J. (2005). Biological sensitivity to context: I. An evolutionary–developmental theory of the origins and functions of stress reactivity. Development and Psychopathology, 17, 271301.CrossRefGoogle ScholarPubMed
Bradley, R. H., Caldwell, B. M., & Rock, S. (1988). Home environment and school performance: A ten-year follow-up and examination of three models of environmental action. Child Development, 59, 852867.Google Scholar
Caldwell, B. M., & Bradley, R. H. (1984). Administration manual, revisited edition: The Home Observation for Measurement of the Environment. Little Rock, AR: University of Arkansas Press.Google Scholar
Caspi, A., Moffitt, T. E., Thornston, A., Freedman, D., Amell, J. W., Harrington, H., et al. (1996). The life history calendar: A research and clinical assessment method for collecting retrospective event-history data. International Journal of Methods in Psychiatric Research, 6, 101114.3.3.CO;2-E>CrossRefGoogle Scholar
Cicchetti, D., & Cohen, D. J. (1995). Perspectives on developmental psychopathology. In Cicchetti, D. & Cohen, D. J. (Eds.), Developmental psychopathology: Vol. 1. Theory and methods (pp. 322). New York: Wiley.Google Scholar
Crockenberg, S. C., & Leerkes, E. (2006). Infant and maternal behavior moderate reactivity to novelty to predict anxious behavior at 2.5 years. Development and Psychopathology, 18, 1734.Google Scholar
Davidov, M., & Grusec, J. E. (2006). Untangling the links of parental responsiveness to distress and warmth to child outcomes. Child Development, 77, 4458.Google Scholar
Degnan, K. A., Almas, A. N., & Fox, N. A. (2010). Temperament and the environment in the etiology of childhood anxiety. Journal of Child Psychology and Psychiatry, 51, 497517.Google Scholar
Egger, H. L., & Angold, A. (2006). Common emotional and behavioral disorders in preschool children: Presentation, nosology, and epidemiology. Journal of Child Psychology and Psychiatry, 47, 313337.Google Scholar
Eley, T. C., Bolton, D., O'Connor, T. G., Perrin, S., Smith, P., & Plomin, R. (2003). A twin study of anxiety-related behaviours in pre-school children. Journal of Child Psychology and Psychiatry, 44, 945960.CrossRefGoogle ScholarPubMed
Feldman, R., Greenbaum, C. W., & Yirmiya, N. (1999). Mother–infant affect synchrony as an antecedent of the emergence of self-control. Developmental Psychology, 35, 223231.Google Scholar
Feng, X., Shaw, D. S., & Silk, J. S. (2008). Developmental trajectories of anxiety symptoms among boys across early and middle childhood. Journal of Abnormal Psychology, 117, 3243.CrossRefGoogle ScholarPubMed
Fox, N. A., Nichols, K. E., Hendersen, H. A., Rubin, K., Schmidt, L., Hamer, D., et al. (2005). Evidence for a gene–environment interaction in predicting behavioral inhibition in middle childhood. Psychological Science, 16, 921926.Google Scholar
Ge, X., Natsuaki, M. N., Martin, D., Leve, L. D., Neiderhiser, J. M., Shaw, D. S., et al. (2008). Bridging the divide: Openness in adoption and post-adoption psychological adjustment. Journal of Family Psychology, 22, 529540.Google Scholar
Goldsmith, H. H., & Lemery, K. S. (2000). Linking temperamental fearfulness and anxiety symptoms: A behavior–genetic perspective. Biological Psychiatry, 48, 11991209.Google Scholar
Goldsmith, H. H., & Rothbart, M. K. (1999a). The Laboratory Temperament Assessment Battery (Lab-TAB): Prelocomotor version, edition 3.1. Arlington, TX: University or Texas at Arlington, Department of Psychology.Google Scholar
Goldsmith, H. H., & Rothbart, M. K. (1999b). The Laboratory Temperament Battery (Lab-TAB): Locomotor version, edition 3.1. Arlington, TX: University or Texas at Arlington, Department of Psychology.Google Scholar
Gottlieb, G. (1998). Normally occuring environmental and behavioral influences on gene activities: From central dogma to probabilistic epigenesis. Psychological Review, 105, 792802.Google Scholar
Gottlieb, G. (2007). Probablistic epigenesis. Developmental Science, 10, 111.Google Scholar
Gross, C., & Hen, R. (2004). The developmental origins of anxiety. Nature Reviews Neuroscience, 5, 545552.CrossRefGoogle ScholarPubMed
Hettema, J. M., Neale, M., & Kendler, K. (2001). A review and meta-analysis of the genetic epidemiology of anxiety disorders. American Journal of Psychiatry, 158, 15681578.Google Scholar
Kagan, J., Reznick, J. S., & Snidman, N. (1988). The physiology and psychology of behavioral inhibition in children Child Development, 58, 14591473.Google Scholar
Kendler, K. S., Neale, M., Kessler, R. C., Heath, A. C., & Eaves, L. J. (1992). The genetic epidemiology of phobias in women: The interrelationship of agorophobia, social phobia, situational phobia, and simple phobia. Archives of General Psychiatry, 43, 173281.Google Scholar
Kendler, K. S., Prescott, C. A., Myers, J., & Neale, M. C. (2003). The structure of genetic and environmental risk factors for common psychiatric and substance use disorders in men and women. Archives of General Psychiatry, 60, 929937.CrossRefGoogle ScholarPubMed
Kessler, R. C., McGonagle, K. A., Shanyang, Z., Nelson, C. B., Hughes, M., Eshleman, S., et al. (1994). Lifetime and 12-month prevalence of DSM-III-R psychiatric disorders in the United States. Archives of General Psychiatry, 51, 819.Google Scholar
Kessler, R. C., & Ustun, T. B. (2004). The World Mental Health (WMH) Survey Initiative version of the World Health Organization (WHO) Composite International Diagnostic Interview (CIDI). International Journal of Methods in Psychiatric Research, 13, 93121.CrossRefGoogle ScholarPubMed
Kochanska, G. (1991). Patterns of inhibition to the unfamiliar in children of normal and affectively ill mothers. Child Development, 62, 250263.Google Scholar
Kochanska, G. (1995). Children's temperament, mothers' disciplne, and security of attachment: Multiple pathways to emerging internalization. Child Development, 66, 597615.Google Scholar
Kochanska, G., Aksan, N., & Joy, M. E. (2007). Children's fearfulness as a moderator of parenting in early socialization: Two longitudinal studies. Developmental Psychology, 43, 222237.CrossRefGoogle ScholarPubMed
Kochanska, G., Philibert, R. A., & Barry, R. A. (2009). Interplay of genes and early mother and child relationship in the development of self-regulation from toddler to preschool age. Journal of Child Psychology and Psychiatry, 50, 13311338.Google Scholar
Kraemer, H. C., Measelle, J. R., Ablow, J. C., Essex, M. J., Boyce, W. T., & Kupfer, D. J. (2003). A new approach to integrating data from multiple informants in psychiatric assessment and research: Mixing and matching contexts and perspectives. American Journal of Psychiatry, 160, 15661577.Google Scholar
Kreider, R. N. (2003). Adopted children and stepchildren 2000: Census 2000 special report (No. CENSR-GRV). Washington, DC: Census Bureau.Google Scholar
Landry, S. H., Smith, K. E., Miller-Loncar, C. L., & Swank, P. R. (1997). Predicting cognitive–linguistic and social growth curves from early maternal behaviors in children at varying degrees of biological risk. Developmental Psychology, 33, 10401053.Google Scholar
Landry, S. H., Smith, K. E., & Swank, P. R. (2006). Responsive parenting: Establishing early foundations for social communication, and independent problem-solving skills. Developmental Psychology, 42, 627642.Google Scholar
Landry, S. H., Smith, K. E., Swank, P. R., Assel, M. A., & Vellet, S. (2001). Does early responsive parenting have a special importance for children's development or is consistency across early childhood necessary? Developmental Psychology, 37, 387403.Google Scholar
Lau, J. Y. F., Gregory, A. M., Goldwin, M. A., Pine, D. S., & Eley, T. C. (2007). Assessing gene–environment interactions on anxiety symptom subtypes across childhood and adolescence. Development and Psychopathology, 19, 11291146.Google Scholar
Leve, L. D., Neiderhiser, J. M., Ge, X., Scaramella, L. V., Conger, R. D., Reid, J. B., et al. (2007). The Early Growth and Development Study: A prospective adoption design. Twin Research and Human Genetics, 10, 8495.Google Scholar
Leve, L. D., Neiderhiser, J. M., Scaramella, L. V., & Reiss, D. (2008). The Early Growth and Development Study: Using the prospective adoption design to examine genotype–environment interplay. Acta Psychologica Sinica, 40, 10081115.Google Scholar
Lieb, R., Wittchen, H. U., Hofler, M., Fuetsch, M., Stein, M. B., & Merikangas, K. R. (2000). Parental psychopathology, parenting styles, and the risk of social phobia in offspring: A prospective–longitudinal community study. Archives of General Psychiatry, 57, 859866.Google Scholar
Mancini, C., Van Amerigen, M., Szatmari, P., Fugerer, C., & Boyle, M. (1996). A high-risk pilot study of the children of adults with social phobia. Journal of the American Academy of Child & Adolescent Psychiatry, 35, 15111517.CrossRefGoogle ScholarPubMed
Massey, S. H., Lieberman, D. Z., Reiss, D., Leve, L. D., Shaw, D. S., & Neiderhiser, J. M. (2010). Association of clinical characteristics and cessation of tobacco, alcohol, and illicit drug use during pregnancy. American Journal on Addictions, 20, 143150.Google Scholar
McLeod, B. D., Wood, J. J., & Weisz, J. R. (2007). Examining the association between parenting and childhood anxiety: A meta-analysis. Clinical Psychology Review, 27, 155172.Google Scholar
McNeil, T. F., & Sjostrom, K. (1995). The McNeil–Sjostrom Scale for obstetric complications. Malmo, Sweden: Lund University, University Hospital, Department of Psychiatry.Google Scholar
Micco, J. A., Henin, A., Mick, E., Kim, S., Hopkins, C. A., Biederman, J., et al. (2009). Anxiety and depressive disorders in offspring at high risk for anxiety: A meta-analysis. Journal of Anxiety Disorders, 23, 11581164.Google Scholar
Moggs, K., Bradley, B. P., & Williams, R. (1995). Attentional bias in anxiety and depression: The role of awareness. British Journal of Clinical Psychology, 34, 1736.Google Scholar
Natsuaki, M. N., Ge, X., Leve, L. D., Neiderhiser, J. M., Shaw, D. S., Conger, R. D., et al. (2010). Genetic liability, environment, and the development of fussiness in toddlers: The roles of maternal depression and parental responsiveness. Developmental Psychology, 46, 11471158.Google Scholar
Neiderhiser, J. M. (2011). Gene–environment interplay helps to explain influences of family relationships on adolescent adjustment and development. In Booth, A., McHale, S. M., & Landale, N. S. (Eds.), Biosocial foundations of family processes. New York: Springer.Google Scholar
Nicodemus, K. K., Marenco, S., Batten, A. J., Vakkalanka, R., Egan, M. F., Straub, R., et al. (2008). Serious obstretric complications interact with hypoxia-regulated/vascular-expression genes to influence schizophrenia risk. Molecular Psychiatry, 13, 873877.Google Scholar
Ollendick, T. H., & Hirshfeld-Becker, D. R. (2002). The developmental psychology of social anxiety disorder. Biological Psychiatry, 51, 4458.Google Scholar
Pauli-Pott, U., Friedl, S., Hinney, A., & Hebeberand, J. (2009). Serotonin transporter gene polymorphism (5-HTTLPR), environmental condition, and developing negative emotionality and fear in early childhood. Journal of Neural Transmission, 116, 503512.Google Scholar
Phares, V., & Compas, B. (1992). The role of fathers in child and adolescent psychopathology: Make a room for daddy. Psychological Bulletin, 111, 387412.Google Scholar
Plomin, R., & McGuffin, P. (2003). Psychopathology in the postgenomic era. Annual Review of Psychology, 54, 205228.Google Scholar
Pluess, M., & Belsky, J. (2010). Differential susceptibility to parenting and quality of chld care. Developmental Psychology, 46, 379390.Google Scholar
Preacher, K. J., Curran, P. J., & Bauer, D. J. (2006). Computational tools for probing interactions in multiple linear regression, multilevel modeling, and latent curve analysis. Journal of Educational and Behavioral Statistics, 31, 437448.Google Scholar
Prior, M., Smart, D., Sanson, A., & Oberklaid, F. (2000). Does shy-inhibited temperament in childhood lead to anxiety problems in adolescence? Journal of the American Academy of Child & Adolescent Psychiatry, 39, 461468.Google Scholar
Rapee, R. M., & Spence, S. H. (2004). The etiology of social phobia: Empirical evidence and an initial model. Clinical Psychology Review, 24, 737767.Google Scholar
Rausenbaum, J. F., Biederman, J., Hirshfeld, D. R., Bolduc, E. A., Faraone, S. V., Kagan, J., et al. (1991). Further evidence of an association between behavioral inhibition and anxiety disorders: Results from a family study of children from a non-clinical sample. Journal of Psychiatric Research, 25, 4965.Google Scholar
Rubin, K. H., Burgess, K. B., & Hastings, P. D. (2002). Stability and social–behavioral consequences of toddlers' inhibited temperament and parenting behaviors. Child Development, 73, 483495.Google Scholar
Rutter, M. (2006). Genes and behavior: Nature–nurture interplay explained. Malden, MA: Blackwell.Google Scholar
Rutter, M., Pickles, A., Murray, R., & Eaves, L. J. (2001). Testing hypotheses on specific environmental causal effects on behavior. Psychological Bulletin, 127, 291324.Google Scholar
Shannahan, M., & Hofer, S. M. (2005). Social context in gene–environment interactions: Retrospect and prospect. Journals of Gerontology, 60B, 6576.Google Scholar
Silberg, J., Rutter, M., Neale, M., & Eaves, L. J. (2001). Genetic moderation of environmental risk for depression and anxiety in adolescent girls. British Journal of Psychiatry 179, 116121.Google Scholar
Sroufe, L. A. (1997). Psychopathology as an outcome of development. Development and Psychopathology, 9, 251268.Google Scholar
van der Bruggen, C. O., Stams, G. J. J. M., & Bogels, S. M. (2008). Research reivew: The relation between child and parent anxiety and parental control: A meta-analytic review. Journal of Child Psychology and Psychiatry, 49, 12571269.Google Scholar
Wakshlag, L. S., & Hans, S. L. (1999). Relation of maternal responsiveness during infancy to the development of behavioral problems in high risk youth. Developmental Psychology, 31, 147169.Google Scholar
Warren, S. L., Huston, L., Egeland, B., & Sroufe, L. A. (1997). Child and adolescent anxiety disorders and early attachment. Journal of American Academy of Child & Adolescent Psychiatry, 36, 637644.Google Scholar
Woodruff-Borden, J., Morrow, C., Bourland, S., & Cambron, S. (2002). The behavior of anxious parents: Examining mechanisms of transmission of anxiety from parent to child. Journal of Clinical Child and Adolescent Psychology, 31, 364374.Google Scholar
Yeung, W. J., Sandberg, J. F., Davis-Kean, P. E., & Hofferth, S. L. (2001). Children's time with fathers in intact families. Journal of Marriage and the Family, 63, 136154.Google Scholar
Zeanah, C. H., Boris, N. W., & Scheeringa, M. S. (1997). Psychopathology in infancy. Journal of Child Psychology and Psychiatry, 38, 8199.Google Scholar