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Dopamine receptor D2 (DRD2), dopamine transporter solute carrier family C6, member 4 (SLC6A3), and catechol-O-methyltransferase (COMT) genes as moderators of the relation between maternal history of maltreatment and infant emotion regulation

Published online by Cambridge University Press:  14 August 2017

Vanessa Villani ,
Jaclyn Ludmer ,
Andrea Gonzalez ,
Robert Levitan ,
James Kennedy ,
Mario Masellis ,
Vincenzo S. Basile ,
Christine Wekerle  and
Leslie Atkinson
Vanessa Villani
Affiliation:
Ryerson University
Jaclyn Ludmer
Affiliation:
Ryerson University
Andrea Gonzalez
Affiliation:
McMaster University
Robert Levitan
Affiliation:
University of Toronto Centre for Addiction and Mental Health
James Kennedy
Affiliation:
University of Toronto Centre for Addiction and Mental Health
Mario Masellis
Affiliation:
Sunnybrook Health Sciences Centre
Vincenzo S. Basile
Affiliation:
Sunnybrook Health Sciences Centre
Christine Wekerle
Affiliation:
McMaster University
Leslie Atkinson*
Affiliation:
Ryerson University
*
Address correspondence and reprint requests to: Leslie Atkinson, Department of Psychology, Ryerson University, 350 Victoria Street, Toronto, Ontario M5B 2K3, Canada; E-mail: [email protected].
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Abstract

Although infants less than 18 months old are capable of engaging in self-regulatory behavior (e.g., avoidance, withdrawal, and orienting to other aspects of their environment), the use of self-regulatory strategies at this age (as opposed to relying on caregivers) is associated with elevated behavioral and physiological distress. This study investigated infant dopamine-related genotypes (dopamine receptor D2 [DRD2], dopamine transporter solute carrier family C6, member 4 [SLC6A3], and catechol-O-methyltransferase [COMT]) as they interact with maternal self-reported history of maltreatment to predict observed infant independent emotion regulation behavior. A community sample (N = 193) of mother–infant dyads participated in a toy frustration challenge at infant age 15 months, and infant emotion regulation behavior was coded. Buccal cells were collected for genotyping. Maternal maltreatment history significantly interacted with infant SLC6A3 and COMT genotypes, such that infants with more 10-repeat and valine alleles of SLC6A3 and COMT, respectively, relative to infants with fewer or no 10-repeat and valine alleles, utilized more independent (i.e., maladaptive) regulatory behavior if mother reported a more extensive maltreatment history, as opposed to less. The findings indicate that child genetic factors moderate the intergenerational impact of maternal maltreatment history. The results are discussed in terms of potential mechanism of Gene × Environment interaction.

Type
Regular Articles
Information
Development and Psychopathology , Volume 30 , Issue 2 , May 2018 , pp. 581 - 592
Copyright
Copyright © Cambridge University Press 2017 

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Footnotes

This research was supported by funds from the Canadian Institutes of Health Research (MOP-64301), Ryerson University, and the Centre for Addiction and Mental Health. The authors acknowledge the contributions of Dr. Susan Goldberg, a Co-Principal Investigator on the grant that supported this work. She died prior to completion of the project, but her influence pervades the manuscript. We thank Emilie Boucher and Monica Tan, as well as other research assistants and students who contributed a great many hours to this project. Of course, we also greatly appreciate the time and effort of the mothers and babies who volunteered to participate in this project.

References

Ainsworth, M. D. S., Blehar, M. C., Waters, E., & Wall, S. (1978). Patterns of attachment: A psychological study of the strange situation. Hillsdale, NJ: Erlbaum.Google Scholar
Atkinson, L., Gonzalez, A., Kashy, D. A., Basile, V. S., Masellis, M., Pereira, J., … Levitan, R. (2013). Maternal sensitivity and infant and mother adrenocortical function across challenges. Psychoneuroendocrinology, 38, 2943–2951. doi:10.1016/j.psyneuen.2013.08.001Google Scholar
Atkinson, L., Jamieson, B., Khoury, J., Ludmer, J., & Gonzalez, A. (2016). Stress physiology in infancy and early childhood: Cortisol flexibility, attunement and coordination. Journal of Neuroendocrinology, 28. doi:10.1111/jne.12408Google Scholar
Atkinson, L., Paglia, A., Coolbear, J., Niccols, A., Poulton, L., Leung, E., & Chisholm, V. C. (2000). L’ évaluation de la sensibilité maternelle dans le contexte de la sécurité d'attachment: Une méta-analyse [Assessing maternal sensitivity in the context of attachment security: A meta-analysis]. In Tarabulsy, G. M., Larose, S., Pederson, D. R., & Moran, G. (Eds.), Attachement et développement: Le rôle des premieres relations dans le développement humain [Attachment and development: The role of first relationships in human development] (pp. 27–56). Québec: Presses de l'Université du Québec.Google Scholar
Beck, A. T., Steer, R. A., & Brown, G. K. (1996). Manual for the Beck Depression Inventory (2nd ed.). San Antonio, TX: Psychological Corporation.Google Scholar
Belsky, J., & Pluess, M. (2009). Beyond diathesis stress: Differential susceptibility to environmental influences. Psychological Bulletin, 135, 885–908. doi:10.1037/a0017376Google Scholar
Bernstein, D. P., & Fink, L. (1998). Childhood Trauma Questionnaire: A retrospective self-report. Professional manual. New York: Psychological Corporation.Google Scholar
Bernstein, D. P., Fink, L., Handelsman, L., Foote, J., Lovejoy, M., Wenzel, K., … Ruggeriero, J. (1994). Initial reliability and validity of a new retrospective measure of child abuse and neglect. American Journal of Psychiatry, 151, 1132–1136. doi:10.1176/ajp.151.8.1132Google Scholar
Bernstein, D. P., Stein, J. A., Newcomb, M. D., Walker, E., Pogge, D., Ahluvalia, T., … Zule, W. (2003). Development and validation of a brief screening version of the childhood trauma questionnaire. Child Abuse and Neglect, 27, 169–190. doi:10.1016/S0145-2134(02)00541-0Google Scholar
Bos, S. C., Pereira, A. T., Marques, M., Maia, B., Soares, M. J., Valente, J., … Azevedo, M. H. (2009). The BDI-II factor structure in pregnancy and postpartum: Two or three factors? European Psychiatry, 24, 334–340. doi:10.1016/j.eurpsy.2008.10.003Google Scholar
Bradley, B., Westen, D., Mercer, K. B., Binder, E. B., Jovanovic, T., Crain, D., … Heim, C. (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:10.1017/S0954579411000162Google Scholar
Brand, S. R., & Brennan, P. A. (2009). Impact of antenatal and postpartum maternal mental illness: How are the children? Clinical Obstetrics and Gynecology, 52, 441–455. doi:10.1097/GRF.0b013e3181b52930Google Scholar
Braungart-Rieker, J. M., & Stifter, C. A. (1996). Infants’ responses to frustrating situations: Continuity and change in reactivity and regulation. Child Development, 67, 1767–1779. doi:10.1111/j.1467-8624.1996.tb01826.xGoogle Scholar
Brooks, K., Xu, X., Zhou, K., Neale, B., Lowe, N., Aneey, R., … Johansson, L. (2006). The analysis of 51 genes in DSM-IV combined type attention deficit hyperactivity disorder: Association signals in DRD4, DAT1, and 16 other genes. Molecular Psychiatry, 11, 934–953. doi:10.1038/sj.mp.4001902Google Scholar
Brummelte, S., & Galea, L. A. M. (2010). Depression during pregnancy and postpartum: Contribution of stress and ovarian hormones. Progress in Neuro-Psychoparmacology and Biological Psychiatry, 34, 766–776. doi:10.1016/j.pnpbp.2009.09.006Google Scholar
Calkins, S. D., Gill, K. L., Johnson, M. C., & Smith, C. L. (1999). Emotional reactivity and emotional regulation strategies as predictors of social behaviour with peers during toddlerhood. Social Development, 8, 310–334. doi:10.1111/1467-9507.00098Google Scholar
Cardon, L. R., & Palmer, L. J. (2003). Population stratification and spurious allelic association. Lancet, 361, 598–604. doi:10.1016/S0140-6736(03)12520-2Google Scholar
Carpenter, L. L., Carvalho, J. P., Tyrka, A. R., Wier, L. M., Mello, A. F., Mello, M. F., … Price, L. H. (2007). Decreased adrenocorticotropic hormone and cortisol responses to stress in health adults reporting significant childhood maltreatment. Biological Psychiatry, 62, 1080–1087. doi:10.1016/j.biopsych.2007.05.002Google Scholar
Cicchetti, D. (Ed.). (1989). Rochester symposium on developmental psychopathology: The emergence of a discipline (Vol. 1). Hillsdale, NJ: Erlbaum.Google Scholar
Cicchetti, D., Rogosch, F. A., & Toth, S. L. (2006). Fostering secure attachment in infants in maltreating families through preventive interventions. Development and Psychopathology, 18, 623–649. doi:10.1017/S0954579406060329Google Scholar
Cicchetti, D., & Toth, S. L. (2009). The past achievements and future promises of developmental psychopathology: The coming of age of a discipline. Journal of Child Psychology and Psychiatry, 50, 16–25. doi:10.1111/j.1469-7610.2008.01979.xGoogle Scholar
Cirulli, F., Berry, A., & Alleva, E. (2003). Early disruption of the mother–infant relationship: Effects on brain plasticity and implications for psychopathology. Neuroscience & Biobehavioral Reviews, 27, 73–82. doi:10.1016/S0149-7634(03)00010-1Google Scholar
Collins, L. M., Schafer, J. L., & Kam, C. M. (2001). A comparison of inclusive and restrictive strategies in modern missing data procedures. Psychological Methods, 6, 330–351. doi:10.1037//1082-989X.6.4.330Google Scholar
Collishaw, S., Dunn, J., O'Connor, T. G., & Golding, J. (2007). Maternal childhood abuse and offspring adjustment over time. Development and Psychopathology, 19, 367–383. doi:10.1017/S0954579407070186Google Scholar
Diener, M. L., Mangelsdorf, S. C., McHale, J. L., & Frosch, C. A. (2002). Infants’ behavioral strategies for emotion regulation with fathers and mothers: Associations with emotional expressions and attachment quality. Infancy, 3, 153–174. doi:10.1207/S15327078IN302_3Google Scholar
Dozois, D. J. A., Dobson, K. S., & Ahnberg, J. L. (1998). A psychometric evaluation of the Beck Depression Inventory—II. Psychological Assessment, 10, 83–89.Google 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. doi:10.1176/appi.aip.2011.11020191Google Scholar
Eisenberg, N., Cumberland, A., Spinrad, T. L., Fabes, R. A., Shepard, S. A., Reiser, M., … Guthrie, I. K. (2001). The relations of regulation and emotionality to children's externalizing and internalizing problem behavior. Child Development, 72, 1112–1134. doi:10.1111/1467-8624.00337Google Scholar
Enlow, M. B., Kullowatz, A., Staudenmayer, J., Spasojevic, J., Ritz, T., & Wright, R. J. (2009). Associations of maternal lifetime trauma and perinatal traumatic stress symptoms with infant cardiorespiratory reactivity to psychological challenge. Psychosomatic Medicine, 71, 607–614. doi:10.1097/PSY.0b013e3181ad1c8bGoogle Scholar
Frigerio, A., Ceppi, E., Rusconi, M., Giorda, R., Raggi, M. E., & Fearon, P. (2009). The role played by the interaction between genetic factors and attachment in the stress response in infancy. Journal of Child Psychology and Psychiatry, 50, 1513–1522. doi:10.1111/j.1469-7610.2009.02126.xGoogle Scholar
Galvin, M., Shekhar, A., Simon, J., Stilwell, B., Eyck, R. T., Laite, G., … Blix, S. (1991). Low dopamine-beta-hydroxylase: A biological sequale of abuse and neglect? Psychiatry Research, 39, 1–11.Google Scholar
Hane, A. A., & Philbrook, L. E. (2012). Beyond licking and grooming: Maternal regulation of infant stress in the context of routine care. Parenting: Science and Practice, 12, 144–153. doi:10.1080/15295192.2012.683341Google Scholar
Holmboe, K., Nemoda, Z., Fearon, R. M. P., Csibra, G., Sasvari-Szakely, M., & Johnson, M. H. (2010). Polymorphisms in dopamine system genes are associated with individual differences in attention in infants. Developmental Psychology, 46, 404–416. doi:10.1037/a0018180Google Scholar
Keller, M. C. (2014). Gene × Environment interaction studies have not properly controlled for potential confounders: The problem and the (simple) solution. Biological Psychiatry, 75, 18–24. doi:10.1016/j.biopsych.2013.09.006Google Scholar
Khoury, J. E., Gonzalez, A., Levitan, R., Masellis, M., Basile, V., & Atkinson, L. (2015). Infant emotion regulation strategy moderates relations between self-reported maternal depressive symptoms and infant HPA activity. Infant and Child Development, 25, 64–83. doi:10.1002/icd.1916Google Scholar
Kopp, C. (1989). Regulation of distress and negative emotions: A development view. Developmental Psychology, 25, 243–254.Google Scholar
Lam, S., Dickerson, S. S., Zoccola, P. M., & Zalvidar, F. (2009). Emotion regulation and cortisol reactivity to a social-evaluative speech task. Psychoneuroendocrinology, 34, 1355–1362. doi:10.1016/j.psyneuen.2009.04.006Google Scholar
Laucht, M., Skowronek, M. H., Becker, K., Schmidt, M. H., Esser, G., Schulze, T. G., & Rietschel, M. (2007). Interacting effects of dopamine transporter gene and psychosocial adversity on attention-deficit/hyperactivity disorder symptoms among 15-year-olds from a high-risk community sample. Archives of General Psychiatry, 64, 585–590.Google Scholar
Little, R. J. (1988). A test of missing completely at random for multivariate data with missing values. Journal of the American Statistical Association, 83, 1198–1202.Google Scholar
Ludmer, J. A., Levitan, R., Gonzalez, A., Kennedy, J., Villani, V., Masellis, M., … Atkinson, L. (2015). DRD2 and SLC6A3 moderate impact of maternal depressive symptoms on infant cortisol. Psychoneuroendocrinology, 62, 243–251. doi:10.1016/j.psyneuen.2015.08.026Google Scholar
Manian, N., & Bornstein, M. H. (2009). Dynamics of emotion regulation in infants of clinically depressed and nondepressed mothers. Journal of Child Psychology and Psychiatry, 50, 1410–1418. doi:10.1111/j.1469-7610.2009.02166.xGoogle Scholar
Markant, J., Cicchetti, D., Hetzel, S., & Thomas, K. M. (2014). Contributions of COMT Val158Met to cognitive stability and flexibility in infancy. Developmental Science, 17, 396–411. doi:10.1111/desc.12128Google Scholar
Meaney, M. J., Brake, W., & Gratton, A. (2002). Environmental regulation of the development of mesolimbic dopamine systems: A neurobiologicqal mechanism for vulnerability to drug abuse. Psychoneuroendocrinology, 27, 127–138.Google Scholar
Miller, E. A., Green, A. E., Fettes, D. L., & Aarons, G. A. (2011). Prevalence of maltreatment among youths in public sectors of care. Child Maltreatment, 16, 196–204. doi:10.1177/1077559511415091Google Scholar
Mills-Koonce, W., Propper, C. B., Gariepy, J., Blair, C., Garrett-Peters, P., & Cox, M. J. (2007). Bidirectional genetic and environmental influences on mother and child behavior: The family system as the unit of analyses. Development and Psychopathology, 19, 1073–1087. doi:10.1017/S0954579407000545Google Scholar
Min, M. O., Singer, L. T, Minnes, S., Kim, H., & Short, E. (2012). Mediating links between maternal childhood trauma and preadolescent behavioral adjustment. Journal of Interpersonal Violence, 28, 831–851. doi:10.1177/0886260512455868Google Scholar
Miranda, J. K., de la Osa, N., Granero, R., & Ezpeleta, L. (2013). Maternal childhood abuse, intimate partner violence, and child psychopathology: The mediator role of mothers’ mental health. Violence Against Women, 19, 50–68. doi:10.1177/1077801212475337Google Scholar
Murray, L., & Cooper, P. J. (1997). Postpartum depression and child development. Psychological Medicine, 27, 253–260.Google Scholar
Paivio, S. C., & Cramer, K. M. (2004). Factor structure and reliability of the Childhood Trauma Questionnaire in a Canadian undergraduate student sample. Child Abuse and Neglect, 28, 889–904.Google Scholar
Pears, K. C., & Capaldi, D. M. (2001). Intergenerational transmission of abuse: A two-generational prospective study of an at-risk sample. Child Abuse and Neglect, 25, 1439–1461. doi:10.1016/S0145-2134(01)00286-1Google Scholar
Pederson, D. R., Moran, G., Sitko, C., & Campbell, K. (1990). Maternal sensitivity and the security of infant-mother attachment: A Q-sort study. Child Development, 61, 1974–1983.Google Scholar
Pereira, J., Vickers, K., Atkinson, L., Gonzalez, A., Wekerle, C., & Levitan, R. (2012). Parenting stress mediates between maternal maltreatment history and maternal sensitivity in a community sample. Child Abuse and Neglect, 36, 433–437. doi:10.1016/j.chiabu.2012.01.006Google Scholar
Prentice, D. A., & Miller, D. T. (1992). When small effects are impressive. Psychological Bulletin, 112, 160–164.Google Scholar
Propper, C., Moore, G. A., Mills-Koonce, W., Halpern, C. T., Hill-Soderlund, A., Calkins, S. D., … Cox, M. (2008). Gene-environment contributions to the development of infant vagal reactivity: The interaction of dopamine and maternal sensitivity. Child Development, 79, 1377–1394. doi:10.1111/j.1467-8624.2008.01194Google Scholar
Roberts, R., O'Connor, T., Dunn, J., & Golding, J. (2004). The effects of child sexual abuse in later family life; mental health, parenting and adjustment of offspring. Child Abuse and Neglect, 28, 525–545. doi:10.1016/j.chiabu.2003.07.006Google Scholar
Roisman, G. I., Newman, D. A., Fraley, 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. doi:10.1017/S0954579412000065Google Scholar
Rothbart, M., & Derryberry, D. (1981). Development of individual differences in infant temperament. In Lamb, M. & Brown, A. (Eds.), Advances in developmental psychology (Vol. 1, pp. 37–87). Hillsdale, NJ: Erlbaum.Google Scholar
Salgado-Pineda, P., Delaveau, P., Blin, O., & Nieoullon, A. (2005). Dopaminergic contribution to the regulation of emotional perception. Clinical Neuropharmacology, 28, 228–237.Google Scholar
Schofield, T. J., Lee, R. D., & Merrick, M. T. (2013). Safe, stable, nurturing relationships as a moderator of intergenerational continuity of child maltreatment: A meta-analysis. Journal of Adolescent Health, 53, 532–538. doi:10.1016/j.adohealth.2013.05.004Google Scholar
Spinhoven, P., Penninx, B. W., Hickendorff, M., van Hemert, A. M., Bernstein, D. P., & Elzinga, B. M. (2014). Childhood Trauma Questionnaire: Factor structure, measurement invariance, and validity across emotional disorders. Psychological Assessment, 26, 717–729. doi:10.1037/pas0000002Google Scholar
Stifter, C. A., & Braungart, J. M. (1995). The regulation of negative reactivity in infancy: Function and development. Developmental Psychology, 31, 448–455.Google Scholar
Streiner, D. L. (2003). Being inconsistent about consistency: When coefficient alpha does and doesn't matter. Journal of Personality Assessment, 80, 217–222.Google Scholar
Streiner, D. L., & Norman, G. R. (2008). Health measurement scales: A practical guide to their development and use. New York: Oxford University Press.Google Scholar
Vandenbergh, D. J., Persico, A. M., Hawkins, A. L., Griffin, C. A., Li, X., Jabs, E. W., & Uhi, G. R. (1992). Human dopamine transporter gene (DAT1) maps to chromosome 5p15.3 and displays a VNTR. Genomics, 14, 1104–1106.Google Scholar
Voelker, P., Sheese, B. E., Rothbart, M. K., & Posner, M. I. (2009). Variations in catechol-O-methyltransferase gene interact with parenting to influence attention in early development. Neuroscience, 164, 121–130. doi:10.1016/j.neuroscience.2009.05.059Google Scholar
Wager, T. D., Davidson, M. L., Hughes, B. L., Lindquist, M. A., & Ochsner, K. N. (2008). Prefrontal-subcortical pathways mediating successful emotion regulation. Neuron, 59, 1037–1050.Google Scholar