Skip to main content Accessibility help
Hostname: page-component-5959bf8d4d-qtfcj Total loading time: 0.601 Render date: 2022-12-08T19:53:19.194Z Has data issue: true Feature Flags: { "useRatesEcommerce": false } hasContentIssue true

Does early maternal responsiveness buffer prenatal tobacco exposure effects on young children's behavioral disinhibition?

Published online by Cambridge University Press:  15 November 2018

Caron A. C. Clark*
Department of Educational Psychology, University of Nebraska-Lincoln, Lincoln, NE, USA
Suena H. Massey
Department of Psychiatry and Behavioral Sciences, Northwestern University Feinberg School of Medicine, Chicago, IL, USA Institute for Innovations in Developmental Sciences, Northwestern University, Chicago, IL, USA
Sandra A. Wiebe
Department of Psychology, University of Alberta, Edmonton, Alberta, Canada
Kimberly Andrews Espy
Office of the Provost, University of San Antonio at Texas, San Antonio, TX, USA; Developmental Cognitive Neuroscience Laboratory, University of Nebraska-Lincoln, Lincoln, NE, USA
Lauren S. Wakschlag
Institute for Innovations in Developmental Sciences, Northwestern University, Chicago, IL, USA Department of Medical Social Sciences, Northwestern University Feinberg School of Medicine, Chicago, IL, USA
Author for correspondence: Caron Clark, Department of Educational Psychology, 241 TEAC Building, University of Nebraska–Lincoln, Lincoln, NE, 68588; E-mail:


Children with prenatal tobacco exposure (PTE) exhibit early self-regulatory impairments, reflecting a life-course persistent propensity toward behavioral disinhibition. Previously, we demonstrated the protective role of parental responsiveness for reducing the risk of exposure-related disruptive behavior in adolescence. Here, we expanded this line of inquiry, examining whether responsiveness moderates the relation of PTE to a broader set of behavioral disinhibition features in early childhood and testing alternative diathesis-stress versus differential susceptibility explanatory models. PTE was assessed prospectively using interviews and bioassays in the Midwestern Infant Development Study (MIDS). Mother-child dyads (N = 276) were re-assessed at approximately 5 years of age in a preschool follow-up. We quantified maternal responsiveness and child behavioral disinhibition using a combination of directly observed activities in the lab and developmentally sensitive questionnaires. Results supported a diathesis-stress pattern. Children with PTE and less responsive mothers showed increased disruptive behavior and lower effortful control compared with children without PTE. In contrast, exposed children with more responsive mothers had self-regulatory profiles similar to their non-exposed peers. We did not observe sex differences. Findings provide greater specification of the protective role of maternal responsiveness for self-regulation in children with PTE and help clarify mechanisms that may underscore trajectories of exposure-related behavioral disinhibition.

Regular Articles
Copyright © Cambridge University Press 2018 

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.)


Ainsworth, M. D. S. (1979). Infant-mother attachment. The American Psychologist, 34(10), 932937. ScholarPubMed
Bale, T. L. (2011). Sex differences in prenatal epigenetic programing of stress pathways. Stress, 14(4), 348356. Scholar
Becker, K., El-Faddagh, M., Schmidt, M. H., Esser, G., & Laucht, M. (2008). Interaction of dopamine transporter genotype with prenatal smoke exposure on ADHD symptoms. Journal of Pediatrics, 152(2), 263270. ScholarPubMed
Beer, C., Israel, C., Johnson, S., Marlow, N., Whitelaw, A., & Glazebrook, C. (2013). Twin birth: An additional risk factor for poorer quality maternal interactions with very preterm infants? Early Human Development, 89(9), 555559. ScholarPubMed
Belsky, J., Bakermans-Kranenburg, M. J., & van Ijzendoorn, M. (2007). For better and for worse: Differential susceptibility to environmental influences. Current Directions in Psychological Science, 16(6), 300304. Scholar
Belsky, J., & Pluess, M. (2009). Beyond diathesis stress: Differential susceptibility to environmental influences. Psychological Bulletin, 135(6), 885908. ScholarPubMed
Bernier, A., Carlson, S. M., & Whipple, N. (2010). From external regulation to self-regulation: Early parenting precursors of young children's executive functioning. Child Development, 81(1), 326339. ScholarPubMed
Betts, K. S., Williams, G. M., Najman, J. M., & Alati, R. (2015). The relationship between maternal depressive, anxious, and stress symptoms during pregnancy and adult offspring behavioral and emotional problems. Depression and Anxiety, 32, 8290. ScholarPubMed
Blair, C., & Raver, C. C. (2015). School readiness and self-regulation: A developmental psychobiological approach. Annual Review of Psychology, 66(1), 711731. ScholarPubMed
Bock, J., Wainstock, T., Braun, K., & Segal, M. (2015). Stress in utero: Prenatal programming of brain plasticity and cognition. Biological Psychiatry, 78(5), 315326. ScholarPubMed
Brooks-Gunn, J., & Klebanov, P. K. (1996). Ethnic differences in children's intelligence test scores: Role of economic deprivation, home environment, and maternal characteristics. Child Development, 67(2), 396408. ScholarPubMed
Bruner, C. (2002). A stitch in time: Calculating the costs of school unreadiness. Washington D.C.: The Finance Project.Google Scholar
Bublitz, M. H., & Stroud, L. R. (2012). Maternal smoking during pregnancy and offspring brain structure and function: Review and agenda for future research. Nicotine & Tobacco Research, 14(4), 388397. ScholarPubMed
Caldwell, B., & Bradley, R. (1984). HOME observation for the measurement of the environment. Little Rock, AR: University of Arkansas.Google Scholar
Carlson, S. M., & Moses, L. J. (2001). Individual differences in inhibitory control and children's theory of mind. Child Development, 72(4), 10321053. ScholarPubMed
Carter, A. S., Gray, S. A. O., Baillargeon, R. H., & Wakschlag, L. S. (2013). A multidimensional approach to disruptive behaviors: Informing life span research from an early childhood perspective. In Tolan, P. H. & Leventhal, B. (Eds.), Disruptive Behavior Disorders (pp. 103135). New York, NY: Springer.CrossRefGoogle Scholar
CDC. (2016). Smoking prevalence and cessation before and during pregnancy: Data from the birth certificate, 2014. Retrieved from Scholar
Chase-Lansdale, L., Wakschlag, L. S., & Brooks-Gunn, J. (1995). A psychological perspective on the development of caring in children and youth: The role of the family. Journal of Adolescence, 18, 515556.CrossRefGoogle Scholar
Chatterton, Z., Hartley, B. J., Seok, M.-H., Mendelev, N., Chen, S., Milekic, M., … Haghighi, F. (2017). In utero exposure to maternal smoking is associated with DNA methylation alterations and reduced neuronal content in the developing fetal brain. Epigenetics & Chromatin, 10(1), 4. ScholarPubMed
Chazan-Cohen, R., Raikes, H., Brooks-Gunn, J., Ayoub, C., Pan, B. A., Kisker, E. E., … Fuligni, A. S. (2009). Low-income children's school readiness: Parent contributions over the first five years. Early Education and Development, 20(6), 958977. Scholar
Clark, C. A. C., Chevalier, N., Nelson, J. M., James, T. D., Garza, J. P., Choi, H.-J., & Espy, K. A. (2016). Executive control in early childhood. Monographs of the Society for Research in Child Development, 81(4), 729. ScholarPubMed
Clark, C. A. C., Espy, K. A., & Wakschlag, L. S. (2016). Developmental pathways from prenatal tobacco and stress exposure to behavioral disinhibition. Neurotoxicology and Teratology, 53, 6474. ScholarPubMed
Clark, C. A. C., Sheffield, T. D., Chevalier, N., Nelson, J. M., Wiebe, S. A., & Espy, K. A. (2013). Charting early trajectories of executive control with the shape school. Developmental Psychology, 49(8), 14811493. ScholarPubMed
Clark, C. A. C., & Woodward, L. J. (2015). Relation of perinatal risk and early parenting to executive control at the transition to school. Developmental Science, 18(4), 525542. Scholar
Cole, P. M., Zahn-Waxler, C., & Smith, K. D. (1994). Expressive control during a disappointment: Variations related to preschoolers’ behavior problems. Developmental Psychology, 30(6), 835846. Scholar
Coolahan, K., McWayne, C., Fantuzzo, J., & Grim, S. (2002). Validation of a multidimensional assessment of parenting styles for low-income African-American families with preschool children. Early Childhood Research Quarterly, 17(3), 356373. Scholar
Cornelius, M. D., Goldschmidt, L., & Day, N. L. (2012). Neurotoxicology and teratology prenatal cigarette smoking: Long-term effects on young adult behavior problems and smoking behavior. Neurotoxicology and Teratology, 34(6), 554559. Scholar
Cornelius, M. D., Goldschmidt, L., De Genna, N. M., & Larkby, C. (2012). Long-term effects of prenatal cigarette smoke exposure on behavior dysregulation among 14-year-old offspring of teenage mothers. Maternal and Child Health Journal, 16, 694705. ScholarPubMed
Cornelius, M. D., Ryan, C. M., Day, N. L., Goldschmidt, L., & Willford, J. A. (2001). Prenatal tobacco effects on neuropsychological outcomes among preadolescents. Journal of Developmental and Behavioral Pediatrics, 22(4), 217225. ScholarPubMed
D'Onofrio, B. M., Singh, A., Iliadou, A., Lambe, M. P., Hultman, C. M., Grann, M., … Lichtenstein, P. (2010). Familial confounding of the association between maternal smoking during pregnancy and offspring criminality: A population-based study in Sweden. Archives of General Psychiatry, 67(5), 529538.CrossRefGoogle ScholarPubMed
de Wolff, M. S., & van Ijzendoorn, M. H. (1997). Sensitivity and attachment: A meta-analysis on parental antecedents of infant attachment. Child Development, 68(4), 571591. ScholarPubMed
Difranza, J. R., Aligne, C. A., & Weitzman, M. (2004). Prenatal and postnatal environmental tobacco exposure and children's health. Pediatrics, 113(4), 10071015.Google ScholarPubMed
Dwyer, J., McQuown, S., & Leslie, F. (2009). The dynamic effects of nicotine on the developing brain. Pharmacology & Therapeutics, 122(2), 125139. ScholarPubMed
Early Childcare Research Network, N. (2005). Characteristics and quality of child care for toddlers and preschoolers. In NICHD (Ed.), Child care and child development: Results from the NICHD study of early child care and youth development (pp. 91102). New York, NY: Guildford Press.Google Scholar
Eiden, R. D., & Leonard, K. E. (2007). A conceptual model for the development of externalizing behavior among kindergarten children of alcoholic families: Role of parenting and children's self-regulation. Developmental Psychology, 43(5), 11871201. ScholarPubMed
Eiden, R. D., Molnar, D. S., Granger, D. A., Colder, C. R., Schuetze, P., & Huestis, M. A. (2015). Prenatal tobacco exposure and infant stress reactivity: Role of child sex and maternal behavior. Developmental Psychobiology, 57(2), 212225. ScholarPubMed
El Marroun, H. Schmidt, M. N., Franken, I. H. A., Jaddoe, V. W. V, Hofman, A., van der Lugt, A., … White, T. (2014). Prenatal tobacco exposure and brain morphology: A prospective study in young children. Neuropsychopharmacology, 39(4), 792800. ScholarPubMed
Ellis, B. J., Boyce, W. T., Belsky, J., Bakermans-Kranenburg, M. J., & van Ijzendoorn, M. H. (2011). Differential susceptibility to the environment: An evolutionary-neurodevelopmental theory. Development and Psychopathology, 23, 728. Scholar
Espy, K. A., Fang, H., Johnson, C., Stopp, C., & Wiebe, S. A. (2011). Prenatal tobacco exposure: Developmental outcomes in the neonatal period. Developmental Psychology, 47, 153156. ScholarPubMed
Estabrook, R., Massey, S. H., Clark, C. A. C., Burns, J. L., Mustanski, B. S., Cook, E. H., … Wakschlag, L. S. (2016). Separating family-level and direct exposure effects of smoking during pregnancy on offspring externalizing symptoms: Bridging the behavior genetic and behavior teratologic divide. Behavior Genetics, 46(3), 389402. ScholarPubMed
Evans, G. W., & Rosenbaum, J. (2008). Self-regulation and the income-achievement gap. Early Childhood Research Quarterly, 23(4), 504514. Scholar
Fang, H., Johnson, C., Chevalier, N., Stopp, C., Wiebe, S., Wakschlag, L. S., & Espy, K. A. (2010). Using propensity score modeling to minimize the influence of confounding risks related to prenatal tobacco exposure. Nicotine and Tobacco Research, 12(12), 12111219. ScholarPubMed
Fang, H., Johnson, C., Stopp, C., & Espy, K. A. (2011). A new look at quantifying tobacco exposure during pregnancy using fuzzy clustering. Neurotoxicology and Teratology, 33(1), 155165. Scholar
Fergusson, D. M., Woodward, L. J., & Horwood, L. J. (1998). Maternal smoking during pregnancy and psychiatric adjustment in late adolescence. Archives of General Psychiatry, 55(8), 721727. ScholarPubMed
Fraley, R. C. (2012). Probing interactions in differential susceptibility research. Retrieved January 1, 2017, from Scholar
Gadow, K. D., & Sprafkin, J. (2000). The Early Childhood Inventory - 4 Screening Manual. Stony Brook, NY: Checkmate Plus.Google Scholar
Gaysina, D., Fergusson, D. M., Leve, L. D., Horwood, J., Reiss, D., Shaw, D. S., … Harold, G. T. (2013). Maternal smoking during pregnancy and offspring conduct problems evidence from 3 independent genetically sensitive research designs. JAMA Psychiatry, 70(9), 956963. ScholarPubMed
Gilman, S. E., Breslau, J., Subramanian, S. V, Hitsman, B., & Koenen, K. C. (2008). Social factors, psychopathology, and maternal smoking during pregnancy. American Journal of Public Health, 98(3), 448453. ScholarPubMed
Godleski, S. A., Eiden, R. D., Schuetze, P., Colder, C. R., & Huestis, M. A. (2016). Tobacco exposure and maternal psychopathology: Impact on toddler problem behavior. Neurotoxicology and Teratology, 57, 8794. ScholarPubMed
Gogtay, N., Giedd, J. N., Lusk, L., Hayashi, K. M., Greenstein, D., Vaituzis, A. C., … Thompson, P. M. (2004). Dynamic mapping of human cortical development during childhood through early adulthood. Proceedings of the National Academy of Sciences of the United States of America, 101(21), 81748179. ScholarPubMed
Gueron-Sela, N., Atzaba-Poria, N., Meiri, G., & Marks, K. (2015). The caregiving environment and developmental outcomes of preterm infants: Diathesis stress or differential susceptibility effects? Child Development, 86(4), 10141030. ScholarPubMed
Hayes, (2018). The Process macro for SPSS and SAS. Retrieved from Scholar
He, X., Lu, J., Dong, W., Jiao, Z., Zhang, C., Yu, Y., … Xu, D. (2017). Prenatal nicotine exposure induces HPA axis-hypersensitivity in offspring rats via the intrauterine programming of up-regulation of hippocampal GAD67. Archives of Toxicology, 91(12), 117. ScholarPubMed
Heath, C. J., & Picciotto, M. R. (2009). Nicotine-induced plasticity during development: Modulation of the cholinergic system and long-term consequences for circuits involved in attention and sensory processing. Neuropharmacology, 56(Suppl 1), 254262. ScholarPubMed
Hill, C., Mascowitz, K., Danis, B., & Wakschlag, L. S. (2008). Validation of a clinically sensitive observational coding system for parenting behaviors: The Parenting Clinical Observation Schedule. Parenting: Science and Practice, 8(2), 153185.CrossRefGoogle Scholar
Himes, S. K., Stroud, L. R., Scheidweiler, K. B., Niaura, R., & Huestis, M. (2013). Prenatal tobacco exposure, biomarkers for tobacco in meconium and neonatal grwoth outcomes. Journal of Pediatrics, 162(5), 970975. Scholar
Hughes, C., Dunn, J., & White, A. (1998). Trick or treat?: Uneven understanding of mind and emotion and executive dysfunction in “hard-to-manage” preschoolers. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 39(7), 981994. ScholarPubMed
Huijbregts, S. C. J., Séguin, J. R., Zoccolillo, M., Boivin, M., & Tremblay, R. E. (2007). Associations of maternal prenatal smoking with early childhood physical aggression, hyperactivity-impulsivity, and their co-occurrence. Journal of Abnormal Child Psychology, 35, 203215. ScholarPubMed
Huijbregts, S. C. J., Seguin, J., Zoccolillo, M., Boivin, M., & Tremblay, R. E. (2008). Maternal prenatal smoking, parental antisocial behavior, and early childhood physical aggression. Development and Psychopathology, 20, 437453. ScholarPubMed
Huijbregts, S. C. J., van Berkel, S. R., Swaab-Barneveld, H., & van Goozen, S. H. M. (2011). Neurobiological and behavioral stress reactivity in children prenatally exposed to tobacco. Psychoneuroendocrinology, 36(6), 913918. ScholarPubMed
Huijbregts, S. C. J., Warren, A. J., De Sonneville, L. M. J., & Swaab-Barneveld, H. (2008). Hot and cool forms of inhibitory control and externalizing behavior in children of mothers who smoked during pregnancy: An exploratory study. Journal of Abnormal Child Psychology, 36, 323333. Scholar
Hutchinson, A. J., Pickett, K. E., Green, J., Wakschlag, L. S., Hutchinson, J., Pickett, E., … Wakschlag, L. S. (2010). Smoking in pregnancy and disruptive behaviour in 3-year-old boys and girls: An analysis of the UK Millennium Cohort Study. Journal of Epidemiology and Community Health, 64(1), 8288. ScholarPubMed
Jacobsen, L. K., Picciotto, M. R., Heath, C. J., Frost, S. J., Tsou, K. A., Dwan, R. A., … Mencl, W. E. (2007). Prenatal and adolescent exposure to tobacco smoke modulates the development of white matter microstructure. Journal of Neuroscience, 27(49), 1349113498. ScholarPubMed
Knopik, V. S., Marceau, K., Bidwell, L. C., Palmer, R. H. C., Smith, T. F., Todorov, A., … Heath, A. C. (2016). Smoking during pregnancy and ADHD risk: A genetically informed, multiple-rater approach. American Journal of Medical Genetics Part B Neuropsychiatric Genetics, 171(7), 941981. Scholar
Kochanska, G., Murray, K. T., & Harlan, E. T. (2000). Effortful control in early childhood: Continuity and change, antecedents, and implications for social development. Developmental Psychology, 36(2), 220232. ScholarPubMed
Kopp, C. B. (1982). Antecedents of self-regulation: A developmental perspective. Developmental Psychology, 18(2), 199214. Scholar
Kristjansson, E. A., Fried, P. A., & Watkinson, B. (1989). Maternal smoking during pregnancy affects children's vigilance performance. Drug and Alcohol Dependence, 24, 1119. ScholarPubMed
Kundakovic, M., & Champagne, F. A. (2015). Early-life experience, epigenetics, and the developing brain. Neuropsychopharmacology, 40(1), 141153. ScholarPubMed
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(4), 627642. ScholarPubMed
Law, K. L., Stroud, L. R., LaGasse, L. L., Niaura, R., Liu, J., & Lester, B. M. (2003). Smoking during pregnancy and newborn neurobehavior. Pediatrics, 111(6), 13181323. ScholarPubMed
Lester, B. M., Lin, H., DeGarmo, D. S., Fisher, P. A., Lagasse, L. L., Levine, T. P., … Higgins, R. D. (2012). Neurobehavioral disinhibition predicts initiation of substance use in children with prenatal cocaine exposure. Drug Alcohol Depend, 126(1–2), 8086. ScholarPubMed
Lester, B. M., & Padbury, J. F. (2009). Third pathophysiology of prenatal cocaine exposure. Developmental Neuroscience, 31, 2335. ScholarPubMed
Li, Y., Gonzalez, P., & Zhang, L. (2012). Fetal stress and programming of hypoxic/ischemic-sensitive phenotype in the neonatal brain: Mechanisms and possible interventions. Progress in Neurobiology, 98(2), 145165. ScholarPubMed
Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., … Meaney, M. J. (1997). Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science, 277(5332), 16591662.CrossRefGoogle ScholarPubMed
Liu, J., Cohen, R. J., Gongvatana, A., Sheinkopf, S. J., & Lester, B. M. (2011). The impact of prenatal exposure to cocaine and tobacco on diffusion tensor imaging and sensation seeking in adolescents. Journal of Pediatrics, 159(5), 771775. ScholarPubMed
Lotfipour, S., Ferguson, E., Leonard, G., Perron, M., Pike, B., Richer, L., & Se, J. R. (2010). Orbitofrontal cortex and drug use during adolescence. Archives of General Psychiatry, 66(11), 12441252.CrossRefGoogle Scholar
Luby, J., Belden, A., Botteron, K., Marrus, N., Harms, M. P., Babb, C., … Barch, D. (2013). The effects of poverty on childhood brain development: The mediating effect of caregiving and stressful life events. JAMA Pediatrics, 167(12), 11351142. ScholarPubMed
Lynch, M. E., Johnson, K. C., Kable, J. A., Carroll, J., & Coles, C. D. (2011). Smoking in pregnancy and parenting stress: Maternal psychological symptoms and socioeconomic status as potential mediating variables. Nicotine and Tobacco Research, 13(7), 532539. ScholarPubMed
Martin, R. P., Dombrowski, S., Mullis, C., Wisenbaker, J., & Huttenen, M. (2006). Smoking during pregnancy: Association with childhood temperament, behavior, and academic performance. Journal of Pediatric Psychology, 31(5), 490500.CrossRefGoogle ScholarPubMed
Maughan, B., Taylor, A., Caspi, A., & Moffitt, T. E. (2004). Prenatal smoking and early childhood conduct problems. Archives of General Psychiatry, 61, 836843. ScholarPubMed
McDonald, S. D., Walker, M., Perkins, S. L., Beyene, J., Murphy, K., Gibb, W., & Ohlsson, A. (2006). The effect of tobacco exposure on the fetal hypothalamic-pituitary-adrenal axis. BJOG, 113(11), 12891295. ScholarPubMed
Merz, E. C., Landry, S. H., Williams, J. M., Barnes, M. A., Eisenberg, N., Spinrad, T. L., … Clancy-Menchetti, J. (2014). Associations among parental education, home environment quality, effortful control, and preacademic knowledge. Journal of Applied Developmental Psychology, 35(4), 304315. ScholarPubMed
Mezzacappa, E., Buckner, J. C., & Earls, F. (2011). Prenatal cigarette exposure and infant learning stimulation as predictors of cognitive control in childhood. Developmental Science, 14(4), 881891. Scholar
Moffitt, T. E. (1993). Adolescence-limited and life-course-persistent antisocial behavior: A developmental taxonomy. Psychological Review, 100(4), 674701. ScholarPubMed
Moffitt, T. E., Arseneault, L., Belsky, D., Dickson, N., Hancox, R. J., Harrington, H., … Caspi, A. (2011). A gradient of childhood self-control predicts health, wealth, and public safety. Proceedings of the National Academy of Sciences of the United States of America, 108(7), 26932698. ScholarPubMed
Monshouwer, K., Huizink, C., Harekeh, Z., Raaijmakers, M. A. J., Reijneveld, S. A., Oldehinkel, A. J., Verhulst, F. C., & Vollebergh, W. A. M. (2011). Prenatal smoking exposure and the risk of behavioral problems and substance use in adolescence: The TRAILS Study. European Addiction Research, 17, 342350. ScholarPubMed
Moos, R. H. (1995). Development and applications of new measures of life stressors, social resources, and coping responses. European Journal of Psychological Assessment, 11(1), 113. Scholar
Moos, R. H., & Moos, B. S. (1994). The Life Stressors and Social Resources Inventory. Odessa, FL: Psychological Assessment Resources.Google Scholar
Mumford, E. A., Hair, E., Yu, T., & Liu, W. (2014). Women's longitudinal smoking patterns from preconception through child's kindergarten entry: Profiles of biological mothers of a 2001 birth cohort. Maternal Child Health Journal, 18(4), 810820. Scholar
Murray, J., Irving, B., Farrington, D. P., Colman, I., & Bloxsom, A. J. (2010). Very early predictors of conduct problems and crime: Results from a national cohort study. Journal of Child Psychology and Psychiatry, 11, 11981207. Scholar
Mychasiuk, R., Muhammad, A., Gibb, R., & Kolb, B. (2013). Long-term alterations to dendritic morphology and spine density associated with prenatal exposure to nicotine. Brain Research, 1499, 5360. ScholarPubMed
Nelson, T., Nelson, J. M., James, T. D., Clark, C. A. C., Kidwell, K. M., & Espy, K. A. (2017). Executive control goes to school: Implications of preschool executive control for observed elementary classroom behavior. Developmental Psychology, 53(5), 836844.CrossRefGoogle Scholar
Nigg, J. T. (2017). Annual Research Review: On the relations among self-regulation, self-control, executive functioning, effortful control, cognitive control, impulsivity, risk-taking, and inhibition for developmental psychopathology. Journal of Child Psychology and Psychiatry and Allied Disciplines, 58(4), 361383. ScholarPubMed
Noland, J. S., Singer, L. T., Short, E. J., Minnes, S., Arendt, R. E., Kirchner, H. L., & Bearer, C. (2005). Prenatal drug exposure and selective attention in preschoolers. Neurotoxicology and Teratology, 27(3), 429438. ScholarPubMed
O'Brien, T. C., Mustanski, B. S., Skol, A., Cook, E. H., & Wakschlag, L. S. (2013). Do dopamine gene variants and prenatal smoking interactively predict youth externalizing behavior? Neurotoxicology and Teratology, 40, 6773. ScholarPubMed
Obradović, J., Bush, N. R., Stamperdahl, J., Adler, N. E., & Boyce, W. T. (2010). Biological sensitivity to context: The interactive effects of stress reactivity and family adversity on socioemotional behavior and school readiness. Child Development, 81(1), 270289. ScholarPubMed
Olivari, M. G., Tagliabue, S., & Confalonieri, E. (2013). Parenting Style and Dimensions Questionnaire: A review of reliability and validity. Marriage and Family Review, 49(6), 465490. Scholar
Paradis, A. D., Fitzmaurice, G., Koenen, K. C., & Buka, S. L. (2011). Maternal smoking during pregnancy and criminal offending among adult offspring. Journal of Epidemiology and Community Health, 65(12), 11451150. ScholarPubMed
Park, A., O'Malley, S. S., King, S. L., & Picciotto, M. R. (2014). Mediating role of stress reactivity in the effects of prenatal tobacco exposure on childhood mental health outcomes. Nicotine & Tobacco Research, 16(2), 174185. ScholarPubMed
Perry, N. B., Mackler, J. S., Calkins, S. D., & Keane, S. P. (2014). A transactional analysis of the relation between maternal sensitivity and child vagal regulation. Developmental Psychology, 50(3), 784793. ScholarPubMed
Pianta, R. C., Nimetz, S. L., & Bennett, E. (1997). Mother-child relationships, teacher-child relationships, and school outcomes in preschool and kindergarten. Early Childhood Research Quarterly, 12(3), 263280. Scholar
Pickett, K. E., Wilkinson, R. G., & Wakschlag, L. S. (2009). The psychosocial context of pregnancy smoking and quitting in the Millennium Cohort Study. Journal of Epidemiology and Community Health, 63, 474480. ScholarPubMed
Pluess, M., & Belsky, J. (2010). Differential susceptibility to parenting and quality child care. Developmental Psychology, 46(2), 379390. ScholarPubMed
Pluess, M., & Belsky, J. (2011). Prenatal programming of postnatal plasticity. Development and Psychopathology, 23(1), 2938. ScholarPubMed
Putnam, S. P., & Rothbart, M. K. (2006). Development of Short and Very Short Forms of the Children's Behavior Questionnaire. Journal of Personality Assessment, 87(1), 103113.CrossRefGoogle Scholar
Rabinowitz, J. A., & Drabick, D. A. G. (2017). Do children fare for better and for worse? Associations among child features and parenting with child competence and symptoms. Developmental Review, 45, 130. Scholar
Ramsay, D. S., Bendersky, M., & Lewis, M. (1996). Effect of prenatal alcohol and cigarette exposure on two and six-month old infants’ adrenocortical reactivity to stress. Journal of Pediatric Psychology, 21(6), 833840. ScholarPubMed
Ridgeway, G. (2006). Assessing the effect of race bias in post-traffic stop outcomes using propensity scores. Journal of Quantitative Criminology, 22(1), 129.CrossRefGoogle Scholar
Robinson, C. C., Mandleco, B., Olsen, S. F., & Hart, C. H. (1999). Authoritative, authoritarian, and permissive parenting practices: Development of a new measure. Psychological Reports, 77, 819830.CrossRefGoogle Scholar
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(2), 389409. ScholarPubMed
Rothbart, M. K., Ahadi, S. A., Hershey, K. L., & Fisher, P. (2001). Investigations of temperament at three to seven years: The Children's Behavior Questionnaire. Child Development, 72(5), 13941408. ScholarPubMed
Rothbart, M. K., Sheese, B. E., Rueda, M. R., & Posner, M. I. (2011). Developing mechanisms of self-regulation in early life. Emotion Review, 3(2), 207213. ScholarPubMed
Roza, S. J., Verhulst, F. C., Jaddoe, V. W. V, Steegers, E. A. P., Mackenbach, J. P., Hofman, A., & Tiemeier, H. (2009). Maternal smoking during pregnancy and child behaviour problems: The Generation R Study. International Journal of Epidemiology, 38(3), 680689. ScholarPubMed
Sameroff, A. (2010). A unified theory of development: A dialectic integration of naure and nurture. Child Development, 81(1), 622. Scholar
Sandman, C. A., Glynn, L. M., & Davis, E. P. (2013). Is there a viability-vulnerability tradeoff? Sex differences in fetal programming. Journal of Psychosomatic Research, 75(4), 327335. Scholar
Schuetze, P., & Eiden, R. (2007). The association between prenatal exposure to cigarettes and infant and maternal negative affect. Infant Behavior and Development, 30(3), 387398. ScholarPubMed
Schuetze, P., Lopez, F., & Granger, D. A. (2009). The association between prenatal exposure to cigarettes and cortisol reactivity in 7-month-old infants. Developmental Psychobiology, 50(8), 819834. Scholar
Shisler, S., Eiden, R. D., Molnar, D. S., Schuetze, P., Coles, C. D., Huestis, M., & Colder, C. R. (2016). Effects of fetal tobacco exposure on focused attention in infancy. Infant Behavior and Development, 45, 810. ScholarPubMed
Simpson, A., & Riggs, K. J. (2006). Conditions under which children experience inhibitory difficulty with a “button-press” go/no-go task. Journal of Experimental Child Psychology, 94, 1826. ScholarPubMed
Slikker, W., Xu, Z. A., Levin, E. D., & Slotkin, T. A. (2005). Mode of action: Disruption of brain cell replication, second messenger, and neurotransmitter systems during development leading to cognitive dysfunction – Developmental neurotoxicity of nicotine. Critical Reviews in Toxicology, 35(8–9), 703711. ScholarPubMed
Slotkin, T. A. (2004). Cholinergic systems in brain development and disruption by neurotoxicants: Nicotine, environmental tobacco smoke, organophosphates. Toxicology and Applied Pharmacology, 198(2), 132151. ScholarPubMed
Slotkin, T. A., MacKillop, E. A., Rudder, C. L., Ryde, I. T., Tate, C. A., & Seidler, F. J. (2007). Permanent, sex-selective effects of prenatal or adolescent nicotine exposure, separately or sequentially, in rat brain regions: Indices of cholinergic and serotonergic synaptic function, cell signaling, and neural cell number and size at 6 months of age. Neuropsychopharmacology, 32(5), 10821097. ScholarPubMed
Slotkin, T. A., Skavicus, S., Card, J., Stadler, A., Levin, E. D., & Seidler, F. J. (2015). Developmental neurotoxicity of tobacco smoke directed toward cholinergic and serotonergic systems: More than just nicotine. Toxicological Sciences, 147(1), 178189. ScholarPubMed
Spinrad, T. L., Eisenberg, N., Silva, K. M., Eggum, N. D., Reiser, M., Edwards, A., … Gaertner, B. M. (2012). Longitudinal relations among maternal behaviors, effortful control and young children's committed compliance. Developmental Psychology, 48(2), 552566. Scholar
Sprafkin, J., Volpe, R. J., Gadow, K. D., Nolan, E. E., & Kelly, K. (2002). A DSM-IV-referenced screening instrument for preschool children: The Early Childhood Inventory-4. Journal of the American Academy of Child and Adolescent Psychiatry, 41(5), 604612. ScholarPubMed
Stroud, L. R., Papandonatos, G. D., Rodriguez, D., Mccallum, M., Salisbury, A. L., Phipps, M. G., … Marsit, C. J. (2014). Maternal smoking during pregnancy and infant stress response: Test of a prenatal programming hypothesis. Psychoneuroendocrinology, 48, 2940. ScholarPubMed
Tandon, M., Si, X., Belden, A., Spitznagel, E., Wakschlag, L. S., & Lubya, J. (2013). Parenting practices in pregnancy smokers compared to non smokers. Journal of Clinical Medical Research, 5(2), 8491. ScholarPubMed
Tarter, R. E. (2002). Etiology of adolescent substance abuse: A developmental perspective. The American Journal on Addictions, 11, 171191. ScholarPubMed
Tarter, R. E., Kirisci, L., Mezzich, A., Cornelius, J., Pajer, K. A., Vanyukov, M., … Clark, D. C. (2003). Neurobehavior disinhibition in childhood predicts early age onset substance use disorder. American Journal of Psychiatry, 160, 10781085.CrossRefGoogle Scholar
Van Ijzendoorn, M. H., Belsky, J., & Bakermans-Kranenburg, M. J. (2012). Serotonin transporter genotype 5HTTLPR as a marker of differential susceptibility: A meta-analysis of child and adolescent gene-by-environment studies. Translational Psychiatry, 2(8), e147. ScholarPubMed
von Suchodoletz, A., Trommsdorff, G., & Heikamp, T. (2011). Linking maternal warmth and responsiveness to children's self-regulation. Social Development, 20(3), 486503. Scholar
Wakschlag, L. S., Briggs-Gowan, M. J., Choi, S. W., Nichols, S. R., Kestler, J., Burns, J. L., … Henry, D. (2014). Advancing a multidimensional, developmental spectrum approach to preschool disruptive behavior. Journal of the American Academy of Child and Adolescent Psychiatry, 53(1), 8296.e3. ScholarPubMed
Wakschlag, L. S., & Hans, S. L. (2002). Maternal smoking during pregnancy and conduct problems in high-risk youth: A developmental framework. Development and Psychopathology, 14, 351369. ScholarPubMed
Wakschlag, L. S., Henry, D. B., Blair, R. J. R., Dukic, V., Burns, J., & Pickett, K. E. (2011). Unpacking the association: Individual differences in the relation of prenatal exposure to cigarettes and disruptive behavior phenotypes. Neurotoxicology and Teratology, 33(1), 145154. ScholarPubMed
Wakschlag, L. S., Kistner, E. O., Pine, D. S., Biesecker, G., Pickett, K. E., Skol, A. D., … Cook, E. (2009). Interaction of prenatal exposure to cigarettes and MAOA genotype in pathways to youth antisocial behavior. Molecular Psychiatry, 15(9), 110. ScholarPubMed
Wakschlag, L. S., Leventhal, B. L., Cook, E., & Pickett, K. E. (2000). Intergenerational health consequences of maternal smoking. TEN, 2(1), 4754.Google Scholar
Wakschlag, L. S., Leventhal, B. L., Pickett, K. E., Pine, D. S., & Carter, A. S. (2006). Elucidating early mechanisms of developmental psychopathology: The case of prenatal smoking and disruptive behavior. Child Development, 77(4), 893906. ScholarPubMed
Wakschlag, L. S., Perlman, S., Blair, R. J. R., Leibenluft, E., Briggs-Gowan, M. J., & Pine, D. S. (2018). The neurodevelopmental basis of early childhood disruptive behavior. Irritable and callous phenotypes as exemplars. American Journal of Psychiatry, 175, 114130.CrossRefGoogle ScholarPubMed
Wakschlag, L. S., Pickett, K. E., Cook, E., Benowitz, N. L., & Leventhal, B. L. (2002). Maternal smoking during pregnancy and severe antisocial behavior in offspring: A review. American Journal of Public Health, 92(6), 966974. ScholarPubMed
Wakschlag, L. S., Tolan, P. H., & Leventhal, B. L. (2010). Research review: “Ain't misbehavin”: Towards a developmentally-specified nosology for preschool disruptive behavior. Journal of Child Psychology and Psychiatry and Allied Disciplines, 51(1), 322. ScholarPubMed
Weaver, K., Campbell, R., Mermelstein, R., & Wakschlag, L. S. (2008). Pregnancy smoking in context: The influence of multiple levels of stress. Nicotine & Tobacco Research, 10(6), 10651073. ScholarPubMed
Wickstrom, R. (2007). Effects of nicotine during pregnancy: Human and experimental evidence. Current Neuropharmacology, 5(3), 213222. ScholarPubMed
Wiebe, S. A., Clark, C. A. C., de Jong, D. M., Chevalier, N., Espy, K. A., & Wakschlag, L. S. (2016). Prenatal tobacco exposure and self-regulation in early childhood: Implications for developmental psychopathology. Development and Psychopathology, 27(2), 397409. Scholar
Wiebe, S. A., Fang, H., Johnson, C., James, K. E., & Espy, K. A. (2014). Determining the impact of prenatal tobacco exposure on self-regulation at 6 months. Developmental Psychology, 50(6), 17461756. ScholarPubMed
Wiebe, S. A., Sheffield, T. D., & Espy, K. A. (2012). Separating the fish from the sharks: A longitudinal study of preschool response inhibition. Child Development, 83(4), 12451261. ScholarPubMed
Willoughby, M. T., Greenberg, M., Blair, C. B., & Stifter, C. (2007). Neurobehavioral consequences of prenatal exposure to smoking at 6 to 8 months of age. Infancy, 12(3), 273301.CrossRefGoogle Scholar
Windham, G. C., Hopkins, B., Fenster, L., & Swan, S. H. (2000). Prenatal active or passive tobacco smoke exposure and the risk of preterm delivery or low birth weight. Epidemiology, 11(4), 427433.CrossRefGoogle ScholarPubMed
Wolfe, C. D., & Bell, M. A. (2004). Working memory and inhibitory control in early childhood: Contributions from physiology, temperament, and language. Developmental Psychobiology, 44(1), 6883. Scholar
Yang, S., Decker, A., & Kramer, M. S. (2013). Exposure to parental smoking and child growth and development: A cohort study. BMC Pediatrics, 13(1), 104. ScholarPubMed
Zucker, R. A., Heitzeg, M. M., & Nigg, J. T. (2011). Parsing the undercontrol-disinhibition pathway to substance use disorders: A multilevel developmental problem. Child Development Perspectives, 5(4), 248255. ScholarPubMed
Cited by