Hostname: page-component-cd4964975-96cn4 Total loading time: 0 Render date: 2023-03-29T01:42:08.752Z Has data issue: true Feature Flags: { "useRatesEcommerce": false } hasContentIssue true

Children's stress regulation mediates the association between prenatal maternal mood and child executive functions for boys, but not girls

Published online by Cambridge University Press:  02 August 2018

Regula Neuenschwander*
University of British Columbia, BC Children's Hospital Research Institute
Kaia Hookenson
University of British Columbia, BC Children's Hospital Research Institute
Ursula Brain
University of British Columbia, BC Children's Hospital Research Institute
Ruth E. Grunau
University of British Columbia, BC Children's Hospital Research Institute
Angela M. Devlin
University of British Columbia, BC Children's Hospital Research Institute
Joanne Weinberg
University of British Columbia, BC Children's Hospital Research Institute
Adele Diamond
University of British Columbia, BC Children's Hospital Research Institute
Tim F. Oberlander
University of British Columbia, BC Children's Hospital Research Institute
Address correspondence and reprint requests to: Regula Neuenschwander, Fabrikstrasse 8 (Büro A 349), CH-3012 Bern, Switzerland; E-mail:


Prenatal exposure to maternal mood disturbances shapes children's cognitive development reflected in the critical construct of executive functions (EFs). Little is known, however, about underlying mechanisms. By examining cortisol responses in both everyday and lab challenge settings, we tested whether the child/offspring hypothalamic–pituitary–adrenal axis mediates effects of prenatal maternal mood on child EFs at age 6. In 107 Canadian children born to women with a wide range of anxious and depressive symptoms during pregnancy, we found that in boys but not girls, depressed and/or anxious prenatal maternal mood is associated with heightened diurnal cortisol levels in everyday settings, as well as heightened cortisol reactivity to a lab challenge and that this heightened reactivity was associated with poorer EFs. Among boys we also observed that cortisol reactivity but not diurnal cortisol mediated the association between depressed and/or anxious prenatal maternal mood and EFs. Depressed and/or anxious prenatal maternal mood was related to child EFs for both girls and boys. To our knowledge, this is the first study to demonstrate a mediating role for child stress regulation in the association between prenatal maternal stress-related mood disturbances and child EFs, providing evidence of a mechanism contributing to fetal programming of cognition.

Special Issue 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.)


Support for this research was provided by a CIHR Grant MOP-89916 (to T.F.O.) and a postdoctoral fellowship from Brain Canada/NeuroDevNet (to R.N.). A. M. D. is supported by an Investigation Grant from BC Children's Hospital research Institute, University of British Columbia. We would like to thank our research assistants for data collection and all children and mothers for their participation.


Alexander, J. K., Hillier, A., Smith, R. M., Tivarus, M. E., & Beversdorf, D. Q. (2007). Beta-adrenergic modulation of cognitive flexibility during stress. Journal of Cognitive Neuroscience, 19, 468478. doi:10.1162/jocn.2007.19.3.468CrossRefGoogle ScholarPubMed
Alexander, N., Rosenlocher, F., Stalder, T., Linke, J., Distler, W., Morgner, J., & Kirschbaum, C. (2012). Impact of antenatal synthetic glucocorticoid exposure on endocrine stress reactivity in term-born children. Journal of Clinical Endocrinology and Metabolism, 97, 35383544. doi:10.1210/jc.2012-1970CrossRefGoogle ScholarPubMed
Alkon, A., Goldstein, L. H., Smider, N., Essex, M. J., Kupfer, D. J., & Boyce, W. T. (2003). Developmental and contextual influences on autonomic reactivity in young children. Developmental Psychobiology, 42, 6478. doi:10.1002/dev.10082CrossRefGoogle ScholarPubMed
Arnsten, A. F. T. (2009). Stress signalling pathways that impair prefrontal cortex structure and function. Nature Review Neuroscience, 10, 410422. doi:10.1038/nrn2648CrossRefGoogle ScholarPubMed
Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2006). Gene-environment interaction of the dopamine D4 receptor (DRD4) and observed maternal insensitivity predicting externalizing behavior in preschoolers. Developmental Psychobiology, 48, 406409. doi:10.1002/dev.20152CrossRefGoogle ScholarPubMed
Barker, D. J. (2003). The developmental origins of adult disease. European Journal of Epidemiology, 18, 733736. doi:10.1023/A:1025388901248CrossRefGoogle ScholarPubMed
Baron, R. M., & Kenny, D. A. (1986). The moderator–mediator variable distinction in social psychological research: Conceptual, strategic, and statistical considerations. Journal of Personality and Social Psychology, 51, 11731182. doi:10.1037/0022-3514.51.6.1173CrossRefGoogle ScholarPubMed
Beijers, R., Buitelaar, J. K., & de Weerth, C. (2014). Mechanisms underlying the effects of prenatal psychosocial stress on child outcomes: Beyond the HPA axis. European Child and Adolescent Psychiatry, 23, 943956. doi:10.1007/s00787-014-0566-3CrossRefGoogle ScholarPubMed
Bennett, H. A., Einarson, A., Taddio, A., Koren, G., & Einarson, T. R. (2004). Prevalence of depression during pregnancy: Systematic review. Obstetrics and Gynecology, 103, 698709. doi:10.1097/01.AOG.0000116689.75396.5fCrossRefGoogle ScholarPubMed
Blair, C., & Berry, D. J. (2017). Moderate within-person variability in cortisol is related to executive function in early childhood. Psychoneuroendocrinology, 81, 8895. doi:10.1016/j.psyneuen.2017.03.026CrossRefGoogle ScholarPubMed
Blair, C., & Diamond, A. (2008). Biological processes in prevention and intervention: The promotion of self-regulation as a means of preventing school failure. Development and Psychopathology, 20, 899911. doi:10.1017/S0954579408000436CrossRefGoogle ScholarPubMed
Blair, C., Granger, D., & Peters Razza, R. (2005). Cortisol reactivity is positively related to executive function in preschool children attending Head Start. Child Development, 76, 554567. doi:10.1111/j.1467-8624.2005.00863.xCrossRefGoogle ScholarPubMed
Blair, C., Granger, D. A., Willoughby, M., Mills-Koonce, R., Cox, M., Greenberg, M. T., … Family Life Project Investigators. (2011). Salivary cortisol mediates effects of poverty and parenting on executive functions in early childhood. Child Development, 82, 19701984. doi:10.1111/j.1467-8624.2011.01643.xCrossRefGoogle ScholarPubMed
Blair, C., & Ursache, A. (2011). A bidirectional model of executive functions and self-regulation. In Vohs, K. D. & Baumeister, R. F. (Eds.), Handbook of self-regulation: Research, theory, and applications (2nd ed., pp. 300320). New York: Guilford Press.Google Scholar
Booth, A., Granger, D. A., & Shirtcliff, E. A. (2008). Gender- and age-related differences in the association between social relationship quality and trait levels of salivary cortisol. Journal of Research on Adolescence, 18, 239260. doi:10.1111/j.1532-7795.2008.00559.xCrossRefGoogle Scholar
Brennan, P. A., Pargas, R., Walker, E. F., Green, P., Newport, D. J., & Stowe, Z. (2008). Maternal depression and infant cortisol: Influences of timing, comorbidity and treatment. Journal of Child Psychology and Psychiatry, 49, 10991107. doi:10.1111/j.1469-7610.2008.01914.xCrossRefGoogle ScholarPubMed
Buchmann, A. F., Zohsel, K., Blomeyer, D., Hohm, E., Hohmann, S., Jennen-Steinmetz, C., … Laucht, M. (2014). Interaction between prenatal stress and dopamine D4 receptor genotype in predicting aggression and cortisol levels in young adults. Psychopharmacology, 231, 30893097. doi:10.1007/s00213-014-3484-7CrossRefGoogle ScholarPubMed
Buss, C., Davis, E. P., Hobel, C. J., & Sandman, C. A. (2011). Maternal pregnancy-specific anxiety is associated with child executive function at 6-9 years age. Stress, 14, 665676. doi:10.3109/10253890.2011.623250CrossRefGoogle ScholarPubMed
Buss, C., Davis, E. P., Muftuler, L. T., Head, K., & Sandman, C. A. (2010). High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6-9-year-old children. Psychoneuroendocrinology, 35, 141153. doi:10.1016/j.psyneuen.2009.07.010CrossRefGoogle ScholarPubMed
Butts, K. A., Weinberg, J., Young, A. H., & Phillips, A. G. (2011). Glucocorticoid receptors in the prefrontal cortex regulate stress-evoked dopamine efflux and aspects of executive function. Proceedings of the National Academy of Sciences of the United States of America, 108, 1845918464. doi:10.1073/pnas.1111746108CrossRefGoogle ScholarPubMed
Capuron, L., & Miller, A. H. (2011). Immune system to brain signaling: Neuropsychopharmacological implications. Pharmacology and Therapeutics, 130, 226238. doi:10.1016/j.pharmthera.2011.01.014CrossRefGoogle ScholarPubMed
Charney, D. S., & Manji, H. K. (2004). Life stress, genes, and depression: Multiple pathways lead to increased risk and new opportunities for intervention. Science Signaling, 2004, re5. doi:10.1126/stke.2252004re5CrossRefGoogle ScholarPubMed
Chau, C. M. Y., Ranger, M., Sulistyoningrum, D., Devlin, A. M., Oberlander, T. F., & Grunau, R. E. (2014). Neonatal pain and COMTVal158Met genotype in relation to serotonin transporter (SLC6A4) promoter methylation in very preterm children at school age. Frontiers in Behavioral Neuroscience, 8, 409. doi:10.3389/fnbeh.2014.00409CrossRefGoogle Scholar
Chrousos, G. P. (2009). Stress and disorders of the stress system. Nature Reviews Endocrinology, 5, 374381. doi:10.1038/nrendo.2009.106CrossRefGoogle ScholarPubMed
Cicchetti, D., & Rogosch, F. A. (1996). Equifinality and multifinality in developmental psychopathology. Development and Psychopathology, 8, 597600. doi:10.1017/S0954579400007318CrossRefGoogle Scholar
Cole, D. A., & Maxwell, S. E. (2003). Testing mediational models with longitudinal data: Questions and tips in the use of structural equation modeling. Journal of Abnormal Psychology, 112, 558577. doi:10.1037/0021-843X.112.4.558CrossRefGoogle ScholarPubMed
Cools, R., & D'Esposito, M. (2011). Inverted-U shaped dopamine actions on human working memory and cognitive control. Biological Psychiatry, 69, e113e125. doi:10.1016/j.biopsych.2011.03.028CrossRefGoogle ScholarPubMed
Coussons-Read, M. E., Okun, M. L., & Nettles, C. D. (2007). Psychosocial stress increases inflammatory markers and alters cytokine production across pregnancy. Brain, Behavior, and Immunity, 21, 343350. doi:10.1016/j.bbi.2006.08.006CrossRefGoogle ScholarPubMed
Davidson, M. C., Amso, D., Anderson, L. C., & Diamond, A. (2006). Development of cognitive control and executive functions from 4 to 13 years: Evidence from manipulations of memory, inhibition, and task switching. Neuropsychologia, 44, 20372078. doi:10.1016/j.neuropsychologia.2006.02.006CrossRefGoogle ScholarPubMed
Davis, E. P., Glynn, L. M., Waffarn, F., & Sandman, C. A. (2011). Prenatal maternal stress programs infant stress regulation. Journal of Child Psychology and Psychiatry, 52, 119129. doi:10.1111/j.1469-7610.2010.02314.xCrossRefGoogle ScholarPubMed
de Bruijn, A. T., van Bakel, H. J., & van Baar, A. L. (2009). Sex differences in the relation between prenatal maternal emotional complaints and child outcome. Early Human Development, 85, 319324. doi:10.1016/j.earlhumdev.2008.12.009CrossRefGoogle ScholarPubMed
de Kloet, E. R., Oitzl, M. S., & Joëls, M. (1999). Stress and cognition: Are corticosteroids good or bad guys? Trends in Neurosciences, 22, 422426.CrossRefGoogle ScholarPubMed
Demir-Lira, Ö. E., Prado, J., & Booth, J. R. (2016). Neural correlates of math gains vary depending on parental socioeconomic status (SES). Frontiers in Psychology, 7, 112. doi:10.3389/fpsyg.2016.00892CrossRefGoogle Scholar
Dennis, C.-L., Falah-Hassani, K., & Shiri, R. (2017). Prevalence of antenatal and postnatal anxiety: Systematic review and meta-analysis. British Journal of Psychiatry, 210, 315323. doi:10.1192/bjp.bp.116.187179CrossRefGoogle ScholarPubMed
Diamond, A. (2011). Biological and social influences on cognitive control processes dependent on prefrontal cortex. Progress in Brain Research, 189, 319339. doi:10.1016/B978-0-444-53884-0.00032-4CrossRefGoogle ScholarPubMed
Diamond, A. (2013). Executive functions. Annual Review of Psychology, 64, 135168. doi:10.1146/annurev-psych-113011-143750CrossRefGoogle ScholarPubMed
Diamond, A., Barnett, W. S., Thomas, J., & Munro, S. (2007). Preschool program improves cognitive control. Science, 318, 13871388. doi:10.1126/science.1151148CrossRefGoogle ScholarPubMed
Diamond, A., & Lee, K. (2011). Interventions shown to aid executive function development in children 4 to 12 years old. Science, 333, 959964. doi:10.1126/science.1204529CrossRefGoogle ScholarPubMed
Diamond, A., & Ling, D. S. (2016). Conclusions about interventions, programs, and approaches for improving executive functions that appear justified and those that, despite much hype, do not. Developmental Cognitive Neuroscience, 18, 3448. doi:10.1016/j.dcn.2015.11.005CrossRefGoogle ScholarPubMed
Diego, M. A., Field, T., Hernandez-Reif, M., Cullen, C., Schanberg, S., & Kuhn, C. (2004). Prepartum, postpartum, and chronic depression effects on newborns. Psychiatry, 67, 6380. doi:10.1521/psyc. ScholarPubMed
DiPietro, J. A., Novak, M. F., Costigan, K. A., Atella, L. D., & Reusing, S. P. (2006). Maternal psychological distress during pregnancy in relation to child development at age two. Child Development, 77, 573587. doi:10.1111/j.1467-8624.2006.00891.xCrossRefGoogle ScholarPubMed
Donzella, B., Gunnar, M. R., Krueger, W. K., & Alwin, J. (2000). Cortisol and vagal tone responses to competitive challenge in preschoolers: Associations with temperament. Developmental Psychobiology, 37, 209220. doi:10.1002/1098-2302(2000)37:4<209::AID-DEV1>3.0.CO;2-S3.0.CO;2-S>CrossRefGoogle ScholarPubMed
Doom, J. R., Cicchetti, D., & Rogosch, F. A. (2014). Longitudinal patterns of cortisol regulation differ in maltreated and nonmaltreated children. Journal of the American Academy of Child & Adolescent Psychiatry, 53, 12061215. doi:10.1016/j.jaac.2014.08.006CrossRefGoogle ScholarPubMed
Dunkel Schetter, C. (2011). Psychological science on pregnancy: Stress processes, biopsychosocial models, and emerging research issues. Annual Review of Psychology, 62, 531558. doi:10.1146/annurev.psych.031809.130727CrossRefGoogle ScholarPubMed
Dunkel Schetter, C., & Tanner, L. (2012). Anxiety, depression and stress in pregnancy: Implications for mothers, children, research, and practice. Current Opinion in Psychiatry, 25, 141148. doi:10.1097/YCO.0b013e3283503680CrossRefGoogle Scholar
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. doi:10.1017/S0954579410000611CrossRefGoogle Scholar
Entringer, S., Buss, C., Kumsta, R., Hellhammer, D. H., Wadhwa, P. D., & Wuest, S. (2009). Prenatal psychosocial stress exposure is associated with subsequent working memory performance in young women. Behavioral Neuroscience, 123, 886893. doi:10.1037/a0016265CrossRefGoogle ScholarPubMed
Entringer, S., Kumsta, R., Hellhammer, D. H., Wadhwa, P. D., & Wust, S. (2009). Prenatal exposure to maternal psychosocial stress and HPA axis regulation in young adults. Hormones and Behavior, 55, 292298. doi:10.1016/j.yhbeh.2008.11.006CrossRefGoogle ScholarPubMed
Felitti, V. J., & Anda, R. F. (2010). The relationship of adverse childhood experiences to adult medical disease, psychiatric disorders and sexual behavior: Implications for healthcare. In Lanius, R. A., Vermetten, E., & Pain, C. (Eds.), The impact of early life trauma on health and disease (pp. 7787). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Felitti, V. J., Anda, R. F., Nordenberg, D., Williamson, D. F., Spitz, A. M., Edwards, V., … Marks, J. S. (1998). Relationship of childhood abuse and household dysfunction to many of the leading causes of death in adults: The adverse childhood experiences (ACE) study. American Journal of Preventive Medicine, 14, 245258. doi:10.1016/S0749-3797(98)00017-8CrossRefGoogle ScholarPubMed
Frodl, T., & O'Keane, V. (2013). How does the brain deal with cumulative stress? A review with focus on developmental stress, HPA axis function and hippocampal structure in humans. Neurobiology of Disease, 52, 2437. doi:10.1016/j.nbd.2012.03.012CrossRefGoogle ScholarPubMed
Fuster, J. M. (2008). The prefrontal cortex (4th ed.). London: Academic Press.CrossRefGoogle Scholar
Glover, V. (2011). Annual Research Review: Prenatal stress and the origins of psychopathology: An evolutionary perspective. Journal of Child Psychology and Psychiatry, 52, 356367. doi:10.1111/j.1469-7610.2011.02371.xCrossRefGoogle Scholar
Glover, V. (2015). Prenatal stress and its effects on the fetus and the child: Possible underlying biological mechanisms. In Antonelli, M. C. (Ed.), Perinatal programming of neurodevelopment (pp. 269283). New York: Springer.CrossRefGoogle Scholar
Glover, V., & Hill, J. (2012). Sex differences in the programming effects of prenatal stress on psychopathology and stress responses: An evolutionary perspective. Physiology and Behavior, 106, 736740. doi:10.1016/j.physbeh.2012.02.011CrossRefGoogle Scholar
Glover, V., O'Connor, T. G., & O'Donnell, K. (2010). Prenatal stress and the programming of the HPA axis. Neuroscience and Biobehavioral Reviews, 35, 1722. doi:10.1016/j.neubiorev.2009.11.008CrossRefGoogle ScholarPubMed
Gluckman, P., & Hanson, M. (2005). The fetal matrix: Evolution, development and disease. New York: Cambridge University Press.Google Scholar
Grant, K. A., McMahon, C., Austin, M. P., Reilly, N., Leader, L., & Ali, S. (2009). Maternal prenatal anxiety, postnatal caregiving and infants' cortisol responses to the still-face procedure. Developmental Psychobiology, 51, 625637. doi:10.1002/dev.20397CrossRefGoogle ScholarPubMed
Grunau, R. E., Cepeda, I. L., Chau, C. M. Y., Brummelte, S., Weinberg, J., Lavoie, P., … Turvey, S. E. (2013). Neonatal pain-related stress and NFKBIA genotype are associated with altered cortisol levels in preterm boys at school age. PLOS ONE, 8, e73926. doi:10.1371/journal.pone.0073926CrossRefGoogle ScholarPubMed
Grunau, R. E., Haley, D. W., Whitfield, M. F., Weinberg, J., Yu, W., & Thiessen, P. (2007). Altered basal cortisol levels at 3, 6, 8 and 18 months in infants born extremely low gestational age. Journal of Pediatrics, 150, 151156. doi:10.1016/j.jpeds.2006.10.053CrossRefGoogle ScholarPubMed
Gunnar, M. R., & Quevedo, L. (2007). The neurobiology of stress and development. Annual Review of Psychology, 58, 145173. doi:10.1146/annurev.psych.58.110405.085605CrossRefGoogle Scholar
Gutteling, B. M., de Weerth, C., & Buitelaar, J. K. (2004). Maternal prenatal stress and 4–6 year old children's salivary cortisol concentrations pre- and post-vaccination. Stress, 7, 257260. doi:10.1080/10253890500044521CrossRefGoogle ScholarPubMed
Gutteling, B. M., de Weerth, C., & Buitelaar, J. K. (2005). Prenatal stress and children's cortisol reaction to the first day of school. Psychoneuroendocrinology, 30, 541549. doi:10.1016/j.psyneuen.2005.01.002CrossRefGoogle Scholar
Hamilton, M. (1960). A rating scale for depression. Journal of Neurology, Neurosurgery & Psychiatry, 23, 5662. doi:10.1136/jnnp.23.1.56CrossRefGoogle Scholar
Hayes, A. F. (2013). Introduction to mediation, moderation, and conditional process analysis: A regression-based approach. New York: Guilford Press.Google Scholar
Hayes, A. F., & Rockwood, N. J. (in press). Regression-based statistical mediation and moderation analysis in clinical research: Observations, recommendations, and implementation. Behaviour Research and Therapy. doi:10.1016/j.brat.2016.11.00CrossRefGoogle Scholar
Hostinar, C. E., & Gunnar, M. (2013). The developmental effects of early life stress: An overview of current theoretical frameworks. Current Directions in Psychological Science, 22, 400406. doi:10.1177/0963721413488889CrossRefGoogle ScholarPubMed
Hughes, C. (2011). Changes and challenges in 20 years of research into the development of executive functions. Infant and Child Development, 20, 251271. doi:10.1002/icd.736CrossRefGoogle Scholar
Johnson, A. C. (2015). Developmental pathways to attention-deficit/hyperactivity disorder and disruptive behavior disorders: Investigating the impact of the stress response on executive functioning. Clinical Psychology Review, 36, 112. doi:10.1016/j.cpr.2014.12.001CrossRefGoogle ScholarPubMed
Kudielka, B. M., & Kirschbaum, C. (2005). Sex differences in HPA axis responses to stress: A review. Biological Psychology, 69, 113132. doi:10.1016/j.biopsycho.2004.11.009CrossRefGoogle ScholarPubMed
Leight, K. L., Fitelson, E. M., Weston, C. A., & Wisner, K. L. (2010). Childbirth and mental disorders. International Review of Psychiatry, 22, 453471. doi:10.3109/09540261.2010.514600CrossRefGoogle ScholarPubMed
Ling, D. S., Kelly, M. K., & Diamond, A. (2016). Human-animal interaction and the development of cognitive control (executive functions). In Freund, L. S., McCune, S., Esposito, L., Gee, N. R., & McCardle, P. (Eds.), Social neuroscience of human-animal interaction. New York: American Psychological Association Press.Google Scholar
Lupien, S. J., Gillin, C. J., & Hauger, R. L. (1999). Working memory is more sensitive than declarative memory to the acute effects of corticosteroids: A dose-response study in humans. Behavioral Neuroscience, 113, 420430. doi:10.1037/0735-7044.113.3.420CrossRefGoogle ScholarPubMed
Lupien, S. J., Maheu, F., Tu, M., Fiocco, A., & Schramek, T. E. (2007). The effects of stress and stress hormones on human cognition: Implications for the field of brain and cognition. Brain and Cognition, 65, 209237. doi:10.1016/j.bandc.2007.02.007CrossRefGoogle ScholarPubMed
Marcus, S. M., Flynn, H. A., Blow, F. C., & Barry, K. L. (2003). Depressive symptoms among pregnant women screened in obstetrics settings. Journal of Women's Health, 12, 373380. doi:10.1089/154099903765448880CrossRefGoogle ScholarPubMed
Matthews, S. G., & Phillips, D. I. (2011). Minireview: Transgenerational inheritance of the stress response: A new frontier in stress research. Endocrinology, 151, 713. doi:10.1210/en.2009-0916CrossRefGoogle Scholar
McEwen, B. S. (2000). Allostasis and allostatic load: Implications for neuropsychopharmacology. Neuropsychopharmacology, 22, 108124. doi:10.1016/S0893-133X(99)00129-3CrossRefGoogle ScholarPubMed
McEwen, B. S., & Morrison, J. H. (2013). The brain on stress: Vulnerability and plasticity of the prefrontal cortex over the life course. Neuron, 79, 1629. doi:10.1016/j.neuron.2013.06.028CrossRefGoogle ScholarPubMed
McEwen, B. S., & Wingfield, J. C. (2003). The concept of allostasis in biology and biomedicine. Hormones & Behavior, 43, 216. doi:10.1016/S0018-506X(02)00024-7CrossRefGoogle ScholarPubMed
Mennes, M., Stiers, P., Lagae, L., & van den Bergh, B. R. H. (2006). Long-term cognitive sequelae of antenatal maternal anxiety: Involvement of the orbitofrontal cortex. Neuroscience and Biobehavioral Reviews, 30, 10781086. doi:10.1016/j.neubiorev.2006.04.003CrossRefGoogle ScholarPubMed
Miller, A. H., & Raison, C. L. (2016). The role of inflammation in depression: From evolutionary imperative to modern treatment target. Nature Reviews Immunology, 16, 2234. doi:10.1038/nri.2015.5CrossRefGoogle ScholarPubMed
Miller, G. E., Chen, E., & Zhou, E. S. (2007). If it goes up, must it come down? Chronic stress and the hypothalamic-pituitary-adrenocortical axis in humans. Psychological Bulletin, 133, 2545. doi:10.1037/0033-2909.133.1.25CrossRefGoogle ScholarPubMed
Moe, V., & Slining, K. (2001). Children prenatally exposed to substances: Gender-related differences in outcome from infancy to 3 years of age. Infant Mental Health Journal, 22, 334350. Scholar
Neuenschwander, R., & Oberlander, T. F. (2017). Developmental origins of self-regulation: Prenatal maternal stress and psychobiological development during childhood. In Deater-Deckard, K. & Panneton, R. K. (Eds.), Parental stress and early child development: Adaptive and maladaptive outcomes (pp. 127156). New York: Springer.CrossRefGoogle Scholar
Noble, K. G., McCandliss, B. D., & Farah, M. J. (2007). Socioeconomic gradients predict individual differences in neurocognitive abilities. Developmental Science, 10, 464480. doi:10.1111/j.1467-7687.2007.00600.xCrossRefGoogle ScholarPubMed
Oberlander, T. F., Warburton, W., Misri, S., Aghajanian, J., & Hertzman, C. (2006). Neonatal outcomes after prenatal exposure to selective serotonin reuptake inhibitor antidepressants and maternal depression using population-based linked health data. Archives of General Psychiatry, 63, 898906. doi:10.1001/archpsyc.63.8.898CrossRefGoogle ScholarPubMed
Oberlander, T. F., Weinberg, J., Papsdorf, M., Grunau, R., Misri, S., & Devlin, A. M. (2008). Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics, 3, 97106. doi:10.4161/epi.3.2.6034CrossRefGoogle ScholarPubMed
Obradović, J., Portilla, X. A., & Ballard, P. J. (2016). Biological sensitivity to family income: Differential effects on early executive functioning. Child Development, 87, 374384. doi:10.1111/cdev.12475CrossRefGoogle ScholarPubMed
O'Connor, T. G., Ben-Shlomo, Y., Heron, J., Golding, J., Adams, D., & Glover, V. (2005). Prenatal anxiety predicts individual differences in cortisol in pre- adolescent children. Biological Psychiatry, 58, 211217. doi:10.1016/j.biopsych.2005.03.032CrossRefGoogle ScholarPubMed
O'Donnell, K. J., Glover, V., Jenkins, J., Browne, D., Ben-Shlomo, Y., Golding, J., & O'Connor, T. G. (2013). Prenatal maternal mood is associated with altered diurnal cortisol in adolescence. Psychoneuroendocrinology, 38, 16301638. doi:10.1016/j.psyneuen.2013.01.008CrossRefGoogle ScholarPubMed
Pauli-Pott, U., & Becker, K. (2011). Neuropsychological basic deficits in preschoolers at risk for ADHD: A meta-analysis. Clinical Psychology Review, 31, 626637. doi:10.1016/j.cpr.2011.02.005CrossRefGoogle ScholarPubMed
Pearson, R. M., Bornstein, M. H., Cordero, M., Scerif, G., Mahedy, L., Evans, J., … Stein, A. (2016). Maternal perinatal mental health and offspring academic achievement at age 16: The mediating role of childhood executive function. Journal of Child Psychology and Psychiatry, 57, 491501. doi:10.1111/jcpp.12483CrossRefGoogle ScholarPubMed
Pluess, M., Velders, F. P., Belsky, J., van IJzendoorn, M. H., Bakermans-Kranenburg, M. J., Jaddoe, V. W. V., … Tiemeier, H. (2011). Serotonin transporter polymorphism moderates effects of prenatal maternal anxiety on infant negative emotionality. Biological Psychiatry, 69, 520525. doi:10.1016/j.biopsych.2010.10.006CrossRefGoogle ScholarPubMed
Pruessner, J. C., Kirschbaum, C., Meinlschmid, G., & Hellhammer, D. H. (2003). Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrinology, 28, 916931. doi:10.1016/S0306-4530(02)00108-7CrossRefGoogle ScholarPubMed
Ramos, B. P., & Arnsten, A. F. (2007). Adrenergic pharmacology and cognition: Focus on the prefrontal cortex. Pharmacology and Therapeutics, 113, 523536. doi:10.1016/j.pharmthera.2006.11.006CrossRefGoogle ScholarPubMed
Rice, F., Harold, G., Boivin, J., van den Bree, M., Hay, D. F., & Thapar, A. (2010). The links between prenatal stress and offspring development and psychopathology: Disentangling environmental and inherited influences. Psychological Medicine, 40, 335345. doi:10.1017/S0033291709005911CrossRefGoogle ScholarPubMed
Sanchez, M. M., Young, L. J., Plotsky, P. M., & Insel, T. R. (2000). Distribution of corticosteroid receptors in the rhesus brain. Journal of Neuroscience, 20, 46574658.CrossRefGoogle ScholarPubMed
Sandman, C. A., Buss, C., Head, K., & Davis, E. P. (2015). Fetal exposure to maternal depressive symptoms is associated with cortical thickness in late childhood. Biological Psychiatry, 77, 324334. doi:10.1016/j.biopsych.2014.06.025CrossRefGoogle ScholarPubMed
Sandman, C. A., Davis, E., & Glynn, L. (2012). Prescient human fetuses thrive. Psychological Science, 23, 93100. doi:10.1177/0956797611422073CrossRefGoogle ScholarPubMed
Seckl, J. R., & Meaney, M. J. (1993). Early life events and later development of ischaemic heart disease. Lancet, 342, 1236. doi:10.1016/0140-6736(93)92215-FCrossRefGoogle ScholarPubMed
Shacka, J. J., Fennell, O. B., & Robinson, S. E. (1997). Prenatal nicotine sex-dependently alters agonist-induced locomotion and stereotypy. Neurotoxicology and Teratology, 19, 467476. doi:10.1016/S0892-0362(97)00063-9CrossRefGoogle ScholarPubMed
Shirtcliff, E. A., Granger, D. A., Booth, A., & Johnson, D. (2005). Low salivary cortisol levels and externalizing behavior problems in youth. Development and Psychopathology, 17, 167184. doi:10.1017/S0954579405050091CrossRefGoogle ScholarPubMed
Simons, S. S. H., Beijers, R., Cillessen, A. H. N., & de Weerth, C. (2015). Development of the cortisol circadian rhythm in the light of stress early in life. Psychoneuroendocrinology, 62, 292300. doi:10.1016/j.psyneuen.2015.08.024CrossRefGoogle ScholarPubMed
Snyder, H. R. (2013). Major depressive disorder is associated with broad impairments on neuropsychological measures of executive function: A meta-analysis and review. Psychological Bulletin, 139, 81132. doi:10.1037/a0028727CrossRefGoogle ScholarPubMed
Spinrad, T. L., Eisenberg, N., Granger, D. A., Eggum, N. D., Sallquist, J., Haugen, R., … Hofer, C. (2009). Individual differences in preschoolers' salivary cortisol and alpha-amylase reactivity: Relations to temperament and maladjustment. Hormones and Behavior, 56, 133139. doi:10.1016/j.yhbeh.2009.03.020CrossRefGoogle ScholarPubMed
Stroud, L. R., Salovey, P., & Epel, E. S. (2002). Sex differences in stress responses: Social rejection versus achievement stress. Biological Psychiatry, 52, 318327. doi:10.1016/S0006-3223(02)01333-1CrossRefGoogle ScholarPubMed
Suurland, J., van der Heijden, K. B., Smaling, H. J. A., Huijbregts, S. C. J., van Goozen, S. H. M., & Swaab, H. (2017). Infant autonomic nervous system response and recovery: Associations with maternal risk status and infant emotion regulation. Development and Psychopathology, 29, 759773. doi:10.1017/S0954579416000456CrossRefGoogle ScholarPubMed
Talge, N. M., Neal, C., & Glover, V. (2007). Antenatal maternal stress and long-term effects on child neurodevelopment: How and why? Journal of Child Psychology and Psychiatry and Allied Disciplines, 48, 245261. doi:10.1111/j.1469-7610.2006.01714.xCrossRefGoogle ScholarPubMed
Tollenaar, M. S., Beijers, R., Jansen, J., Riksen-Walraven, J. M. A., & de Weerth, C. (2011). Maternal prenatal stress and cortisol reactivity to stressors in human infants. Stress, 14, 5365. doi:10.3109/10253890.2010.499485CrossRefGoogle ScholarPubMed
van den Bergh, B. R. H., Mennes, M., Oosterlaan, J., Stevens, V., Stiers, P., Marcoen, A., & Lagae, L. (2005). High antenatal maternal anxiety is related to impulsivity during performance on cognitive tasks in 14- and 15-year-olds. Neuroscience and Biobehavioral Reviews, 29, 259269. doi:10.1016/j.neubiorev.2004.10.010CrossRefGoogle ScholarPubMed
van den Bergh, B. R. H., Mennes, M., Stevens, V., van der Meere, J., Börger, N., Stiers, P., … Lagae, L. (2006). ADHD deficit as measured in adolescent boys with a continuous performance task is related to antenatal maternal anxiety. Pediatric Research, 59, 7882. doi:10.1203/01.pdr.0000191143.75673.52CrossRefGoogle ScholarPubMed
van den Bergh, B. R. H., Mulder, E. J., Mennes, M., & Glover, V. (2005). Antenatal maternal anxiety and stress and the neurobehavioural development of the fetus and child: Links and possible mechanisms: A review. Neuroscience and Biobehavioral Reviews, 29, 237258. doi:10.1016/j.neubiorev.2004.10.007CrossRefGoogle ScholarPubMed
van den Bergh, B. R. H., van Calster, B., Smits, T., van Huffel, S., & Lagae, L. (2008). Antenatal maternal anxiety is related to HPA-axis dysregulation and self-reported depressive symptoms in adolescence: A prospective study on the fetal origins of depressed mood. Neuropsychopharmacology, 33, 536545. doi:10.1038/sj.npp.1301450CrossRefGoogle ScholarPubMed
Vänskä, M., Punamäki, R.-L., Lindblom, J. K., Tolvanen, A., Flykt, M., Unkila-Kallio, L., … Tiitinen, A. (2015). Timing of early maternal mental health and child cortisol regulation. Infant and Child Development, 25, 461483. doi:10.1002/icd.1948CrossRefGoogle Scholar
Vijayraghavan, S., Wang, M., Birnbaum, S. G., Williams, G. V., & Arnsten, A. F. T. (2007). Inverted-U dopamine D1 receptor actions on prefrontal neurons engaged in working memory. Nature Neuroscience, 10, 376384. doi:10.1038/nn1846CrossRefGoogle ScholarPubMed
Wagner, S., Cepeda, I. L., Krieger, D., Maggi, S., D'Angiulli, A., Weinberg, J., & Grunau, R. E. (2015). Higher cortisol is associated with poorer executive functioning in preschool children: The role of parenting stress, parent coping and quality of daycare. Child Neuropsychology, 3, 117.Google Scholar
Weikum, W. M., Brain, U., Chau, C. M. Y., Grunau, R. E., Boyce, T., Diamond, A., & Oberlander, T. F. (2013). Prenatal serotonin reuptake inhibitor (SRI) antidepressant exposure and serotonin transporter promoter genotype (SLC6A4) influence executive functions at 6 years of age. Frontiers in Cellular Neuroscience, 7, 112. doi:10.3389/fncel.2013.00180CrossRefGoogle Scholar
Weinstock, M. (2008). The long-term behavioural consequences of prenatal stress. Neuroscience and Biobehavioral Reviews, 32, 10731086. doi:10.1016/j.neubiorev.2008.03.002CrossRefGoogle ScholarPubMed
Wright, A., & Diamond, A. (2014). An effect of inhibitory load in children while keeping working memory load constant. Frontiers in Psychology, 5, 213. doi:10.3389/fpsyg.2014.00213CrossRefGoogle ScholarPubMed
Zaitchik, D., Iqbal, Y., & Carey, S. (2014). The effect of executive function on biological reasoning in young children: An individual differences study. Child Development, 85, 160175. doi:10.1111/cdev.12145CrossRefGoogle ScholarPubMed
Zhang, T. Y., Chretien, P., Meaney, M. J., & Gratton, A. (2005). Influence of naturally occurring variations in maternal care on prepulse inhibition of acoustic startle and the medial prefrontal cortical dopamine response to stress in adult rats. Journal of Neuroscience, 25, 14931502. doi:10.1523/JNEUROSCI.3293-04.2005CrossRefGoogle ScholarPubMed
Zijlmans, M. A., Riksen-Walraven, J. M., & de Weerth, C. (2015). Associations between maternal prenatal cortisol concentrations and child outcomes: A systematic review. Neuroscience and Biobehavioral Reviews, 53, 124. doi:10.1016/j.neubiorev.2015.02.015CrossRefGoogle ScholarPubMed
Supplementary material: File

Neuenschwander et al. supplementary material

Table S1

Download Neuenschwander et al. supplementary material(File)
File 28 KB
Supplementary material: File

Neuenschwander et al. supplementary material

Table S2

Download Neuenschwander et al. supplementary material(File)
File 29 KB