Abstract
Two separate lines of inquiry indicate (a) that prenatal stress is associated with heightened behavioral and physiological reactivity, and (b) that these postnatal phenotypes are associated with increased susceptibility to both positive and negative developmental experiences and environmental exposures. This research considered together raises the intriguing hypothesis first advanced by Pluess and Belsky (Dev Psychopathol 23:29–38, 2011) that prenatal-stress fosters, promotes or “programs” postnatal developmental plasticity. In this paper, we review further evidence consistent with this proposition, including a novel animal study which experimentally manipulated both prenatal stress and postnatal rearing. Directions for future work focused on mechanisms mediating the plasticity-inducing effects of prenatal stress and the moderators of such effects are outlined.
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Anderson DK, Rhees RW, Fleming DE (1985) Effects of prenatal stress on differentiation of the sexually dimorphic nucleus of the preoptic area (SDN-POA) of the rat brain. Brain Res 332(1):113–118
Aye IL, Keelan JA (2013) Placental ABC transporters, cellular toxicity and stress in pregnancy. Chem Biol Interact 203(2):456–466. https://doi.org/10.1016/j.cbi.2013.03.007
Babineau V, Green CG, Jolicoeur-Martineau A, Bouvette-Turcot AA, Minde K, Sassi R, St-André M, Carrey N, Atkinson L, Kennedy JL, Lydon J (2015) Prenatal depression and 5-HTTLPR interact to predict dysregulation from 3 to 36 months–A differential susceptibility model. J Child Psychol Psychiatry 56(1):21–29
Baibazarova E, van de Beek C, Cohen-Kettenis PT, Buitelaar J, Shelton KH, van Goozen SH (2013) Influence of prenatal maternal stress, maternal plasma cortisol and cortisol in the amniotic fluid on birth outcomes and child temperament at 3 months. Psychoneuroendocrinology 38:907–915. https://doi.org/10.1016/j.psyneuen.2012.09.015
Bakermans-Kranenburg MJ, van IJzendoorn MH (2015) The hidden efficacy of interventions: gene × environment experiments from a differential susceptibility perspective. Annu Rev Psychol 66:381–409
Bateson P, Barker D, Clutton-Brock T, Deb D, D’udine B, Foley RA et al (2004) Developmental plasticity and human health. Nature 430(6998):419–421. https://doi.org/10.1038/nature02725
Beijers R, Buitelaar JK, de Weerth C (2014) Mechanisms underlying the effects of prenatal psychosocial stress on child outcomes: beyond the HPA axis. Eur Child Adolesc Psychiatry 23(10):943–956
Belsky J (1997) Variation in susceptibility to rearing influences: an evolutionary argument. Psychol Inq 8:182–186. https://doi.org/10.1207/s15327965pli0803_3
Belsky J (2000) Conditional and alternative reproductive strategies: individual differences in susceptibility to rearing experiences. In: Genetic influences on human fertility and sexuality. Springer, Boston, MA, pp 127–146
Belsky J (2005) Differential susceptibility to rearing influences: an evolutionary hypothesis and some evidence. In: Ellis B, Bjorklund D (eds) Origins of the social mind: evolutionary psychology and child development. Guildford, New York, pp 139–163
Belsky J, Pluess M (2009) Beyond diathesis stress: differential susceptibility to environmental influences. Psychol Bull 135:885. https://doi.org/10.1037/a0017376
Belsky J, Pluess M (2013) Beyond risk, resilience, and dysregulation: phenotypic plasticity and human development. Dev Psychopathol 25:1243. https://doi.org/10.1017/s095457941300059x
Belsky J, Bakermans-Kranenburg MJ, Van Ijzendoorn MH (2007) For better and for worse differential susceptibility to environmental influences. Curr Dir Psychol Sci 16:300–304. https://doi.org/10.1111/j.1467-8721.2007.00525.x
Blackford JU, Avery SN, Shelton RC, Zald DH (2009) Amygdala temporal dynamics: temperamental differences in the timing of amygdala response to familiar and novel faces. BMC Neurosci 10(1):145
Blakeley PM, Capron LE, Jensen AB, O’Donnell KJ, Glover V (2013) Maternal prenatal symptoms of depression and down regulation of placental monoamine oxidase A expression. J Psychosom Res 75:341–345. https://doi.org/10.1016/j.jpsychores.2013.07.002
Bloch B, Guitteny AF, Chouham S, Mougin C, Roget A, Teoule R (1990) Topography and ontogeny of the neurons expressing vasopressin, oxytocin, and somatostatin genes in the rat brain: an analysis using radioactive and biotinylated oligonucleotides. Cell Mol Neurobiol 10:99–112. https://doi.org/10.1007/BF00733638
Bogdan R, Agrawal A, Gaffrey MS, Tillman R, Luby JL (2014) Serotonin transporter-linked polymorphic region (5-HTTLPR) genotype and stressful life events interact to predict preschool-onset depression: a replication and developmental extension. J Child Psychol Psychiatry 55:448–457. https://doi.org/10.1111/jcpp.12142
Börzsönyi B, Demendi C, Pajor A, Rigó J, Marosi K, Ágota A et al (2012) Gene expression patterns of the 11β-hydroxysteroid dehydrogenase 2 enzyme in human placenta from intrauterine growth restriction: the role of impaired feto-maternal glucocorticoid metabolism. Eur J Obstet Gynecol Reproductive Biol 161:12–17. https://doi.org/10.1016/j.ejogrb.2011.12.013
Boyce WT, Ellis BJ (2005) Biological sensitivity to context: I. An evolutionary–developmental theory of the origins and functions of stress reactivity. Dev Psychopathol 17(2):271–301
Boyce WT, Adams S, Tschann JM, Cohen F, Wara D, Gunnar MR (1995) Adrenocortical and behavioral predictors of immune responses to starting school. Pediatr Res 38:1009–1017. https://doi.org/10.1203/00006450-199512000-00030
Brody GH, Miller GE, Yu T, Beach SR, Chen E (2016) Supportive family environments ameliorate the link between racial discrimination and epigenetic aging: a replication across two longitudinal cohorts. Psychol Sci 27:530–541. https://doi.org/10.1177/0956797615626703
Brunton PJ, Russell JA (2010) Prenatal social stress in the rat programmes neuroendocrine and behavioural responses to stress in the adult offspring: Sex-specific effects. J Neuroendocrinol 22:258–271. https://doi.org/10.1111/j.1365-2826.2010.01969.x
Bush NR, Allison AL, Miller AL, Deardorff J, Adler NE, Boyce WT (2017) Socioeconomic disparities in childhood obesity risk: association with an oxytocin receptor polymorphism. JAMA Pediatr 171(1):61–67
Canli T, Lesch KP (2007) Long story short: the serotonin transporter in emotion regulation and social cognition. Nat Neurosci 10:1103–1109. https://doi.org/10.1038/nn1964
Carter CS (2014) Oxytocin pathways and the evolution of human behavior. Annu Rev Psychol 65:17–39. https://doi.org/10.1146/annurev-psych-010213-115110
Carter CS, Grippo AJ, Pournajafi-Nazarloo H, Ruscio MG, Porges SW (2008) Oxytocin, vasopressin and sociality. Prog Brain Res 170:331–336. https://doi.org/10.1016/s0079-6123(08)00427-5
Champoux M, Bennett A, Shannon C, Higley JD, Lesch KP, Suomi SJ (2002) Serotonin transporter gene polymorphism, differential early rearing, and behavior in rhesus monkey neonates. Mol Psychiatry 7(10):1058. https://doi.org/10.1038/sj.mp.4001157
Charil A, Laplante DP, Vaillancourt C, King S (2010) Prenatal stress and brain development. Brain Res Rev 65(1):56–79
Chen FR, Raine A, Rudo-Hutt AS, Glenn AL, Soyfer L, Granger DA (2015) Harsh discipline and behavior problems: the moderating effects of cortisol and alpha-amylase. Biol Psychol 104:19–27. https://doi.org/10.1016/j.biopsycho.2014.11.005
Cicchetti D, Rogosch FA, Thibodeau EL (2012) The effects of child maltreatment on early signs of antisocial behavior: genetic moderation by tryptophan hydroxylase, serotonin transporter, and monoamine oxidase A genes. Dev Psychopathol 24:907–928. https://doi.org/10.1017/S0954579612000442
Conradt E, Measelle J, Ablow JC (2013a) Poverty, problem behavior, and promise: differential susceptibility among infants reared in poverty. Psychol Sci 24:235–242. https://doi.org/10.1177/0956797612457381
Conradt E, Lester BM, Appleton AA, Armstrong DA, Marsit CJ (2013b) The roles of DNA methylation of NR3C1 and 11β-HSD2 and exposure to maternal mood disorder in utero on newborn neurobehavior. Epigenetics 8(12):1321–1329. https://doi.org/10.4161/epi.26634
Conway A, Stifter CA (2012) Longitudinal antecedents of executive function in preschoolers. Child Dev 83:1022–1036. https://doi.org/10.1111/j.1467-8624.2012.01756.x
Coussons-Read ME, Okun ML, Nettles CD (2007) Psychosocial stress increases inflammatory markers and alters cytokine production across pregnancy. Brain Behav Immun 21:343–350. https://doi.org/10.1016/j.bbi.2006.08.006
Cruceanu C, Matosin N, Binder EB (2017) Interactions of early-life stress with the genome and epigenome: from prenatal stress to psychiatric disorders. Curr Opin Behav Sci 14:167–171. https://doi.org/10.1016/j.cobeha.2017.04.001
Das P, Kemp AH, Liddell BJ, Brown KJ, Olivieri G, Peduto A, Gordon E, Williams LM (2005) Pathways for fear perception: modulation of amygdala activity by thalamo-cortical systems. Neuroimage 26(1):141–148
Davis M, Whalen PJ (2001) The amygdala: vigilance and emotion. Mol Psychiatry 6(1):13
Davies PT, Sturge-Apple ML, Cicchetti D (2011) Interparental aggression and children’s adrenocortical reactivity: testing an evolutionary model of allostatic load. Dev Psychopathol 23:801–814. https://doi.org/10.1017/S0954579411000319
Davis EP, Sandman CA (2010) The timing of prenatal exposure to maternal cortisol and psychosocial stress is associated with human infant cognitive development. Child Dev 81:131–148. https://doi.org/10.1111/j.1467-8624.2009.01385.x
Davis EP, Snidman N, Wadhwa PD, Glynn LM, Schetter CD, Sandman CA (2004) Prenatal maternal anxiety and depression predict negative behavioral reactivity in infancy. Infancy 6:319–331. https://doi.org/10.1207/s15327078in0603_1
Davis EP, Glynn LM, Dunkel-Schetter C, Hobel C, Chicz-Demet A, Sandman CA (2005) Corticotropin-releasing hormone during pregnancy is associated with infant temperament. Dev Neurosci 27:299–305
Davis EP, Glynn LM, Schetter CD, Hobel C, Chicz-Demet A, Sandman CA (2007) Prenatal exposure to maternal depression and cortisol influences infant temperament. J Am Acad Child Adolesc Psychiatry 46:737–746. https://doi.org/10.1097/chi.0b013e318047b775
Davis EP, Glynn LM, Waffarn F, Sandman CA (2011) Prenatal maternal stress programs infant stress regulation. J Child Psychol Psychiatry 52:119–129. https://doi.org/10.1111/j.1469-7610.2010.02314.x
de Weerth C, van Hees Y, Buitelaar JK (2003) Prenatal maternal cortisol levels and infant behavior during the first 5 months. Early Human Dev 74:139–151. https://doi.org/10.1016/s0378-3782(03)00088-4
Del Giudice M (2012) Fetal programming by maternal stress: insights from a conflict perspective. Psychoneuroendocrinology 37(10):1614–1629
Del Giudice M, Barrett ES, Belsky J, Hartman S, Martel MM, Sangenstedt S, Kuzawa CW (2018) Individual differences in developmental plasticity: a role for early androgens? Psychoneuroendocrinology 90:165–173
Demendi C, Börzsönyi B, Pajor A, Rigó J, Nagy ZB, Szentpéteri I, Joó JG (2012) Abnormal fetomaternal glucocorticoid metabolism in the background of premature delivery: placental expression patterns of the 11β-hydroxysteroid dehydrogenase 2 gene. Eur J Obstet Gynecol Reprod Biol 165:210–214. https://doi.org/10.1016/j.ejogrb.2012.08.009
Devlin AM, Brain U, Austin J, Oberlander TF (2010) Prenatal exposure to maternal depressed mood and the MTHFR C677T variant affect SLC6A4 methylation in infants at birth. PloS One 5(8):e12201. https://doi.org/10.1371/journal.pone.0012201
Devries GJ, Buijs RM, Van Leeuwen FW, Caffe AR, Swaab DF (1985) The vasopressinergic innervation of the brain in normal and castrated rats. J Comp Neurol 233:236–254. https://doi.org/10.1002/cne.902330206
Dich N, Doan SN, Evans GW (2015) Children’s emotionality moderates the association between maternal responsiveness and allostatic load: investigation into differential susceptibility. Child Dev 86:936–944. https://doi.org/10.1111/cdev.12346
DiPietro JA, Novak MF, Costigan KA, Atella LD, Reusing SP (2006) Maternal psychological distress during pregnancy in relation to child development at age two. Child Dev 77(3):573–587. https://doi.org/10.1111/j.1467-8624.2006.00891.x
Dix T, Yan N (2014) Mothers' depressive symptoms and infant negative emotionality in the prediction of child adjustment at age 3: testing the maternal reactivity and child vulnerability hypotheses. Dev Psychopathol 26(1):111–124
Ellis BJ, Boyce WT, Belsky J, Bakermans-Kranenburg MJ, Van IJzendoorn MH (2011a) Differential susceptibility to the environment: an evolutionary–neurodevelopmental theory. Dev Psychopathol 23:7–28. https://doi.org/10.1017/S0954579410000611
Ellis BJ, Shirtcliff EA, Boyce WT, Deardorff J, Essex MJ (2011b) Quality of early family relationships and the timing and tempo of puberty: effects depend on biological sensitivity to context. Dev Psychopathol 23:85–99. https://doi.org/10.1017/S0954579410000660
Entringer S, Buss C, Wadhwa PD (2015) Prenatal stress, development, health and disease risk: a psychobiological perspective—2015 Curt Richter Award Paper. Psychoneuroendocrinology 62:366–375. doi.:https://doi.org/10.1016/j.psyneuen.2015.08.019
Essex MJ, Armstrong JM, Burk LR, Goldsmith HH, Boyce WT (2011) Biological sensitivity to context moderates the effects of the early teacher–child relationship on the development of mental health by adolescence. Dev Psychopathol 23:149–161. https://doi.org/10.1017/s0954579410000702
Field T, Diego M, Dieter J, Hernandez-Reif M, Schanberg S, Kuhn C et al (2004) Prenatal depression effects on the fetus and the newborn. Infant Behav Dev 27:216–229. https://doi.org/10.1016/s0163-6383(04)00012-8
Gangestad SW, Caldwell Hooper AE, Eaton MA (2012) On the function of placental corticotropin-releasing hormone: a role in maternal-fetal conflicts over blood glucose concentrations. Biol Rev 87(4):856–873
Gaspar P, Cases O, Maroteaux L (2003) The developmental role of serotonin: news from mouse molecular genetics. Nat Rev Neurosci 4(12):1002–1012. https://doi.org/10.1038/nrn1256
Gitau R, Fisk NM, Glover V (2004) Human fetal and maternal corticotrophin releasing hormone responses to acute stress. Arch Dis Child Fetal Neonatal Ed 89(1):F29–F32
Gitau R, Adams D, Fisk NM, Glover V (2005) Fetal plasma testosterone correlates positively with cortisol. Arch Dis Child Fetal Neonatal Ed 90(2):F166–F169
Glover V (2011) Annual research review: prenatal stress and the origins of psychopathology: an evolutionary perspective. J Child Psychol Psychiatry 52:356–367. https://doi.org/10.1111/j.1469-7610.2011.02371.x
Glover V (2014) Maternal depression, anxiety and stress during pregnancy and child outcome; what needs to be done. Best Pract Res Clin Obstet Gynaecol 28(1):25–35. https://doi.org/10.1016/j.bpobgyn.2013.08.017
Green BB, Armstrong DA, Lesseur C, Paquette AG, Guerin DJ, Kwan LE, Marsit CJ (2015) The role of placental 11-beta hydroxysteroid dehydrogenase type 1 and type 2 methylation on gene expression and infant birth weight. Biol Reprod 92(6):149–151
Green CG, Babineau V, Jolicoeur-Martineau A, Bouvette-Turcot AA, Minde K, Sassi R et al (2017) Prenatal maternal depression and child serotonin transporter linked polymorphic region (5-HTTLPR) and dopamine receptor D4 (DRD4) genotype predict negative emotionality from 3 to 36 months. Dev Psychopathol 29:901–917. https://doi.org/10.1017/S0954579416000560
Grossman AW, Churchill JD, McKinney BC, Kodish IM, Otte SL, Greenough WT (2003) Experience effects on brain development: Possible contributions to psychopathology. J Child Psychol Psychiatry 44(1):33–63. https://doi.org/10.1111/1469-7610.t01-1-00102
Grundwald NJ, Benítez DP, Brunton PJ (2016) Sex-dependent effects of prenatal stress on social memory in rats: a role for differential expression of central vasopressin-1a receptors. J Neuroendocrinol. https://doi.org/10.1111/jne.12343
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 Dev 86(4):1014–1030. https://doi.org/10.1111/cdev.12359
Gutteling BM, de Weerth C, Buitelaar JK (2005) Prenatal stress and children’s cortisol reaction to the first day of school. Psychoneuroendocrinology 30:541–549. https://doi.org/10.1016/j.psyneuen.2005.01.002
Hankin BL, Nederhof E, Oppenheimer CW, Jenness J, Young JF, Abela JRZ et al (2011) Differential susceptibility in youth: evidence that 5-HTTLPR x positive parenting is associated with positive affect ‘for better and worse’. Transl Psychiatry 1(10):e44. https://doi.org/10.1038/tp.2011.44
Hariri AR, Mattay VS, Tessitore A, Kolachana B, Fera F, Goldman D, Egan MF, Weinberger DR (2002) Serotonin transporter genetic variation and the response of the human amygdala. Science 297(5580):400–403
Hartman S, Belsky J (2018) Prenatal programming of postnatal plasticity revisited—And extended. Dev Psychopathol 30(3):825–842
Hartman S, Sung S, Simpson JA, Schlomer GL, Belsky J (2017) Decomposing environmental unpredictability in forecasting adolescent and young adult development: a two-sample study. Dev Psychopathol 30(4):1321–1332
Hartman S, Freeman SM, Bales KL, Belsky J (2018) Prenatal stress as a risk—and an opportunity—factor. Psychol Sci 29(4):572–580
Henry C, Kabbaj M, Simon H, Moal M, Maccari S (1994) Prenatal stress increases the hypothalamo-pituitary-adrenal axis response in young and adult rats. J Neuroendocrinol 6(3):341–345. https://doi.org/10.1111/j.1365-2826.1994.tb00591.x
Herman JP, Cullinan WE (1997) Neurocircuitry of stress: central control of the hypothalamo–pituitary–adrenocortical axis. Trends Neurosci 20(2):78–84
Hertzman C, Power C (2004) Child development as a determinant of health across the life course. Curr Paediatr 14(5):438–443
Hompes T, Izzi B, Gellens E, Morreels M, Fieuws S, Pexsters A et al (2013) Investigating the influence of maternal cortisol and emotional state during pregnancy on the DNA methylation status of the glucocorticoid receptor gene (NR3C1) promoter region in cord blood. J Psychiatr Res 47(7):880–891. https://doi.org/10.1016/j.jpsychires.2013.03.009
Howland MA, Sandman CA, Glynn LM, Crippen C, Davis EP (2016) Fetal exposure to placental corticotropin-releasing hormone is associated with child self-reported internalizing symptoms. Psychoneuroendocrinology 67:10–17
Huizink AC, De Medina PGR, Mulder EJ, Visser GH, Buitelaar JK (2002) Psychological measures of prenatal stress as predictors of infant temperament. J Am Acad Child Adolesc Psychiatry 41(9):1078–1085
Jaffee SR, Price TS (2007) Gene–environment correlations: a review of the evidence and implications for prevention of mental illness. Mol Psychiatry 12:432–442. https://doi.org/10.1038/sj.mp.4001950
Jansson T, Powell TL (2007) Role of the placenta in fetal programming: Underlying mechanisms and potential interventional approaches. Clin Sci 113(1):1–13. https://doi.org/10.1042/CS20060339
Johansson A, Bergman H, Corander J, Waldman ID, Karrani N, Salo B et al (2012) Alcohol and aggressive behavior in men–moderating effects of oxytocin receptor gene (OXTR) polymorphisms. Genes Brain Behavior 11(2):214–221. https://doi.org/10.1111/j.1601-183X.2011.00744.x
Kagan J, Snidman N (2004) The long shadow of temperament. Belknap Press/Harvard University Press, Cambridge, MA, US
Kertes DA, Kamin HS, Hughes DA, Rodney NC, Bhatt S, Mulligan CJ (2016) Prenatal maternal stress predicts methylation of genes regulating the hypothalamic–pituitary–adrenocortical system in mothers and newborns in the Democratic Republic of Congo. Child Dev 87(1):61–72. https://doi.org/10.1111/cdev.12487
Khashan AS, Abel KM, McNamee R, Pedersen MG, Webb RT, Baker PN et al (2008) Higher risk of offspring schizophrenia following antenatal maternal exposure to severe adverse life events. Arch Gen Psychiatry 65(2):146–152. https://doi.org/10.1001/archgenpsychiatry.2007.20
Kim S, Kochanska G (2012) Child temperament moderates effects of parent–child mutuality on self-regulation: a relationship-based path for emotionally negative infants. Child Dev 83:1275–1289. https://doi.org/10.1111/j.1467-8624.2012.01778.x
Kim SJ, Young LJ, Gonen D, Veenstra-VanderWeele J, Courchesne R, Courchesne E et al (2002) Transmission disequilibrium testing of arginine vasopressin receptor 1A (AVPR1A) polymorphisms in autism. Mol Psychiatry 7(5):503. https://doi.org/10.1038/sj.mp.4001125
Kochanska G, Kim S, Barry RA, Philibert RA (2011) Children’s genotypes interact with maternal responsive care in predicting children’s competence: diathesis–stress or differential susceptibility? Dev Psychopathol 23:605–616. https://doi.org/10.1017/S0954579411000071
Kofman O (2002) The role of prenatal stress in the etiology of developmental behavioural disorders. Neurosci Biobehav Rev 26(4):457–470. https://doi.org/10.1016/S0149-7634(02)00015-5
Kraszpulski M, Dickerson PA, Salm AK (2006) Prenatal stress affects the developmental trajectory of the rat amygdala. Stress 9(2):85–95
Lakatos K, Nemoda Z, Birkas E, Ronai Z, Kovacs E, Ney K et al (2003) Association of D4 dopamine receptor gene and serotonin transporter promoter polymorphisms with infants’ response to novelty. Mol Psychiatry 8:90–97. https://doi.org/10.1038/sj.mp.4001212
Landry SH, Smith KE, Swank PR, Assel MA, Vellet S (2001) Does early responsive parenting have a special importance for children’s development or is consistency across early childhood necessary? Dev Psychol 37:387. https://doi.org/10.1037/0012-1649.37.3.387
Landry SH, Smith KE, Swank PR (2006) Responsive parenting: establishing early foundations for social, communication, and independent problem-solving skills. Dev Psychol 42(4):627. https://doi.org/10.1037/0012-1649.42.4.627
Laplante DP, Barr RG, Brunet A, Du Fort GG, Meaney ML, Saucier JF et al (2004) Stress during pregnancy affects general intellectual and language functioning in human toddlers. Pediatr Res 56(3):400–410. https://doi.org/10.1203/01.PDR.0000136281.34035.44
Laplante DP, Brunet A, Schmitz N, Ciampi A, King S (2008) Project ice storm: prenatal maternal stress affects cognitive and linguistic functioning in 5½-year-old children. J Am Acad Child Adolesc Psychiatry 47(9):1063–1072. https://doi.org/10.1097/CHI.0b013e31817eec80
Laplante DP, Brunet A, King S (2015) The effects of maternal stress and illness during pregnancy on infant temperament: project ice storm. Pediatr Res 79:107–113. https://doi.org/10.1038/pr.2015.177
Laurent HK, Leve LD, Neiderhiser JM, Natsuaki MN, Shaw DS, Harold GT, Reiss D (2013) Effects of prenatal and postnatal parent depressive symptoms on adopted child HPA regulation: independent and moderated influences. Dev Psychol 49(5):876. https://doi.org/10.1037/a0028800
Lee PR, Brady DL, Shapiro RA, Dorsa DM, Koenig JI (2007) Prenatal stress generates deficits in rat social behavior: reversal by oxytocin. Brain Res 1156:152–167. https://doi.org/10.1016/j.brainres.2007.04.042
Lilliecreutz C, Larén J, Sydsjö G, Josefsson A (2016) Effect of maternal stress during pregnancy on the risk for preterm birth. BMC Pregnancy Childbirth 16:5. https://doi.org/10.1186/s12884-015-0775-x
Lin Y, Xu J, Huang J, Jia Y, Zhang J, Yan C, Zhang J (2017) Effects of prenatal and postnatal maternal emotional stress on toddlers’ cognitive and temperamental development. J Affect Disord 207:9–17
Lupien SJ, McEwen BS, Gunnar MR, Heim C (2009) Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 10(6):434–445. https://doi.org/10.1038/nrn2639
Maccari S, Krugers HJ, Morley-Fletcher S, Szyf M, Brunton PJ (2014) The consequences of early-life adversity: neurobiological, behavioural and epigenetic adaptations. J Neuroendocrinol 26:707–723. https://doi.org/10.1111/jne.12175
Makino S, Gold PW, Schulkin J (1994) Corticosterone effects on corticotropin-releasing hormone mRNA in the central nucleus of the amygdala and the parvocellular region of the paraventricular nucleus of the hypothalamus. Brain Res 640(1–2):105–112
Martin RP, Noyes J, Wisenbaker J, Huttenen MO (1999) Prediction of early childhood negative emotionality and inhibition from maternal distress during pregnancy. Merrill Palmer Q 45:370–391. https://doi.org/10.1353/mpq.2008.0013
Mason WA, Mendoza SP (1998) Generic aspects of primate attachments: parents, offspring and mates. Psychoneuroendocrinology 23(8):765–778. https://doi.org/10.1016/S0306-4530(98)00054-7
Mastorakos G, Ilias I (2003) Maternal and fetal hypothalamic-pituitary-adrenal axes during pregnancy and postpartum. Ann N Y Acad Sci 997(1):136–149
McGowan PO, Suderman M, Sasaki A, Huang TC, Hallett M, Meaney MJ, Szyf M (2011) Broad epigenetic signature of maternal care in the brain of adult rats. PloS One 6(2):e14739. https://doi.org/10.1371/journal.pone.0014739
Merlot E, Couret D, Otten W (2008) Prenatal stress, fetal imprinting and immunity. Brain Behav Immun 22:42–51. https://doi.org/10.1016/j.bbi.2007.05.007
Mesiano S (2014) The endocrinology of human pregnancy and fetal-placental neuroendocrine development. In: Strauss JF, Barbieri R (eds) Yen and Jaffe’s reproductive endocrinology: physiology, pathophysiology, and clinical management. Saunders, Philadelphia, pp 243–271
Meyer-Lindenberg A, Kolachana B, Gold B, Olsh A, Nicodemus KK, Mattay V et al (2009) Genetic variants in AVPR1A linked to autism predict amygdala activation and personality traits in healthy humans. Mol Psychiatry 14(10):968–975. https://doi.org/10.1038/mp.2008.54
Miyagawa K, Tsuji M, Fujimori K, Saito Y, Takeda H (2011) Prenatal stress induces anxiety-like behavior together with the disruption of central serotonin neurons in mice. Neurosci Res 70(1):111–117
Moore SR, Depue RA (2016) Neurobehavioral foundation of environmental reactivity. Psychol Bull 142(2):107. https://doi.org/10.1037/bul0000028
Mueller BR, Bale TL (2008) Sex-specific programming of offspring emotionality after stress early in pregnancy. J Neurosci 28(36):9055–9065
NICHD Early Child Care Research Network (2005) Child Care and child development: results of the NICHD study of early child care and youth development. Guilford Press, New York. https://doi.org/10.1523/JNEUROSCI.1424-08.2008
Nolvi S, Karlsson L, Bridgett DJ, Korja R, Huizink AC, Kataja EL, Karlsson H (2016) Maternal prenatal stress and infant emotional reactivity six months postpartum. J Affect Disord 199:163–170
O’connor TG, Heron J, Golding J, Glover V (2003) Maternal antenatal anxiety and behavioural/emotional problems in children: a test of a programming hypothesis. J Child Psychol Psychiatry 44(7):1025–1036. https://doi.org/10.1111/1469-7610.00187
O’donnell K, O’connor TG, Glover V (2009) Prenatal stress and neurodevelopment of the child: focus on the HPA axis and role of the placenta. Dev Neurosci 31(4):285–292
O’Donnell KJ, Jensen AB, Freeman L, Khalife N, O’Connor TG, Glover V (2012) Maternal prenatal anxiety and downregulation of placental 11β-HSD2. Psychoneuroendocrinology 37(6):818–826. https://doi.org/10.1016/j.psyneuen.2011.09.014
Oberlander TF, Weinberg J, Papsdorf M, Grunau R, Misri S, Devlin AM (2008) Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics 3(2):97–106. https://doi.org/10.4161/epi.3.2.6034
Obradović J, Bush NR, Stamperdahl J, Adler NE, Boyce WT (2010) Biological sensitivity to context: the interactive effects of stress reactivity and family adversity on socioemotional behavior and school readiness. Child Dev 81:270–289. https://doi.org/10.1111/j.1467-8624.2009.01394.x
Obradović J, Bush NR, Boyce WT (2011) The interactive effect of marital conflict and stress reactivity on externalizing and internalizing symptoms: the role of laboratory stressors. Dev Psychopathol 23:101–114. https://doi.org/10.1017/s0954579410000672
Obradović J, Portilla XA, Ballard PJ (2016) Biological sensitivity to family income: differential effects on early executive functioning. Child Dev 87(2):374–384. https://doi.org/10.1111/cdev.12475
Olofsdotter S, Åslund C, Furmark T, Comasco E, Nilsson KW (2017) Differential susceptibility effects of oxytocin gene (OXT) polymorphisms and perceived parenting on social anxiety among adolescents. Dev Psychopathol. https://doi.org/10.1017/S0954579417000967
Parker GA, Royle NJ, Hartley IR (2002) Intrafamilial conflict and parental investment: a synthesis. Philos Trans R Soc B Biol Sci 357(1419):295–307
Pearson J, Tarabulsy GM, Bussières EL (2015) Foetal programming and cortisol secretion in early childhood: a meta-analysis of different programming variables. Infant Behav Dev 40:204–215
Pena CJ, Monk C, Champagne FA (2012) Epigenetic effects of prenatal stress on 11β-hydroxysteroid dehydrogenase-2 in the placenta and fetal brain. PloS One 7(6):e39791. https://doi.org/10.1371/journal.pone.0039791
Perkeybile AM, Griffin LL, Bales KL (2013) Natural variation in early parental care correlates with social behaviors in adolescent prairie voles (Microtus ochrogaster). Front Behav Neurosci 7:21. https://doi.org/10.3389/fnbeh.2013.00021
Pitzer M, Jennen-Steinmetz C, Esser G, Schmidt MH, Laucht M (2011) Differential susceptibility to environmental influences: the role of early temperament and parenting in the development of externalizing problems. Compr Psychiatry 52:650–658. https://doi.org/10.1016/j.comppsych.2010.10.017
Pluess M, Belsky J (2011) Prenatal programming of postnatal plasticity. Dev Psychopathol 23:29–38. https://doi.org/10.1017/s0954579410000623
Pluess M, Belsky J (2013) Vantage sensitivity: individual differences in response to positive experiences. Psychol Bull 139(4):901. https://doi.org/10.1037/a0030196
Pluess M, Velders FP, Belsky J, van IJzendoorn MH, Bakermans-Kranenburg MJ, Jaddoe VW et al (2011) Serotonin transporter polymorphism moderates effects of prenatal maternal anxiety on infant negative emotionality. Biol Psychiat 69(6):520–525. https://doi.org/10.1016/j.biopsych.2010.10.006
Poehlmann J, Hane A, Burnson C, Maleck S, Hamburger E, Shah PE (2012) Preterm infants who are prone to distress: differential effects of parenting on 36-month behavioral and cognitive outcomes. J Child Psychol Psychiatry 53(10):1018–1025. https://doi.org/10.1111/j.1469-7610.2012.02564.x
Ponder KL, Salisbury A, McGonnigal B, Laliberte A, Lester B, Padbury JF (2011) Maternal depression and anxiety are associated with altered gene expression in the human placenta without modification by antidepressant use: implications for fetal programming. Dev Psychobiol 53(7):711–723. https://doi.org/10.1002/dev.20549
Poulin MJ, Holman EA, Buffone A (2012) The neurogenetics of nice: receptor genes for oxytocin and vasopressin interact with threat to predict prosocial behavior. Psychol Sci 23(5):446–452. https://doi.org/10.1177/0956797611428471
Prichard ZM, Mackinnon AJ, Jorm AF, Easteal S (2007) AVPR1A and OXTR polymorphisms are associated with sexual and reproductive behavioral phenotypes in humans. Hum Mutat 28(11):1150–1150. https://doi.org/10.1002/humu.9510
Qiu A, Anh TT, Li Y, Chen H, Rifkin-Graboi A, Broekman BF, Kwek K, Saw SM, Chong YS, Gluckman PD, Fortier MV (2015) Prenatal maternal depression alters amygdala functional connectivity in 6-month-old infants. Transl Psychiatry 5(2):e508
Radtke KM, Ruf M, Gunter HM, Dohrmann K, Schauer M, Meyer A, Elbert T (2011) Transgenerational impact of intimate partner violence on methylation in the promoter of the glucocorticoid receptor. Transl Psychiatry 1(7):e21. https://doi.org/10.1038/tp.2011.21
Räikkönen K, Pesonen AK, Heinonen K, Lahti J, Komsi N, Eriksson JG et al (2009) Maternal licorice consumption and detrimental cognitive and psychiatric outcomes in children. Am J Epidemiol 170(9):1137–1146
Räikkönen K, Seckl JR, Heinonen K, Pyhälä R, Feldt K, Jones A et al (2010) Maternal prenatal licorice consumption alters hypothalamic–pituitary–adrenocortical axis function in children. Psychoneuroendocrinology 35(10):1587–1593
Räikkönen K, Pesonen AK, O’reilly JR, Tuovinen S, Lahti M, Kajantie E et al (2015) Maternal depressive symptoms during pregnancy, placental expression of genes regulating glucocorticoid and serotonin function and infant regulatory behaviors. Psychol Med 45(15):3217–3226. https://doi.org/10.1017/S003329171500121X
Räikkönen K, Martikainen S, Pesonen AK, Lahti J, Heinonen K, Pyhälä R et al (2017) Maternal licorice consumption during pregnancy and pubertal, cognitive, and psychiatric outcomes in children. Am J Epidemiol 185(5):317–328
Raver CC, Blair C, Willoughby M (2012) Poverty as a predictor of 4-year-olds’ executive function: new perspectives on models of differential susceptibility. Dev Psychol 49:292. https://doi.org/10.1037/a0028343
Rice F, Harold GT, Boivin J, Hay DF, Van Den Bree M, Thapar A (2009) Disentangling prenatal and inherited influences in humans with an experimental design. Proc Natl Acad Sci 106(7):2464–2467
Rice F, Harold GT, Boivin J, Van den Bree M, Hay DF, Thapar A (2010) The links between prenatal stress and offspring development and psychopathology: disentangling environmental and inherited influences. Psychol Med 40(2):335–345. https://doi.org/10.1017/S0033291709005911
Rifkin-Graboi A, Bai J, Chen H, Hameed WB, Sim LW, Tint MT, Leutscher-Broekman B, Chong YS, Gluckman PD, Fortier MV, Meaney MJ (2013). Prenatal maternal depression associates with microstructure of right amygdala in neonates at birth. Biol Psychiatry 74(11):837–844
Rioux C, Castellanos-Ryan N, Parent S, Vitaro F, Tremblay RE, Séguin JR (2016) Differential susceptibility to environmental influences: interactions between child temperament and parenting in adolescent alcohol use. Dev Psychopathol 28:265–275. https://doi.org/10.1019/S0954579415000437
Roisman GI, Newman DA, Fraley RC, Haltigan JD, Groh AM, Haydon KC (2012) Distinguishing differential susceptibility from diathesis–stress: recommendations for evaluating interaction effects. Dev Psychopathol 24(02):389–409. https://doi.org/10.1017/S0954579412000065
Rothbart MK, Bates JE (2006) Temperament. Handb Child Psychol. https://doi.org/10.1002/9780470147658.chpsy0303
Rubin DM, O'Reilly AL, Luan X, Localio AR (2007) The impact of placement stability on behavioral well-being for children in foster care. Pediatrics 119(2):336–344
Saxbe DE, Margolin G, Spies Shapiro LA, Baucom BR (2012) Does dampened physiological reactivity protect youth in aggressive family environments? Child Dev 83:821–830. https://doi.org/10.1111/j.1467-8624.2012.01752.x
Schlomer GL, Giudice DM, Ellis BJ (2011) Parent–offspring conflict theory: an evolutionary framework for understanding conflict within human families. Psychol Rev 118(3):496
Seckl JR, Holmes MC (2007) Mechanisms of disease: glucocorticoids, their placental metabolism and fetal ‘programming’ of adult pathophysiology. Nat Clin Pract Endocrinol Metab 3(6):479–488. https://doi.org/10.1038/ncpendmet0515
Seymour B, Dolan R (2008) Emotion, decision making, and the amygdala. Neuron 58(5):662–671
Shackman AJ, Fox AS, Oler JA, Shelton SE, Davidson RJ, Kalin NH (2013) Neural mechanisms underlying heterogeneity in the presentation of anxious temperament. Proceedings of the National Academy of Sciences, 201214364
Shapiro GD, Fraser WD, Frasch MG, Séguin JR (2013) Psychosocial stress in pregnancy and preterm birth: associations and mechanisms. J Perinat Med 41(6):631–645. https://doi.org/10.1515/jpm-2012-0295
Sharp H, Hill J, Hellier J, Pickles A (2015) Maternal antenatal anxiety, postnatal stroking and emotional problems in children: outcomes predicted from pre-and postnatal programming hypotheses. Psychol Med 45(2):269–283. https://doi.org/10.1017/S0033291714001342
Slagt M, Dubas JS, Deković M, van Aken MA (2016) Differences in sensitivity to parenting depending on child temperament: a meta-analysis. Psychol Bull 142:1068–1110. https://doi.org/10.1037/bul0000061
St-Pierre J, Laurent L, King S, Vaillancourt C (2016) Effects of prenatal maternal stress on serotonin and fetal development. Placenta 48:S66–S71. https://doi.org/10.1016/j.placenta.2015.11.013
Swenson RR, Beckwith BE, Lamberty KJ, Krebs SJ, Tinius TP (1990) Prenatal exposure to AVP or caffeine but not oxytocin alters learning in female rats. Peptides 11:927–932. https://doi.org/10.1016/0196-9781(90)90011-s
Tabak BA, Meyer ML, Castle E, Dutcher JM, Irwin MR, Han JH et al (2015) Vasopressin, but not oxytocin, increases empathic concern among individuals who received higher levels of paternal warmth: a randomized controlled trial. Psychoneuroendocrinology 51:253–261. https://doi.org/10.1016/j.psyneuen.2014.10.006
Takahashi LK, Kalin NH (1991) Early developmental and temporal characteristics of stress-induced secretion of pituitary-adrenal hormones in prenatally stressed rat pups. Brain Res 558(1):75–78. https://doi.org/10.1016/0006-8993(91)90715-8
Tarabulsy GM, Pearson J, Vaillancourt-Morel MP, Bussières EL, Madigan S, Lemelin JP et al (2014) Meta-analytic findings of the relation between maternal prenatal stress and anxiety and child cognitive outcome. J Dev Behav Pediatrics 35(1):38–43
Tottenham N, Sheridan MA (2010) A review of adversity, the amygdala and the hippocampus: a consideration of developmental timing. Front Hum Neurosci 3:68
Tribollet E, Goumaz M, Raggenbass M, Dubois-Dauphin M, Dreifuss JJ (1991) Early appearance and transient expression of vasopressin receptors in the brain of rat fetus and infant: an autoradiographical and electrophysiological study. Dev Brain Res 58(1):13–24. https://doi.org/10.1016/0165-3806(91)90232-8
Trivers RL (1974) Parent-offspring conflict. Integr Comp Biol 14(1):249–264
Unternaehrer E, Bolten M, Nast I, Staehli S, Meyer AH, Dempster E et al (2016) Maternal adversities during pregnancy and cord blood oxytocin receptor (OXTR) DNA methylation. Soc Cognitive Affect Neurosci 11(9):1460–1470. https://doi.org/10.1093/scan/nsw051
Van IJzendoorn MH, Belsky J, Bakermans-Kranenburg MJ (2012) Serotonin transporter genotype 5HTTLPR as a marker of differential susceptibility? A meta-analysis of child and adolescent gene-by-environment studies. Transl Psychiatry 2(8):e147. https://doi.org/10.1038/tp.2012.73
Van den Berg H, Bus AG (2014) Beneficial effects of BookStart in temperamentally highly reactive infants. Learn Ind Differ 36:69–75. https://doi.org/10.1016/j.lindif.2014.10.008
Van den Bergh BR, Mulder EJ, 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. Neurosci Biobehav Rev 29:237–258. https://doi.org/10.1016/j.neubiorev.2004.10.007
Van den Hove DLA, Lauder JM, Scheepens A, Prickaerts JHHJ, Blanco CE, Steinbusch HWM (2006) Prenatal stress in the rat alters 5-HT 1A receptor binding in the ventral hippocampus. Brain Res 1090:29–34. https://doi.org/10.1016/j.brainres.2006.03.057
Van den Bergh BR, 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 33:536–545. https://doi.org/10.1038/sj.npp.1301450
Van den Bergh BR, van den Heuvel MI, Lahti M, Braeken M, de Rooij SR, Entringer S et al (2017) Prenatal developmental origins of behavior and mental health: the influence of maternal stress in pregnancy. Neurosci Biobehav Rev. https://doi.org/10.1016/j.neubiorev.2017.07.003
Wadhwa PD, Glynn L, Hobel CJ, Garite TJ, Porto M, Chicz-DeMet A et al (2002) Behavioral perinatology: biobehavioral processes in human fetal development. Regul Pept 108:149–157. https://doi.org/10.1016/S0167-0115(02)00102-7
Walum H, Westberg L, Henningsson S, Neiderhiser JM, Reiss D, Igl W et al (2008) Genetic variation in the vasopressin receptor 1a gene (AVPR1A) associates with pair-bonding behavior in humans. Proc Natl Acad Sci 105(37):14153–14156. https://doi.org/10.1073/pnas.0803081105
Watson ED, Cross JC (2005) Development of structures and transport functions in the mouse placenta. Physiology 20(3):180–193. https://doi.org/10.1152/physiol.00001.2005
Welberg LAM, Seckl JR, Holmes MC (2001) Prenatal glucocorticoid programming of brain corticosteroid receptors and corticotrophin-releasing hormone: possible implications for behaviour. Neuroscience 104(1):71–79
Whitaker-Azmitia PM, Druse M, Walker P, Lauder JM (1996) Serotonin as a developmental signal. Behav Brain Res 73:19–29. https://doi.org/10.1016/0166-4328(96)00071-X
Wigger A, Sánchez MM, Mathys KC, Ebner K, Frank E, Liu D et al (2004) Alterations in central neuropeptide expression, release, and receptor binding in rats bred for high anxiety: critical role of vasopressin. Neuropsychopharmacology 29:1–14. https://doi.org/10.1038/sj.npp.1300290
Wroble-Biglan MC, Dietz LJ, Pienkosky TV (2009) Prediction of infant temperament from catecholamine and self-report measures of maternal stress during pregnancy. J Reprod Infant Psychol 27(4):374–389
Yehuda R, Engel SM, Brand SR, Seckl J, Marcus SM, Berkowitz GS (2005) Transgenerational effects of posttraumatic stress disorder in babies of mothers exposed to the World Trade Center attacks during pregnancy. J Clin Endocrinol Metab 90:4115–4118. https://doi.org/10.1210/jc.2005-0550
Zijlmans MA, Korpela K, Riksen-Walraven JM, de Vos WM, de Weerth C (2015a) Maternal prenatal stress is associated with the infant intestinal microbiota. Psychoneuroendocrinology 53:233–245. https://doi.org/10.1016/j.psyneuen.2015.01.006
Zijlmans MA, Riksen-Walraven JM, de Weerth C (2015b) Associations between maternal prenatal cortisol concentrations and child outcomes: a systematic review. Neurosci Biobehav Rev 53:1–24
Zuckerman M (1999) Diathesis-stress models. American Psychological Association, Washington, DC
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We would like to thank one of the self-identified reviewers, Marco Del Giudice, for his comments which greatly enhanced and extended the paper.
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Hartman, S., Belsky, J. Prenatal stress and enhanced developmental plasticity. J Neural Transm 125, 1759–1779 (2018). https://doi.org/10.1007/s00702-018-1926-9
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DOI: https://doi.org/10.1007/s00702-018-1926-9