Biological Psychiatry
Volume 67, Issue 11 , Pages 1026-1032 , 1 June 2010

Maternal Prenatal Cortisol and Infant Cognitive Development: Moderation by Infant–Mother Attachment

  • Kristin Bergman

      Affiliations

    • Institute of Reproductive and Developmental Biology, Imperial College London, Hammersmith Campus, London, United Kingdom
  • ,
  • Pampa Sarkar

      Affiliations

    • Institute of Reproductive and Developmental Biology, Imperial College London, Hammersmith Campus, London, United Kingdom
  • ,
  • Vivette Glover

      Affiliations

    • Institute of Reproductive and Developmental Biology, Imperial College London, Hammersmith Campus, London, United Kingdom
  • ,
  • Thomas G. O'Connor

      Affiliations

    • Wynne Center for Family Research, Department of Psychiatry, University of Rochester Medical Center, Rochester, New York
    • Corresponding Author InformationAddress correspondence to Tom O'Connor, Ph.D., Department of Psychiatry, University of Rochester Medical Center, Rochester, New York, 14642

Received 26 May 2009 ,Revised 9 November 2009 ,Accepted 8 January 2010.

References 

  1. Barker DJ. In utero programming of chronic disease. Clin Sci Lond. 1998;95:115–128
  2. Gluckman PD, Hanson M. The Fetal Matrix. New York: Cambridge University Press; 2005;
  3. Brown AS, Susser ES. Prenatal nutritional deficiency and risk of adult schizophrenia. Schizophr Bull. 2008;34:1054–1063
  4. Rutter M, O'Connor TG. Are there biological programming effects for psychological development? (Findings from a study of Romanian adoptees). Dev Psychol. 2004;40:81–94
  5. Khashan AS, Abel KM, McNamee R, Pedersen MG, Webb RT, Baker PN, et al. Higher risk of offspring schizophrenia following antenatal maternal exposure to severe adverse life events. Arch Gen Psychiatry. 2008;65:146–152
  6. Bergman K, Sarkar P, O'Connor TG, Modi N, Glover V. Maternal stress during pregnancy predicts cognitive ability and fearfulness in infancy. J Am Acad Child Adolesc Psychiatry. 2007;46:1454–1463
  7. Laplante DP, Barr RG, Brunet A, Galbaud du Fort G, Meaney ML, Saucier JF, et al. Stress during pregnancy affects general intellectual and language functioning in human toddlers. Pediatr Rev. 2004;56:400–410
  8. Davis EP, Glynn LM, Schetter CD, Hobel C, Chicz-Demet A, Sandman CA. Prenatal exposure to maternal depression and cortisol influences infant temperament. J Am Acad Child Adolesc Psychiatry. 2007;46:737–746
  9. Huizink AC, Robles de Medina PG, Mulder EJ, Visser GH, Buitelaar JK. Stress during pregnancy is associated with developmental outcome in infancy. J Child Psychol Psychiatry. 2003;44:810–818
  10. Van den Bergh BR, Marcoen A. High antenatal maternal anxiety is related to ADHD symptoms, externalizing problems, and anxiety in 8-and 9-year-olds. Child Dev. 2004;75:1085–1097
  11. O'Connor TG, Heron J, Golding J, Glover V. Maternal antenatal anxiety and behavioural/emotional problems in children: A test of a programming hypothesis. J Child Psychol Psychiatry. 2003;44:1025–1036
  12. Talge NM, Neal C, Glover V. Antenatal maternal stress and long-term effects on child neurodevelopment: How and why?. J Child Psychol Psychiatry. 2007;48:245–261
  13. Coe CL, Lubach GR, Karaszewski JW, Ershler WB. Prenatal endocrine activation alters postnatal cellular immunity in infant monkeys. Brain Behav Immun. 1996;10:221–234
  14. Coe CL, Kramer M, Czéh B, Gould E, Reeves AJ, Kirschbaum C, et al. Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys. Biol Psychiatry. 2003;54:1025–1034
  15. Maccari S, Darnaudery M, Morley-Fletcher S, Zuena AR, Cinque C, Van Reeth O, et al. Prenatal stress and long-term consequences: Implications of glucocorticoid hormones. Neurosci Biobehav Rev. 2003;27:119–127
  16. Weinstock M. Alterations induced by gestational stress in brain morphology and behaviour of the offspring. Prog Neurobiol. 2001;65:427–451
  17. Schneider ML, Coe CL, Lubach GR. Endocrine activation mimics the adverse effects of prenatal stress on the neuromotor development of the infant primate. Dev Psychobiol. 1992;25:427–439
  18. Setiawan E, Jackson MF, MacDonald JF, Matthews SG. Effects of repeated prenatal glucocorticoid exposure on long-term potentiation in the juvenile guinea-pig hippocampus. J Physiol. 2007;581:1033–1042
  19. Coe CL, Lubach GR. Developmental consequences of antenatal dexamethasone treatment in nonhuman primates. Neurosci Biobehav Rev. 2005;29:227–235
  20. Sizonenko SV, et al. Impact of intrauterine growth restriction and glucocorticoids on brain development: Insights using advanced magnetic resonance imaging. Mol Cell Endocrinol. 2006;254–255:163–171
  21. Salaria S, Chana G, Caldara F, Feltrin E, Altieri M, Faggioni F, et al. Microarray analysis of cultured human brain aggregates following cortisol exposure: Implications for cellular functions relevant to mood disorders. Neurobiol Dis. 2006;23:630–636
  22. Heim C, Nater UM, Maloney E, Boneva R, Jones JF, Reeves WC. Childhood trauma and risk for chronic fatigue syndrome: Association with neuroendocrine dysfunction. Arch Gen Psychiatry. 2009;66:72–80
  23. Gunnar MR, Quevedo KM. Early care experiences and HPA axis regulation in children: A mechanism for later trauma vulnerability. Prog Brain Res. 2008;167:137–149
  24. Tyrka AR, Wier L, Price LH, Ross N, Anderson GM, Wilkinson CW, et al. Childhood parental loss and adult hypothalamic-pituitary-adrenal function. Biol Psychiatry. 2008;63:1147–1154
  25. Newcomer JW, Selke G, Melson AK, Hershey T, Craft S, Richards K, et al. Decreased memory performance in healthy humans induced by stress-level cortisol treatment. Arch Gen Psychiatry. 1999;56:527–533
  26. Sapolsky RM. Why stress is bad for your brain. Science. 1996;273:749–750
  27. Maccari S, Piazza PV, Kabbaj M, Barbazanges A, Simon H, Le Moal M. Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress. J Neurosci. 1995;15:110–116
  28. Wakshlak A, Weinstock M. Neonatal handling reverses behavioral abnormalities induced in rats by prenatal stress. Physiol Behav. 1990;48:289–292
  29. Suomi SJ. Risk, resilience, and gene × environment interactions in rhesus monkeys. Ann N Y Acad Sci. 2006;1094:52–62
  30. Sarkar P, Bergman K, Fisk NM, O'Connor TG, Glover V. Ontogeny of foetal exposure to maternal cortisol using midtrimester amniotic fluid as a biomarker. Clin Endocrinol (Oxf). 2007;66:636–640
  31. Hadlock FP, Kent WR, Loyd JL, Harrist RB, Deter RL, Park SK. An evaluation of two methods for measuring fetal head and body circumferences. J Ultrasound Med. 1982;1:359–360
  32. Ainsworth MDS, Blehar MC, Waters E, Wall S. Patterns of Attachment: A Psychological Study of the Strange Situation. Hillsdale, NJ: Erlbaum; 1978;
  33. Main M, Solomon J. Procedures for identifying infants as disorganized/disoriented during the strange situation. In:  Greenberg M,  Cicchetti D,  Cummings EM editor. Attachment in the Preschool Years. Chicago: University of Chicago Press; 1990;
  34. van Ijzendoorn MH, Schuengel C, Bakermans-Kranenburg MJ. Disorganized attachment in early childhood: Meta-analysis of precursors, concomitants, and sequelae. Dev Psychopathol. 1999;11:225–249
  35. Belsky J, Rovine M, Taylor DG. The Pennsylvania infant and family development project III (The origins of individual differences in infant–mother attachment: Maternal and infant contributions). Child Dev. 1984;55:718–728
  36. Waters E. The reliability and stability of individual differences in infant–mother attachment. Child Dev. 1978;49:483–494
  37. Bayley N. Bayley Scales of Infant Development. 2nd ed.. New York: Psychological Corporation; 1983;
  38. Spielberger CDGI, Lushene RE. Manual for the State–Trait Anxiety Inventory. Palo Alto, CA: Consulting Psychologists Press; 1983;
  39. Cox JL, Holden JM, Sagovsky R. Detection of postnatal depression (Development of the 10-item Edinburgh postnatal depression scale). Br J Psychiatry. 1987;150:782–786
  40. Barnett BE, Hanna B, Parker G. Life event scales for obstetric groups. J Psychosom Res. 1983;27:313–320
  41. Buitelaar JK, Huizink AC, Mulder EJ, de Medina PG, Visser GH. Prenatal stress and cognitive development and temperament in infants. Neurobiol Aging. 2003;24(suppl 1):S53–S60
  42. Matthews SG. Antenatal glucocorticoids and programming of the developing CNS. Pediatr Review. 2000;47:291–300
  43. Challis JR, Sloboda D, Matthews SG, Holloway A, Alfaidy N, Patel FA, et al. The fetal placental hypothalamic-pituitary-adrenal (HPA) axis, parturition and post natal health. Mol Cell Endocrinol. 2001;185:135–144
  44. Lewinn KZ, Stroud LR, Molnar BE, Ware JH, Koenen KC, Buka SL. Elevated maternal cortisol levels during pregnancy are associated with reduced childhood IQ. Int J Epidemiol. 2009;
  45. Mitra R, Sapolsky RM. Acute corticosterone treatment is sufficient to induce anxiety and amygdaloid dendritic hypertrophy. Proc Natl Acad Sci U S A. 2008;105:5573–5578
  46. Uno H, Eisele S, Sakai A, Shelton S, Baker E, DeJesus O, et al. Neurotoxicity of glucocorticoids in the primate brain. Horm Behav. 1994;28:336–348
  47. Glover V, Bergman K, Sarkar P, O'Connor TG. Association between maternal and amniotic fluid cortisol is moderated by maternal anxiety. Psychoneuroendocrinology. 2009;34:430–435
  48. Hofer MA. Hidden regulators in attachment, separation, and loss. Monogr Soc Res Child Dev. 1994;59:192–207
  49. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR, et al. Epigenetic programming by maternal behavior. Nat Neurosci. 2004;7:847–854
  50. Francis D, Diorio J, Liu D, Meaney MJ. Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science. 1999;286:1155–1158
  51. Nelson CA, Zeanah CH, Fox NA, Marshall PJ, Smyke AT, Guthrie D. Cognitive recovery in socially deprived young children: The Bucharest early intervention project. Science. 2007;318:1937–1940
  52. Bergman K, Sarkar P, Glover V, O'Connor TG. Quality of child–parent attachment moderates the impact of antenatal stress on child fearfulness. J Child Psychol Psychiatry. 2008;49:1089–1098

PII: S0006-3223(10)00013-2

doi: 10.1016/j.biopsych.2010.01.002

Biological Psychiatry
Volume 67, Issue 11 , Pages 1026-1032 , 1 June 2010