Fetal exposure to maternal depressive symptoms is associated with cortical thickness in late childhood

Biological Psychiatry

Volumn 77, Issue 4, 2015, Pages 324-334

  Sandman, Curt A ^a,b   Buss, Claudia ^b,c   Head, Kevin ^a   Davis, Elysia Poggi ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d UNIVERSITY OF DENVER   (United States)

Author keywords

Childhood risk; Externalizing behavior; Fetal programming; Maternal depression; Prefrontal cortex; Structural mri

Indexed keywords

ADULT; ARTICLE; BRAIN ATROPHY; BRAIN CORTEX; BRAIN MAPPING; BRAIN SIZE; CHILD; CHILD BEHAVIOR; CHILDHOOD; DYSPHORIA; FEMALE; FETUS; FRONTAL LOBE; GESTATIONAL AGE; HUMAN; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; PREFRONTAL CORTEX; PRENATAL EXPOSURE; PRENATAL STRESS; PRIORITY JOURNAL; PROSPECTIVE STUDY; PUERPERAL DEPRESSION; RIGHT HEMISPHERE; RISK FACTOR; SCHOOL CHILD; DEPRESSION; HEMISPHERIC DOMINANCE; PATHOLOGY; PREGNANCY; PREGNANT WOMAN; PSYCHOLOGY;

ADULT; CEREBRAL CORTEX; CHILD; CHILD BEHAVIOR; DEPRESSION; FEMALE; FUNCTIONAL LATERALITY; HUMANS; LONGITUDINAL STUDIES; MAGNETIC RESONANCE IMAGING; MALE; PREGNANCY; PREGNANT WOMEN; PRENATAL EXPOSURE DELAYED EFFECTS; PROSPECTIVE STUDIES;

EID: 84922624902     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2014.06.025     Document Type: Article

References (102)

1. Fihrer I, McMahon CA, Taylor AJ (2009): The impact of postnatal and concurrent maternal depression on child behaviour during the early school years. J Affect Disord 119:116-123.
2. Kurstjens S, Wolke D (2001): Effects of maternal depression on cognitive development of children over the first 7 years of life. J Child Psychol Psychiatry 42:623-636.
3. Conroy S, Pariante CM, Marks MN, Davies HA, Farrelly S, Schacht R, Moran P (2012): Maternal psychopathology and infant development at 18 months: The impact of maternal personality disorder and depression. J Am Acad Child Adolesc Psychiatry 51:51-61.
4. McMahon C, Barnett B, Kowalenko N, Tennant C, Don N (2001): Postnatal depression, anxiety and unsettled infant behaviour. Aust N Z J Psychiatry 35:581-588.
5. Zelkowitz P, Papageorgiou A, Bardin C, Wang T (2009): Persistent maternal anxiety affects the interaction between mothers and their very low birthweight children at 24 months. Early Hum Dev 85:51-58.
6. Cornish AM, McMahon CA, Ungerer JA, Barnett B, Kowalenko N, Tennant C (2005): Postnatal depression and infant cognitive and motor development in the second postnatal year: The impact of depression chronicity and infant gender. Infant Behav Dev 28: 407-417.
7. Murray L, Arteche A, Fearon P, Halligan S, Croudace T, Cooper P (2010): The effects of maternal postnatal depression and child sex on academic performance at age 16 years: A developmental approach. J Child Psychol Psychiatry 51:1150-1159.
8. Brennan PA, Hammen C, Andersen MJ, Bor W, Najman JM, Williams GM (2000): Chronicity, severity, and timing of maternal depressive symptoms: Relationships with child outcomes at age 5. Dev Psychol 36:759-766.
9. Murray L, Sinclair D, Cooper P, Ducournau P, Turner P, Stein A (1999): The socioemotional development of 5-year-old children of postnatally depressed mothers. J Child Psychol Psychiatry 40:1259-1271.
10. Hay DF, Kumar R (1995): Interpreting the effects of mothers' postnatal depression on children's intelligence: A critique and re-analysis. Child Psychiatry Hum Dev 25:165-181.
11. Hay DF, Pawlby S, Sharp D, Asten P, Mills A, Kumar R (2001): Intellectual problems shown by 11-year-old children whose mothers had postnatal depression. J Child Psychol Psychiatry 42:871-889.
12. Verbeek T, Bockting CLH, van Pampus MG, Ormel J, Meijer JL, Hartman CA, Burger H (2012): Postpartum depression predicts offspring mental health problems in adolescence independently of parental lifetime psychopathology. J Affect Disord 136:948-954.
13. Moehler E, Kagan J, Parzer P, Brunner R, Reck C, Wiebel A, et al. (2007): Childhood behavioral inhibition and maternal symptoms of depression. Psychopathology 40:446-452.
14. Marcus Y, Altman-Gueta H, Wolff Y, Gurevitz M (2011): Rubisco mutagenesis provides new insight into limitations on photosynthesis and growth in Synechocystis PCC6803. J Exp Bot 62:4173-4182.
15. De Bellis MD, Keshavan MS, Beers SR, Hall J, Frustaci K, Masalehdan A, et al. (2001): Sex differences in brain maturation during childhood and adolescence. Cerebral Cortex 11:552-557.
16. Gerardin P, Wendland J, Bodeau N, Galin A, Bialobos S, Tordjman S, et al. (2011): Depression during pregnancy: Is the developmental impact earlier in boys? A prospective case-control study. J Clin Psychiatry 72:378-387.
17. Casey BJ, Jones RM, Hare TA (2008): The adolescent brain. Ann N Y Acad Sci 1124:111-126.
18. Sandman CA, Davis EP, Glynn LM (2012): Prescient human fetuses thrive. Psychol Sci 23:93-100.
19. 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.
20. Blair MM, Glynn LM, Sandman CA, Davis EP (2011): Prenatal maternal anxiety and early childhood temperament. Stress 14: 644-651.
21. Buss C, Davis EP, Muftuler LT, Head K, Sandman CA (2010): High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6-9-year-old children. Psychoneuroendocrinology 35:141-153.
22. Dunkel Schetter C (2009): Stress processes in pregnancy and preterm birth. Curr Dir Psychol Sci 18:204-209.
23. Dunkel Schetter C (2011): Psychological science on pregnancy: Stress processes, biopsychosocial models, and emerging research issues. Annu Rev Psychol 62:531-558.
24. Talge NM, Neal C, Glover V (2007): Antenatal maternal stress and long-term effects on child neurodevelopment: How and why? J Child Psychol Psychiatry 48:245-261.
25. 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.
26. Davis EP, Snidman N, Wadhwa PD, Dunkel Schetter C, Glynn L, Sandman CA (2004): Prenatal maternal anxiety and depression predict negative behavioral reactivity in infancy. Infancy 6:319-331.
27. Rotenberg S, McGrath JJ, Roy-Gagnon MH, Tu MT (2012): Stability of the diurnal cortisol profile in children and adolescents. Psychoneuroendocrinology 37:1981-1989.
28. Kerr DC, Leve LD, Harold GT, Natsuaki MN, Neiderhiser JM, Shaw DS, Reiss D (2013): Influences of biological and adoptive mothers' depression and antisocial behavior on adoptees' early behavior trajectories. J Abnorm Child Psychol 41:723-734.
29. Barker ED, Jaffee SR, Uher R, Maughan B (2011): The contribution of prenatal and postnatal maternal anxiety and depression to child maladjustment. Depress Anxiety 28:696-702.
30. Evans J, Melotti R, Heron J, Ramchandani P, Wiles N, Murray L, Stein A (2011): The timing of maternal depressive symptoms and child cognitive development: A longitudinal study. J Child Adolesc Psychiatry 53:632-640.
31. Korhonen M, Luoma I, Salmelin R, Tamminen T (2012): A longitudinal study of maternal prenatal, postnatal and concurrent depressive symptoms and adolescent well-being. J Affect Disord 136:680-692.
32. Peterson BS, Warner V, Bansal R, Zhu H, Hao X, Liu J, et al. (2009): Cortical thinning in persons at increased familial risk for major depression. Proc Natl Acad Sci U S A 106:6273-6278.
33. Peterson BS, Weissman MM (2011): A brain-based endophenotype for major depressive disorder. Annu Rev Med 62:461-474.
34. Tu PC, Chen LF, Hsieh JC, Bai YM, Li CT, Su TP (2012): Regional cortical thinning in patients with major depressive disorder: A surface-based morphometry study. Psychiatry Res 202:206-213.
35. Fallucca E, MacMaster FP, Haddad J, Easter P, Dick R, May G, et al. (2011): Distinguishing between major depressive disorder and obsessive-compulsive disorder in children by measuring regional cortical thickness. Arch Gen Psychiatry 68:527-533.
36. Lyoo IK, Sung YH, Dager SR, Friedman SD, Lee JY, Kim SJ, et al. (2006): Regional cerebral cortical thinning in bipolar disorder. Bipolar Disord 8:65-74.
37. Lupien SJ, Parent S, Evans AC, Tremblay RE, Zelazo PD, Corbo V, et al. (2011): Larger amygdala but no change in hippocampal volume in 10-year-old children exposed to maternal depressive symptomatology since birth. Proc Natl Acad Sci U S A 108:14324-14329.
38. Tollenaar MS, Beijers R, Jansen J, Riksen-Walraven JM, de Weerth C (2011): Maternal prenatal stress and cortisol reactivity to stressors in human infants. Stress 14:53-65.
39. Diener C, Kuehner C, Brusniak W, Ubl B, Wessa M, Flor H (2012): A meta-analysis of neurofunctional imaging studies of emotion and cognition in major depression. Neuroimage 61:677-685.
40. O'Brien GD, Queenan JT, Campbell S (1981): Assessment of gestational age in the second trimester by real-time ultrasound measurement of the femur length. Am J Obstet Gynecol 139:540-545.
41. Hobel CJ (1982): Identification of the patient at risk. In: Schwartz RH, Schneider J, editors. Perinatal Medicine: Management of the High Risk Fetus and Neonate. Baltimore: Williams & Wilkins, 3-28.
42. Hobel CJ, Youkeles L, Forsythe A (1979): Prenatal and intrapartum high-risk screening. II. Risk factors reassessed. Am J Obstet Gynecol 135:1051-1056.
43. Santor DA, Coyne JC (1997): Shortening the CES-D to improve its ability to detect cases of depression. Psychol Assess 9:233-243.
44. Radloff LS (1977): The CES-D scale: A self-report depression scale for research in the general population. Appl Psychol Meas 1:385-401.
45. Beck AT, Steer RA, Carbin MG (1988): Psychometric properties of the Beck Depression Inventory: Twenty-five years of evaluation. Clin Psychol Rev 8:77-100.
46. Armstrong J, Goldstein L (2003): Manual for the MacArthur Health and Behavior Questionnaire (HBQ 1.0). Pittsburgh: MacArthur Foundation Research Network on Psychopathology and Development, University of Pittsburgh.
47. Oldfield RC (1971): The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia 9:97-113.
48. Achenbach TM, Rescorla LA (2001): Manual for the ASEBA School- Age Forms and Profiles: An Integrated System of Multi-Informant Assessment. Burlington, VT: University of Vermont, Reaserch Center for Children, Youth, & Families.
49. Sled JG, Zijdenbos AP, Evans AC (1998): A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imaging 17:87-97.
50. Fischl B, van der Kouwe A, Destrieux C, Halgren E, Ségonne F, Salat D, et al. (2004): Automatically parcellating the human cerebral cortex. Cerebral Cortex 14:11-22.
51. Fischl B, Salat D, Busa E, Albert M, Dieterich M, Haselgrove C, et al. (2002): Whole brain segmentation: Automated labeling of neuroanatomical structures in the human brain. Neuron 33:341-355.
52. Dale AM, Fischl B, Sereno MI (1999): Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 9:179-194.
53. Fischl B, Dale AM (2000): Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci U S A 97:11050-11055.
54. Dale AM, Sereno MI (1993): Improved localization of cortical activity by combining EEG and MEG with MRI cortical surface reconstruction: A linear approach. J Cogn Neurosci 5:162-176.
55. Fischl B, Sereno MI, Tootell RBH, Dale AM (1999): High-resolution intersubject averaging and a coordinate system for the cortical surface. Hum Brain Mapp 8:272-284.
56. Baron RM, Kenny DA (1986): The moderator-mediator variable distinction in social psychological research: Conceptual, strategic, and statistical considerations. J Pers Soc Psychol 51:1173-1182.
57. Johnson SB, Blum RW, Giedd JN (2009): Adolescent maturity and the brain: The promise and pitfalls of neuroscience research in adolescent health policy. J Adolesc Health 45:216-221.
58. Lagopoulos J, Hermens DF, Naismith SL, Scott EM, Hickie IB (2012): Frontal lobe changes occur early in the course of affective disorders in young people. BMC Psychiatry 12:1-7.
59. Sacher J, Neumann J, Fünfstück T, Soliman A, Villringer A, Schroeter ML (2012): Mapping the depressed brain: A meta-analysis of structural and functional alterations in major depressive disorder. J Affect Disord 140:142-148.
60. Hamilton JP, Etkin A, Furman DJ, Lemus MG, Johnson RF, Gotlib IH (2012): Functional neuroimaging of major depressive disorder: A meta-analysis and new integration of baseline activation and neural response data. Am J Psychiatry 169:693-703.
61. Vizueta N, Rudie JD, Townsend JD, Torrisi S, Moody TD, Bookheimer SY, Altshuler LL (2012): Regional fMRI hypoactivation and altered functional connectivity during emotion processing in nonmedicated depressed patients with bipolar II disorder. Am J Psychiatry 169:831-840.
62. Diener SJ, Wessa M, Ridder S, Lang S, Diers M, Steil R, Flor H (2012): Enhanced stress analgesia to a cognitively demanding task in patients with posttraumatic stress disorder. J Affect Disord 136: 1247-1251.
63. Fu CHY, Steiner H, Costafreda SG (2013): Predictive neural biomarkers of clinical response in depression: A meta-analysis of functional and structural neuroimaging studies of pharmacological and psychological therapies. Neurobiol Dis 52:75-83.
64. van Tol MJ, van der Wee NJ, van den Heuvel OA, Nielen MM, Demenescu LR, Aleman A, et al. (2010): Regional brain volume in depression and anxiety disorders. Arch Gen Psychiatry 67:1002-1011.
65. Sandman CA, Davis EP, Buss C, Glynn LM (2012): Exposure to prenatal psychobiological stress exerts programming influences on the mother and her fetus. Neuroendocrinology 5:675-690.
66. Sandman CA, Davis EP (2012): Neurobehavioral risk is associated with gestational exposure to stress hormones. Exp Rev Endocrinol Metab 7:445-459.
67. Sandman CA, Davis EP (2010): Gestational stress influences cognition and behavior. Future Neurol 5:675-690.
68. Davis EP, Sandman CA (2012): Prenatal psychobiological predictors of anxiety risk in preadolescent children. Psychoneuroendocrinology 37:1224-1233.
69. Knorr U, Vinberg M, Kessing LV, Wetterslev J (2010): Salivary cortisol in depressed patients versus control persons: A systematic review and meta-analysis. Psychoneuroendocrinology 35:1275-1286.
70. Stetler C, Miller GE (2011): Depression and hypothalamic-pituitaryadrenal activation: A quantitative summary of four decades of research. Psychosom Med 73:114-126.
71. Foland-Ross LC, Hardin MG, Gotlib IH (2013): Neurobiological markers of familial risk for depression. Curr Top Behav Neurosci 14:181-206.
72. Schutter DJ (2012): The cerebello-hypothalamic-pituitary-adrenal axis dysregulation hypothesis in depressive disorder. Med Hypotheses 79:779-783.
73. Behnken A, Bellingrath S, Symanczik JP, Rieck MJ, Zavorotnyy M, Domschke K, et al. (2013): Associations between cognitive performance and cortisol reaction to the DEX/CRH test in patients recovered from depression. Psychoneuroendocrinology 38:447-454.
74. Brown ES, Varghese FP, McEwen BS (2004): Association of depression with medical illness: Does cortisol play a role? Biol Psychiatry 55:1-9.
75. Bao AM, Meynen G, Swaab DF (2008): The stress system in depression and neurodegeneration: Focus on the human hypothalamus. Brain Res Rev 57:531-553.
76. 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 3:97-106.
77. Marcus SM, Lopez JF, McDonough S, MacKenzie MJ, Flynn HA, Neal CR, et al. (2011): Depressive symptoms during pregnancy: Impact on neuroendocrine and neonatal outcomes. Infant Behav Dev 34:26-34.
78. Barbazanges A, Piazza PV, Le Moal M, Maccari S (1996): Maternal glucocorticoid secretion mediates long-term effects of prenatal stress. J Neurosci 16:3943-3949.
79. Pruessner JC, Dedovic K, Khalili-Mahani N, Engert V, Pruessner M, Buss C, et al. (2008): Deactivation of the limbic system during acute psychosocial stress: Evidence from positron emission tomography and functional magnetic resonance imaging studies. Biol Psychiatry 63:234-240.
80. Teicher MH, Andersen SL, Polcari A, Anderson CM, Navalta CP, Kim DM (2003): The neurobiological consequences of early stress and childhood maltreatment. Neurosci Biobehav Rev 27:33-44.
81. Uno H, Lohmiller L, Thieme C, Kemnitz JW, Engle MJ, Roecker EB, Farrel EB (1990): Brain damage induced by prenatal exposure todexamethasone in fetal macaques. I. Hippocampus. Brain Res Dev Brain Res 53:157-167.
82. Davis EP, Sandman CA, Buss C, Wing DA, Head K (2013): Fetal glucocorticoid exposure is associated with preadolescent brain development. Biol Psychiatry 74:647-655.
83. Tauber SC, Schlumbohm C, Schilg L, Fuchs E, Nau R, Gerber J (2006): Intrauterine exposure to dexamethasone impairs proliferation but not neuronal differentiation in the dentate gyrus of newborn common marmoset monkeys. Brain Pathol 16:209-217.
84. Buss C, Davis EP, Shahbaba B, Pruessner JC, Head K, Sandman CA (2012): Maternal cortisol over the course of pregnancy and subsequent child amygdala and hippocampus volumes and affective problems. Proc Natl Acad Sci U S A 109:E1312-E1319.
85. Davis EP, Townsend EL, Gunnar MR, Guiang SF, Lussky RC, Cifuentes RF, Georgieff MK (2006): Antenatal betamethasone treatment has a persisting influence on infant HPA axis regulation. J Perinatol 26:147-153.
86. Yim IS, Glynn LM, Dunkel-Schetter C, Hobel CJ, Chicz-DeMet A, Sandman CA (2009): Risk of postpartum depressive symptoms with elevated corticotropin-releasing hormone in human pregnancy. Arch Gen Psychiatry 66:162-169.
87. Yim IS, Glynn LM, Schetter CD, Hobel CJ, Chicz-Demet A, Sandman CA (2010): Prenatal beta-endorphin as an early predictor of postpartum depressive symptoms in euthymic women. J Affect Disord 125:128-133.
88. Johnson MB, Kawasawa YI, Mason CE, Krsnik Ž, Coppola G, Bogdanović D, et al. (2009): Functional and evolutionary insights into human brain development through global transcriptome analysis. Neuron 62:494-509.
89. Kostovic I, Judas M, Rados M, Hrabac P (2002): Laminar organization of the human fetal cerebrum revealed by histochemical markers and magnetic resonance imaging. Cereb Cortex 12:536-544.
90. Bourgeois JP, Goldman-Rakic PS, Rakic P (1994): Synaptogenesis in the prefrontal cortex of rhesus monkeys. Cereb Cortex 4:78-96.
91. Becker LE, Armstrong DL, Chan F, Wood MM (1984): Dendritic development in human occipital cortical neurons. Brain Res 315: 117-124.
92. Huttenlocher PR, Dabholkar AS (1997): Regional differences in synaptogenesis in human cerebral cortex. J Comp Neurol 387: 167-178.
93. Nishikuni K, Ribas GC (2012): Study of fetal and postnatal morphological development of the brain sulci. J Neurosurg Pediatr 11:1-11.
94. Spreafico R, Arcelli P, Frassoni C, Canetti P, Giaccone G, Rizzuti T, et al. (1999): Development of layer I of the human cerebral cortex after midgestation: Architectonic findings, immunocytochemical identification of neurons and glia, and in situ labeling of apoptotic cells. J Comp Neurol 410:126-142.
95. Kang HJ, Kawasawa YI, Cheng F, Zhu Y, Xu X, Li M, et al. (2011): Spatio-temporal transcriptome of the human brain. Nature 478: 483-489.
96. Muftuler LT, Davis EP, Buss C, Head K, Hasso AN, Sandman CA (2011): Cortical and subcortical changes in typically developing preadolescent children. Brain Res 1399:15-24.
97. Denver RJ (1997): Environmental stress as a developmental cue: Corticotropin-releasing hormone is a proximate mediator of adaptive phenotypic plasticity in amphibian metamorphosis. Horm Behav 31: 169-179.
98. Coall DA, Chisholm JS (2003): Evolutionary perspectives on pregnancy: Maternal age at menarche and infant birth weight. Soc Sci Med 57:1771-1781.
99. Coall DA, Chisholm JS (2010): Reproductive development and parental investment during pregnancy: Moderating influence of mother's early environment. Am J Hum Biol 22:143-153.
100. Nettle D, Coall DA, Dickins TE (2010): Birthweight and paternal involvement predict early reproduction in British women: Evidence from the National Child Development Study. Am J Hum Biol 22:172-179.
101. Lyall AE, Shi F, Geng X, Woolson S, Li G, Wang L, et al. (2014): Dynamic development of regional cortical thickness and surface area in early childhood [published online ahead of print March 2]. Cereb Cortex.
102. Jacobs B, Schall M, Prather M, Kapler E, Driscoll L, Baca S, et al. (2001): Regional dendritic and spine variation in human cerebral cortex: A quantitative Golgi study. Cereb Cortex 11:558-571.