Prenatal Maternal Cortisol Has Sex-Specific Associations with Child Brain Network Properties

Cerebral Cortex

Volumn 27, Issue 11, 2017, Pages 5230-5241

  Kim, Dae Jin ^a   Davis, Elysia Poggi ^b,c   Sandman, Curt A ^c   Sporns, Olaf ^a   O'Donnell, Brian F ^a   Buss, Claudia ^c,d   Hetrick, William P ^a  

^a INDIANA UNIVERSITY   (United States)

^b UNIVERSITY OF DENVER   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

connectome; fetal programming; maternal cortisol; pregnancy; sex differences

Indexed keywords

HYDROCORTISONE;

ARTICLE; ASSOCIATION; BRAIN FUNCTION; CHILD; CLINICAL ARTICLE; CONNECTOME; EARLY LIFE STRESS; FEMALE; FUNCTIONAL CONNECTIVITY; GESTATIONAL AGE; HUMAN; HYDROCORTISONE BLOOD LEVEL; LONGITUDINAL STUDY; MALE; PREGNANCY; PRENATAL PERIOD; PRIORITY JOURNAL; PROBLEM BEHAVIOR; PROGENY; PROSPECTIVE STUDY; SEX DIFFERENCE; BLOOD; BRAIN; DIAGNOSTIC IMAGING; GROWTH, DEVELOPMENT AND AGING; IMAGE PROCESSING; NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PRENATAL EXPOSURE; SEXUAL CHARACTERISTICS;

BRAIN; CHILD; FEMALE; HUMANS; HYDROCORTISONE; IMAGE PROCESSING, COMPUTER-ASSISTED; LONGITUDINAL STUDIES; MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PROBLEM BEHAVIOR; PROSPECTIVE STUDIES; SEX CHARACTERISTICS;

EID: 85034738788     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhw303     Document Type: Article

References (78)

1. Achard S, Bullmore E. 2007. Efficiency and cost of economical brain functional networks. PLoS Comput Biol. 3:e17.
2. Achard S, Salvador R, Whitcher B, Suckling J, Bullmore E. 2006. A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs. J Neurosci. 26:63-72.
3. Achenbach TM, Rescorla L. 2001. Manual for the ASEBA schoolage forms &profiles: an integrated system of multiinformant assessment. Burlington, VT: ASEBA.
4. Aiken CE, Ozanne SE. 2013. Sex differences in developmental programming models. Reproduction. 145:R1-13.
5. Amaral LA, Scala A, Barthelemy M, Stanley HE. 2000. Classes of small-world networks. Proc Natl Acad Sci USA. 97: 11149-11152.
6. Amat J, Baratta MV, Paul E, Bland ST, Watkins LR, Maier SF. 2005. Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nat Neurosci. 8:365-371.
7. Bale TL, Epperson CN. 2015. Sex differences and stress across the lifespan. Nat Neurosci. 18:1413-1420.
8. Ball G, Aljabar P, Zebari S, Tusor N, Arichi T, Merchant N, Robinson EC, Ogundipe E, Rueckert D, Edwards AD, et al. 2014. Rich-club organization of the newborn human brain. Proc Natl Acad Sci USA. 111:7456-7461.
9. Bassett DS, Bullmore ET, Meyer-Lindenberg A, Apud JA, Weinberger DR, Coppola R. 2009. Cognitive fitness of costefficient brain functional networks. Proc Natl Acad Sci USA. 106:11747-11752.
10. Bassett DS, Porter MA, Wymbs NF, Grafton ST, Carlson JM, Mucha PJ. 2013. Robust detection of dynamic community structure in networks. Chaos. 23:013142.
11. Behan AT, van den Hove DL, Mueller L, Jetten MJ, Steinbusch HW, Cotter DR, Prickaerts J. 2011. Evidence of femalespecific glial deficits in the hippocampus in a mouse model of prenatal stress. Eur Neuropsychopharmacol. 21:71-79.
12. Bellani M, Baiano M, Brambilla P. 2011. Brain anatomy of major depression II. Focus on amygdala. Epidemiol Psychiatr Sci. 20:33-36.
13. Bergman K, Glover V, Sarkar P, Abbott DH, O'Connor TG. 2010. In utero cortisol and testosterone exposure and fear reactivity in infancy. Horm Behav. 57:306-312.
14. Blondel VD, Guillaume JL, Lambiotte R, Lefebvre E. 2008. Fast unfolding of communities in large networks. J Stat Mech-Theory E. 2008:P10008
15. Bullmore E, Sporns O. 2012. The economy of brain network organization. Nat Rev Neurosci. 13:336-349.
16. Buss C, Davis EP, Class QA, Gierczak M, Pattillo C, Glynn LM, Sandman CA. 2009. Maturation of the human fetal startle response: evidence for sex-specific maturation of the human fetus. Early Hum Dev. 85:633-638.
17. 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 USA. 109: E1312-1319.
18. Buss C, Lord C, Wadiwalla M, Hellhammer DH, Lupien SJ, Meaney MJ, Pruessner JC. 2007. Maternal care modulates the relationship between prenatal risk and hippocampal volume in women but not in men. J Neurosci. 27: 2592-2595.
19. Chklovskii DB, Schikorski T, Stevens CF. 2002. Wiring optimization in cortical circuits. Neuron. 34:341-347.
20. Chrousos GP, Kino T. 2007. Glucocorticoid action networks and complex psychiatric and/or somatic disorders. Stress. 10: 213-219.
21. Clifton VL. 2010. Review: Sex and the human placenta: mediating differential strategies of fetal growth and survival. Placenta. 31(Suppl):S33-39.
22. Colizza V, Flammini A, Serrano MA, Vespignani A. 2006. Detecting rich-club ordering in complex networks. Nat Phys. 2:110-115.
23. 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.
24. Davis EP, Pfaff D. 2014. Sexually dimorphic responses to early adversity: implications for affective problems and autism spectrum disorder. Psychoneuroendocrinology. 49:11-25.
25. Davis EP, Sandman CA. 2012. Prenatal psychobiological predictors of anxiety risk in preadolescent children. Psychoneuroendocrinology. 37:1224-1233.
26. 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.
27. 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.
28. Davis EP, Waffarn F, Sandman CA. 2011. Prenatal treatment with glucocorticoids sensitizes the hpa axis response to stress among full-term infants. Dev Psychobiol. 53: 175-183.
29. de Weerth C, van Hees Y, Buitelaar JK. 2003. Prenatal maternal cortisol levels and infant behavior during the first 5 months. Early Hum Dev. 74:139-151.
30. Edelmann MN, Sandman CA, Glynn LM, Wing DA, Davis EP. 2016. Antenatal glucocorticoid treatment is associated with diurnal cortisol regulation in term-born children. Psychoneuroendocrinology. 72:106-112.
31. Gabory A, Roseboom TJ, Moore T, Moore LG, Junien C. 2013. Placental contribution to the origins of sexual dimorphism in health and diseases: sex chromosomes and epigenetics. Biol Sex Differ. 4:5.
32. Geuze E, Vermetten E, Bremner JD. 2005. MR-based in vivo hippocampal volumetrics: 2. Findings in neuropsychiatric disorders. Mol Psychiatry. 10:160-184.
33. Giannopoulos G, Jackson K, Tulchinsky D. 1982. Glucocorticoid metabolism in human placenta, decidua, myometrium and fetal membranes. J Steroid Biochem. 17:371-374.
34. Giedd JN, Raznahan A, Mills KL, Lenroot RK. 2012. Review: magnetic resonance imaging of male/female differences in human adolescent brain anatomy. Biol Sex Differ. 3:19.
35. Gitau R, Cameron A, Fisk NM, Glover V. 1998. Fetal exposure to maternal cortisol. Lancet. 352:707-708.
36. Gong G, Rosa-Neto P, Carbonell F, Chen ZJ, He Y, Evans AC. 2009. Age-and gender-related differences in the cortical anatomical network. J Neurosci. 29:15684-15693.
37. Hagmann P, Cammoun L, Gigandet X, Meuli R, Honey CJ, Wedeen VJ, Sporns O. 2008. Mapping the structural core of human cerebral cortex. PLoS Biol. 6:e159.
38. Halpern DF. 2000.Sex differences in cognitive abilities. Mahwah, NJ: L. Erlbaum Associates.
39. Ingalhalikar M, Smith A, Parker D, Satterthwaite TD, Elliott MA, Ruparel K, Hakonarson H, Gur RE, Gur RC, Verma R. 2014. Sex differences in the structural connectome of the human brain. Proc Natl Acad Sci USA. 111:823-828.
40. Jacobs N, Van Gestel S, Derom C, Thiery E, Vernon P, Derom R, Vlietinck R. 2001. Heritability estimates of intelligence in twins: effect of chorion type. Behav Genet. 31:209-217.
41. Kim DJ, Davis EP, Sandman CA, Sporns O, O'Donnell BF, Buss C, Hetrick WP. 2014. Longer gestation is associated with more efficient brain networks in preadolescent children. Neuroimage. 100:619-627.
42. Kim DJ, Davis EP, Sandman CA, Sporns O, O'Donnell BF, Buss C, Hetrick WP. 2015. Children's intellectual ability is associated with structural network integrity. Neuroimage. 124:550-556.
43. Kostovic I, Jovanov-Milosevic N. 2006. The development of cerebral connections during the first 20-45 weeks' gestation. Semin Fetal Neonatal Med. 11:415-422.
44. Lancichinetti A, Fortunato S. 2012. Consensus clustering in complex networks. Sci Rep. 2:336.
45. Latora V, Marchiori M. 2001. Efficient behavior of small-world networks. Phys Rev Lett. 87:198701.
46. Latora V, Marchiori M. 2003. Economic small-world behavior in weighted networks. Eur Phys J B. 32:249-263.
47. Laughlin SB, Sejnowski TJ. 2003. Communication in neuronal networks. Science. 301:1870-1874.
48. Lewis G, Rice F, Harold GT, Collishaw S, Thapar A. 2011. Investigating environmental links between parent depression and child depressive/anxiety symptoms using an assisted conception design. J Am Acad Child Adolesc Psychiatry. 50:451-459e451.
49. Lim S, Han CE, Uhlhaas PJ, Kaiser M. 2015. Preferential detachment during human brain development: age-and sexspecific structural connectivity in diffusion tensor imaging (DTI) data. Cereb Cortex. 25:1477-1489.
50. Maslov S, Sneppen K. 2002. Specificity and stability in topology of protein networks. Science. 296:910-913.
51. McMullen S, Langley-Evans SC, Gambling L, Lang C, Swali A, McArdle HJ. 2012. A common cause for a common phenotype: The gatekeeper hypothesis in fetal programming. Med Hypotheses. 78:88-94.
52. Melnick M, Myrianthopoulos NC, Christian JC. 1978. The effects of chorion type on variation in IQ in the NCPP twin population. Am J Hum Genet. 30:425-433.
53. Mueller BR, Bale TL. 2008. Sex-specific programming of offspring emotionality after stress early in pregnancy. J Neurosci. 28:9055-9065.
54. Murmu MS, Salomon S, Biala Y, Weinstock M, Braun K, Bock J. 2006. Changes of spine density and dendritic complexity in the prefrontal cortex in offspring of mothers exposed to stress during pregnancy. Eur J Neurosci. 24:1477-1487.
55. Murphy VE, Smith R, Giles WB, Clifton VL. 2006. Endocrine regulation of human fetal growth: the role of the mother, placenta, and fetus. Endocr Rev. 27:141-169.
56. Mwaniki MK, Atieno M, Lawn JE, Newton CR. 2012. Long-term neurodevelopmental outcomes after intrauterine and neonatal insults: a systematic review. Lancet. 379:445-452.
57. Nicolaides NC, Galata Z, Kino T, Chrousos GP, Charmandari E. 2010. The human glucocorticoid receptor: molecular basis of biologic function. Steroids. 75:1-12.
58. Opsahl T, Colizza V, Panzarasa P, Ramasco JJ. 2008. Prominence and control: the weighted rich-club effect. Phys Rev Lett. 101:168702.
59. Peacock JL, Marston L, Marlow N, Calvert SA, Greenough A. 2012. Neonatal and infant outcome in boys and girls born very prematurely. Pediatr Res. 71:305-310.
60. Radloff LS. 1977. The CESD scale: a self-report depression scale for research in the general population. Appl Psychol Meas. 1: 385-401
61. Rubinov M, Sporns O. 2010. Complex network measures of brain connectivity: uses and interpretations. Neuroimage. 52:1059-1069.
62. Ryman SG, van den Heuvel MP, Yeo RA, Caprihan A, Carrasco J, Vakhtin AA, Flores RA, Wertz C, Jung RE. 2014. Sex differences in the relationship between white matter connectivity and creativity. Neuroimage. 101:380-389.
63. Saif Z, Dyson RM, Palliser HK, Wright IM, Lu N, Clifton VL. 2016. Identification of eight different isoforms of the glucocorticoid receptor in guinea pig placenta: relationship to preterm delivery, sex and betamethasone exposure. PLoS One. 11: e0148226.
64. Sandman CA, Buss C, Head K, Davis EP. 2015. Fetal exposure to maternal depressive symptoms is associated with cortical thickness in late childhood. Biol Psychiatry. 77:324-334.
65. Sandman CA, Davis EP. 2012. Neurobehavioral risk is associated with gestational exposure to stress hormones. Expert Rev Endocrinol Metab. 7:445-459.
66. Sandman CA, Glynn LM, Davis EP. 2013. Is there a viabilityvulnerability tradeoff? Sex differences in fetal programming. J Psychosom Res. 75:327-335.
67. Spielberger C. 1983. State-trait anxiety inventory. Redwood City, CA: Mind Garden.
68. Sporns O. 2011. Networks of the brain. Cambridge, MA: MIT Press.
69. Sporns O, Betzel RF. 2016. Modular brain networks. Annu Rev Psychol. 67:613-640.
70. Sun Y, Lee R, Chen Y, Collinson S, Thakor N, Bezerianos A, Sim K. 2015. Progressive gender differences of structural brain networks in healthy adults: a longitudinal, diffusion tensor imaging study. PLoS One. 10:e0118857.
71. Taylor PA, Biswal B. 2011. Geometric analysis of the bdependent effects of Rician signal noise on diffusion tensor imaging estimates and determining an optimal b value. Magn Reson Imaging. 29:777-788.
72. Taylor PA, Saad ZS. 2013. FATCAT: (an efficient) Functional and Tractographic Connectivity Analysis Toolbox. Brain Connect. 3:523-535.
73. Ter Wolbeek M, Kavelaars A, de Vries WB, Tersteeg-Kamperman M, Veen S, Kornelisse RF, van Weissenbruch M, Baerts W, Liem KD, van Bel F, et al. 2015. Neonatal glucocorticoid treatment: long-term effects on the hypothalamus-pituitary-adrenal axis, immune system, and problem behavior in 14-17 year old adolescents. Brain Behav Immun. 45:128-138.
74. Torday JS, Nielsen HC, Fencl Mde M, Avery ME. 1981. Sex differences in fetal lung maturation. Am Rev Respir Dis. 123:205-208.
75. van den Heuvel MP, Kahn RS, Goni J, Sporns O. 2012. High-cost, high-capacity backbone for global brain communication. Proc Natl Acad Sci USA. 109:11372-11377.
76. van den Heuvel MP, Sporns O. 2011. Rich-club organization of the human connectome. J Neurosci. 31:15775-15786.
77. Walker MG, Fitzgerald B, Keating S, Ray JG, Windrim R, Kingdom JC. 2012. Sex-specific basis of severe placental dysfunction leading to extreme preterm delivery. Placenta. 33:568-571.
78. Woon FL, Hedges DW. 2008. Hippocampal and amygdala volumes in children and adults with childhood maltreatment-related posttraumatic stress disorder: a meta-analysis. Hippocampus. 18:729-736.