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Neurobehavioral Consequences of Fetal Exposure to Gestational Stress

  • Chapter
Fetal Development

Abstract

Through intimate communications with the mother, the fetus receives information that is integrated into its neurodevelopmental program to prepare for life after birth. Because the fetal nervous system develops at rapid speed, at precise times and in a specific sequence from conception to birth, disruption in the timing or sequence of development results in tissue remodeling and altered function. Fetal exposures to maternal signals of psychobiological stress are associated with increased risk for behavioral disorders and alterations in brain structures. We have devoted nearly three decades exploring the effects of psychobiological stress in several large cohorts of mothers and their offspring. The focus of this chapter is on the persisting developmental plasticity induced by fetal exposure and adaptation to signals of stress and adversity. Specifically the emphasis is on the emotional, cognitive, and neurological consequences for the newborn, infant, toddler, and child, exposed as fetuses to maternal stress. We review evidence that maternal psychological states and experiences during pregnancy, including stress exposures, mood, fears, and concerns about the course of her pregnancy as well as the level of biological stress signals, exert programming influences on the developing fetus.

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Notes

  1. 1.

    The device and administration influences the results (Kisilevsky, Fearon, & Muir 1998). On the mother’s abdomen we applied a 1 s administration of the VAS (72 dB, 75 Hz + 10 % harmonics ranging from 20 to 9000 Hz; EAL Model 146, Corometric Medical System, CT, USA).

  2. 2.

    It is unknown why measures of distress relevant to pregnancy have a greater impact on child outcome than measures of generalized anxiety. But it is probable that a woman’s fears, beliefs and concerns about pregnancy has direct and local implications for well-being and is the primary source of anxiety during pregnancy. As such, it may be the most important psychosocial index of anxiety that can affect birth and child outcome.

References

  • Abdou, C. M., Dunkel Schetter, C., Campos, B., Hilmert, C. J., Dominguez, T. P., Hobel, C. J., …, Sandman, C. (2010). Communalism predicts prenatal affect, stress, and physiology better than ethnicity and socioeconomic status. Cultural Diversity & Ethnic Minority Psychology, 16, 395–403. doi:10.1037/a0019808.

    Google Scholar 

  • Achenbach, T. M., & Rescorla, L. A. (2001). Manual for the ASEBA school-age forms and profiles. Burlington, VT: University of Vermont.

    Google Scholar 

  • Adams, K. M., & Nelson, J. L. (2004). Microchimerism - An investigative frontier in autoimmunity and transplantation. Journal of the American Medical Association, 291, 1127–1131. doi:10.1001/jama.291.9.1127.

    Article  PubMed  Google Scholar 

  • Almli, C. R., Ball, R. H., & Wheeler, M. E. (2001). Human fetal and neonatal movement patterns: Gender differences and fetal-to-neonatal continuity. Developmental Psychobiology, 38, 252–273. doi:10.1002/dev.1019.

    Article  PubMed  Google Scholar 

  • Appley, M. H., & Trumbull, R. (1967). Psychobiological stress: Issues in research. Toronto, ON: Appleton.

    Google Scholar 

  • Armitage, J. A., Taylor, P. D., & Poston, L. (2005). Experimental models of developmental programming: Consequences of exposure to an energy rich diet during development. Journal of Physiology, 565, 3–8. doi:10.1113/jphysiol.2004.079756.

    Article  PubMed  PubMed Central  Google Scholar 

  • Avishai-Eliner, S., Brunson, K. L., Sandman, C. A., & Baram, T. Z. (2002). Stressed-out, or in (utero)? Trends in Neurosciences, 25, 518–524. doi:10.1016/S0166-2236(02)02241-5.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ballard, J. L., Khoury, J. C., Wedig, K., Wang, L., Eilers-Walsman, B. L., & Lipp, R. (1991). New Ballard score, expanded to include extremely premature infants. Journal of Pediatrics, 199, 417–423. doi:10.1016/S0022-3476(05)82056-6.

    Article  Google Scholar 

  • Barker, D. J. (1998). Mothers, babies and health in later life. Edinburgh: Churchill Livingston.

    Google Scholar 

  • Barker, E. D., Jaffee, S. R., Uher, R. U., & Maughan, B. (2011). The contribution of prenatal and postnatal maternal anxiety and depression to child maladjustment. Depression and Anxiety, 28, 696–702. doi:10.1002/da.20856.

    Article  PubMed  Google Scholar 

  • Barker, D. J., Osmond, C., Simmonds, S. J., & Wield, G. A. (1993). The relation of small head circumference and thinness at birth to death from cardiovascular disease in adult life. BMJ, 306(6875), 422–426.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bayley, N. (1993). Bayley scales of infant development (2nd ed.). San Antonio, TX: The Psychological Corporation.

    Google Scholar 

  • Becker, L. E., Armstrong, D. L., Chan, F., & Wood, M. M. (1984). Dendritic development in human occipital cortical neurons. Brain Research, 315, 117–124. doi:10.1016/0165-3806(84)90083-X.

    Article  PubMed  Google Scholar 

  • Beckwith, B. E., Sandman, C. A., Hothersall, D., & Kastin, A. J. (1977). Influence of neonatal injections of alpha-MSH on learning, memory and attention in rats. Physiology and Behavior, 18, 63–71. doi:10.1016/0031-9384(77)90095-6.

    Article  PubMed  Google Scholar 

  • Benirschke, K., & Kaufmann, P. (1995). Pathology of the human placenta (3rd ed.). New York, NY: Springer.

    Book  Google Scholar 

  • Bergman, K., Sarkar, P., O’Connor, T. G., Modi, N., & Glover, V. (2007). Maternal stress during pregnancy predicts cognitive ability and fearfulness in infancy. Journal of the American Academy of Child and Adolescent Psychiatry, 46, 1454–1463. doi:10.1097/chi.0b013e31814a62f6.

    Article  PubMed  Google Scholar 

  • Bianchi, D. W., Zickwolf, G. K., Weil, G. J., Sylvester, S., & DeMaria, M. A. (1996). Male fetal progenitor cells persist in maternal blood for as long as 27 years postpartum. Proceedings of the National Academy of Sciences of the United States of America, 93, 705–708. doi:10.1073/pnas.93.2.705.

    Article  PubMed  PubMed Central  Google Scholar 

  • Blair, K. S., Geraci, M., Smith, B. W., Hollon, N., DeVido, J., Otero, M., …, Pine, D. S. (2012). Reduced dorsal anterior cingulate cortical activity during emotional regulation and top-down attentional control in generalized social phobia, generalized anxiety disorder, and comorbid generalized social phobia/generalized anxiety disorder. Biological Psychiatry, 72, 476–482. doi:10.1016/j.biopsych.2012.04.013.

    Google Scholar 

  • Blair, M. M., Glynn, L. M., Sandman, C. A., & Davis, E. P. (2011). Prenatal maternal anxiety and early childhood temperament. Stress, 14, 644–651. doi:10.3109/10253890.2011.594121.

    Article  PubMed  Google Scholar 

  • Boes, A. D., McCormick, L. M., Coryell, W. H., & Nopoulos, P. (2008). Rostral anterior cingulate cortex volume correlates with depressed mood in normal healthy children. Biological Psychiatry, 63, 391–397. doi:10.1016/j.biopsych.2007.07.018.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bohnert, K. M., & Breslau, N. (2008). Stability of psychiatric outcomes of low birth weight: A longitudinal investigation. Archives of General Psychiatry, 65, 1080–1086. doi:10.1001/archpsyc.65.9.1080.

    Article  PubMed  Google Scholar 

  • Bourgeois, J. P., Goldman-Rakic, P. S., & Rakic, P. (1994). Synaptogenesis in the prefrontal cortex of rhesus monkeys. Cerebral Cortex, 4, 78–96. doi:10.1093/cercor/4.1.78.

    Article  PubMed  Google Scholar 

  • Buss, C., Davis, E. P., Class, Q. A., Gierczak, M., Pattillo, C., Glynn, L. M., & Sandman, C. A. (2009). Maturation of the human fetal startle response: evidence for sex-specific maturation of the human fetus. Early Human Development, 85, 633–638. doi:10.1016/j.earlhumdev.2009.08.001.

    Google Scholar 

  • 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, 665–676. doi:10.3109/10253890.2011.623250.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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, 141–153. doi:10.1016/j.psyneuen.2009.07.010.

    Article  PubMed  PubMed Central  Google Scholar 

  • Buss, C., Davis, E. P., Shahbaba, B., Pruessner, J. C., Head, K., & Sandman, C. A. (2012). Maternal cortisol over the course of pregnancy and subsequent child amygdala and hippocampus volumes and affective problems. Proceedings of the National Academy of Sciences of the United States of America, 109, E1312–E1319. doi:10.1073/pnas.1201295109.

    Article  PubMed  PubMed Central  Google Scholar 

  • Campbell, E. A., Linton, E. A., Wolfe, C. D., Scraggs, P. R., Jones, M. T., & Lowry, P. J. (1987). Plasma corticotropin-releasing hormone concentrations during pregnancy and parturition. Journal of Clinical Endocrinology and Metabolism, 64, 1054–1059. doi:10.1210/jcem-64-5-1054.

    Article  PubMed  Google Scholar 

  • Campos, B., Schetter, C. D., Abdou, C. M., Hobel, C. J., Glynn, L. M., & Sandman, C. A. (2008). Familialism, social support, and stress: positive implications for pregnant Latinas. Cultural Diversity & Ethnic Minority Psychology, 14, 155–162. doi:10.1037/1099-9809.14.2.155.

    Article  Google Scholar 

  • Cao, X., Laplante, D. P., Brunet, A., Ciampi, A., & King, S. (2014). Prenatal maternal stress affects motor function in 5½-year-old children: Project Ice Storm. Developmental Psychobiology, 56, 117–125. doi:10.1002/dev.21085.

    Article  PubMed  Google Scholar 

  • Champney, T. F., Sahley, T. L., & Sandman, C. A. (1976). Effects of neonatal cerebral ventricular injection of ACTH 4-9 and subsequent adult injections on learning in male and female albino rats. Pharmacology, Biochemistry and Behavior, 5, 3–9. doi:10.1016/0091-3057(76)90321-X.

    Article  PubMed  Google Scholar 

  • Chan, E. C., Smith, R., Lewin, T., Brinsmead, M. W., Zhang, H. P., Cubis, J., …, Hurt, D. (1993). Plasma corticotropin-releasing hormone, beta-endorphin and cortisol inter-relationships during human pregnancy. Acta Endocrinologica (Copenhagen), 128, 339–344. doi:10.1530/acta.0.1280339.

    Google Scholar 

  • Chrousos, G. P. (1992). Regulation and dysregulation of the hypothalamic-pituitary-adrenal axis. The corticotropin-releasing hormone perspective. Endocrinology and Metabolism Clinics of North America, 21(4), 833–858.

    PubMed  Google Scholar 

  • Class, Q. A., Buss, C., Davis, E. P., Gierczak, M., Pattillo, C., Chicz-DeMet, A., & Sandman, C. A. (2008). Low levels of corticotropin-releasing hormone during early pregnancy are associated with precocious maturation of the human fetus. Developmental Neuroscience, 30, 419–426. doi:10.1159/000191213.

    Google Scholar 

  • Cleal, J. K., Poore, K. R., Boullin, J. P., Khan, O., Chau, R., Hambidge, O., …, Green, L. R. (2007). Mismatched pre- and postnatal nutrition leads to cardiovascular dysfunction and altered renal function in adulthood. Proceedings of the National Academy of Sciences of the United States of America, 104, 9529–9533. doi:10.1073/pnas.0610373104.

    Google Scholar 

  • Clifton, V. L. (2010). Review: Sex and the human placenta: Mediating differential strategies of fetal growth and survival. Placenta, 31, S33–S39. doi:10.1016/j.placenta.2009.11.010.

    Article  PubMed  Google Scholar 

  • Cooperstock, M., & Campbell, J. (1996). Excess males in preterm birth: Interactions with gestational age, race, and multiple birth. Obstetrics and Gynecology, 88, 189–193. doi:10.1016/0029-7844(96)00106-8.

    Article  PubMed  Google Scholar 

  • Costello, E. J., Worthman, C., Erkanli, A., & Angold, A. (2007). Prediction from low birth weight to female adolescent depression: A test of competing hypotheses. Archives of General Psychiatry, 64, 338–344. doi:10.1001/archpsyc.64.3.338.

    Article  PubMed  Google Scholar 

  • Cratty, M. S., Ward, H. E., Johnson, E. A., Azzaro, A. J., & Birkle, D. L. (1995). Prenatal stress increases corticotropin-releasing factor (CRF) content and release in rat amygdala minces. Brain Research, 675, 297–302. doi:10.1016/0006-8993(95)00087-7.

    Article  PubMed  Google Scholar 

  • Davis, E. P., Buss, C., Muftuler, L. T., Head, K., Hasso, A., Wing, D. A., …, Sandman, C. A. (2011). Children’s brain development benefits from longer gestation. Frontiers in Psychology, 2, 1. doi:10.3389/fpsyg.2011.00001.

    Google Scholar 

  • Davis, E. P., Glynn, L. M., Dunkel-Schetter, C., Hobel, C., Chicz-Demet, A., & Sandman, C. A. (2005). Corticotropin-releasing hormone during pregnancy is associated with infant temperament. Developmental Neuroscience, 27, 299–305. doi:10.1159/000086709.

    Article  PubMed  Google Scholar 

  • Davis, E. P., Glynn, L. M., Dunkel-Schetter, C. D., Hobel, C., Chicz-Demet, A., & Sandman, C. A. (2007). Prenatal exposure to maternal depression and cortisol influences infant temperament. Journal of the American Academy of Child and Adolescent Psychiatry, 46, 737–746. doi:10.1097/chi.0b013e318047b775.

    Article  PubMed  Google Scholar 

  • 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, 119–129. doi:10.1111/j.1469-7610.2010.02314.x.

    Article  PubMed  PubMed Central  Google Scholar 

  • Davis, J. O., Phelps, J. A., & Bracha, H. S. (1995). Prenatal development of monozygotic twins and concordance for schizophrenia. Schizophrenia Bulletin, 21(3), 357–366.

    Article  PubMed  Google Scholar 

  • Davis, E. P., & Sandman, C. A. (2010). The timing of prenatal exposure to maternal cortisol and psychosocial stress is associated with human infant cognitive development. Child Development, 81, 131–148. doi:10.1111/j.1467-8624.2009.01385.x.

    Article  PubMed  PubMed Central  Google Scholar 

  • Davis, E. P., & Sandman, C. A. (2012). Prenatal psychobiological predictors of anxiety risk in preadolescent children. Psychoneuroendocrinology, 37, 1224–1233. doi:10.1016/j.psyneuen.2011.12.016.

    Article  PubMed  PubMed Central  Google Scholar 

  • Davis, E. P., Sandman, C. A., Buss, C., Wing, D. A., & Head, K. (2013). Fetal glucocorticoid exposure is associated with preadolescent brain development. Biological Psychiatry, 74, 647–655. doi:10.1016/j.biopsych.2013.03.009.

    Article  PubMed  PubMed Central  Google Scholar 

  • Davis, E. P., Snidman, N., Wadhwa, P. D., Dunkel-Schetter, C., Glynn, L., & Sandman, C. A. (2004). Prenatal maternal anxiety and depression predict negative behavioral reactivity in infancy. Infancy, 6, 319–331. doi:10.1207/s15327078in0603_1.

    Article  Google Scholar 

  • Davis, E. P., Waffarn, F., Uy, C., Hobel, C. J., Glynn, L. M., & Sandman, C. A. (2009). Effect of prenatal glucocorticoid treatment on size at birth among infants born at term gestation. Journal of Perinatology, 29, 731–737. doi:10.1038/jp.2009.85.

    Article  PubMed  PubMed Central  Google Scholar 

  • Davis, E. P., Waffarn, F., & Sandman, C. A. (2011). Prenatal treatment with glucocorticoids sensitizes the HPA axis response to stress among full-term infants. Developmental Psychobiology, 53, 175–183. doi:10.1002/dev.20510.

    Article  PubMed  Google Scholar 

  • de Weerth, C., & Buitelaar, J. K. (2005). Cortisol awakening response in pregnant women. Psychoneuroendocrinology, 30, 902–907. doi:10.1016/j.psyneuen.2005.05.003.

    Article  PubMed  Google Scholar 

  • de Weerth, C., Van Hees, Y., & Buitelaar, J. (2003). Prenatal maternal cortisol levels and infant behavior during the first 5 months. Early Human Development, 74, 139–151. doi:10.1016/S0378-3782(03)00088-4.

    Article  PubMed  Google Scholar 

  • DiPietro, J. A., Bornstein, M. H., Costigan, K. A., Pressman, E. K., Hahn, C. S., Painter, K., …, Yi, L. J. (2002). What does fetal movement predict about behavior during the first two years of life? Developmental Psychobiology, 40, 358–371. doi:10.1002/dev.10025.

    Google Scholar 

  • DiPietro, J. A., Bornstein, M. H., Hahn, C. S., Costigan, K., & Achy-Brou, A. (2007). Fetal heart rate and variability: stability and prediction to developmental outcomes in early childhood. Child Development, 78, 1788–1798. doi:10.1111/j.1467-8624.2007.01099.x.

    Article  PubMed  PubMed Central  Google Scholar 

  • DiPietro, J. A., Costigan, K. A., Pressman, E. K., & Doussard-Roosevelt, J. A. (2000). Antenatal origins of individual differences in heart rate. Developmental Psychobiology, 37, 221–228. doi:10.1002/1098-2302(2000)37:4<221::AID-DEV2>3.0.CO;2-A.

    Article  PubMed  Google Scholar 

  • DiPietro, J. A., Costigan, K. A., & Pressman, E. K. (2002). Fetal state concordance predicts infant state regulation. Early Human Development, 68, 1–13. doi:10.1016/S0378-3782(02)00006-3.

    Article  PubMed  Google Scholar 

  • DiPietro, J. A., Costigan, K. A., & Voegtline, K. M. (2015). Studies in fetal behavior: Revisited, renewed and reimagined. Child Development Monograph, July, 2015.

    Google Scholar 

  • DiPietro, J. A., Hodgson, D. M., Costigan, K. A., & Johnson, T. R. (1996). Fetal antecedents of infant temperament. Child Development, 67, 2568–2583. doi:10.2307/1131641.

    Article  PubMed  Google Scholar 

  • DiPietro, J. A., Irizarry, R. A., Hawkins, M., Costigan, K. A., & Pressman, E. K. (2001). Cross-correlation of fetal cardiac and somatic activity as an indicator of antenatal neural development. American Journal of Obstetrics and Gynecology, 185, 1421–1428. doi:10.1067/mob.2001.119108.

    Article  PubMed  Google Scholar 

  • DiPietro, J. A., Novak, M. F. S. X., Costigan, K. A., Atela, L. D., & Ruesing, S. P. (2006). Maternal psychological distress during pregnancy in relation to child development at age two. Child Development, 77, 573–587. doi:10.1111/j.1467-8624.2006.00891.x.

    Article  PubMed  Google Scholar 

  • Dominguez, T. P., Dunkel-Schetter, C., Glynn, L. M., Hobel, C., & Sandman, C. A. (2008). Racial differences in birth outcomes: the role of general, pregnancy, and racism stress. Health Psychology, 27, 194–203. doi:10.1037/0278-6133.27.2.194.

    Article  PubMed  PubMed Central  Google Scholar 

  • Dunkel-Schetter, C., & Glynn, L. (2011). Stress in pregnancy: Empirical evidence and theoretical issues to guide interdisciplinary research. In R. Contrada & A. Baum (Eds.), Handbook of stress science: Biology, psychology, and health (pp. 321–344). New York, NY: Springer.

    Google 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. Developmental Psychopathology, 23, 7–28. doi:10.1017/S0954579410000611.

    Article  Google Scholar 

  • Ellman, L. M., Dunkel-Schetter, C., Hobel, C. J., Chicz-DeMet, A., Glynn, L. M., & Sandman, C. A. (2008). Timing of fetal exposure to stress hormones: Effects on newborn physical and neuromuscular maturation. Developmental Psychobiology, 50, 232–241. doi:10.1002/dev.20293.

    Article  PubMed  PubMed Central  Google Scholar 

  • Entringer, S., Buss, C., Andersen, J. A., Chicz-De Met, A., & Wadhwa, P. (2011). Ecological momentary assessment of maternal cortisol profiles over a multiple-day period predicts the length of human gestation. Psychosomatic Medicine, 73, 469–474. doi:10.1097/PSY.0b013e31821fbf9a.

    Article  PubMed  PubMed Central  Google Scholar 

  • Entringer, S., Buss, C., Shirtcliff, E. A., Cammack, A. L., Yim, I. S., Chicz-DeMet, A., …, Wadhwa, P. D. (2009). Attenuation of maternal psychophysiological stress responses and the maternal cortisol awakening response (CAR) over the course of human pregnancy. Stress, 13, 258–268. doi:10.3109/10253890903349501.

    Google Scholar 

  • Etkin, A., & Schatzberg, A. F. (2011). Common abnormalities and disorder-specific compensation during implicit regulation of emotional processing in generalized anxiety and major depressive disorders. The American Journal of Psychiatry, 168, 968–978. doi:10.1176/appi.ajp.2011.10091290.

    Article  PubMed  Google Scholar 

  • 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. Journal of Child Psychology & Psychiatry, 53, 632–640. doi:10.1111/j.1469-7610.2011.02513.x.

    Google Scholar 

  • Fallucca, E., MacMaster, F. P., Haddad, J., Easter, P., Dick, R., May, G., …, Rosenberg, D.R. (2011). Distinguishing between major depressive disorder and obsessive-compulsive disorder in children by measuring regional cortical thickness. Archives of General Psychiatry, 68, 527–533. doi:10.1001/archgenpsychiatry.2011.36.

    Google Scholar 

  • Fihrer, I., McMahon, C. A., & Taylor, A. J. (2009). The impact of postnatal and concurrent maternal depression on child behaviour during the early school years. Journal of Affective Disorders, 119, 116–123. doi:10.1016/j.jad.2009.03.001.

    Article  PubMed  Google Scholar 

  • Fowden, A. L., Coan, P. M., Angiolini, E., Burton, G. J., & Constancia, M. (2011). Imprinted genes and the epigenetic regulation of placental phenotype. Progress in Biophysics and Molecular Biology, 106, 281–288. doi:10.1016/j.pbiomolbio.2010.11.005.

    Article  PubMed  Google Scholar 

  • Fowden, A. L., Forhead, A. J., Coan, P. M., & Burton, G. J. (2008). The placenta and intrauterine programming. Journal of Neuroendocrinology, 20, 439–450. doi:0.1111/j.1365-2826.2008.01663.x.

    Google Scholar 

  • Gartstein, M. A., & Rothbart, M. K. (2003). Studying infant temperament via the Revised Infant Behavior Questionnaire. Infant Behavior and Development, 26, 64–86. doi:10.1016/S0163-6383(02)00169-8.

    Article  Google Scholar 

  • Gluckman, P. D., & Hanson, M. A. (2004a). Developmental origins of disease paradigm: A mechanistic and evolutionary perspective. Pediatric Research, 56, 311–317. doi:10.1203/01.PDR.0000135998.08025.FB.

    Article  PubMed  Google Scholar 

  • Gluckman, P. D., & Hanson, M. A. (2004b). Living with the past: Evolution, development, and patterns of disease. Science, 305, 1733–1736. doi:10.1126/science.1095292.

    Article  PubMed  Google Scholar 

  • Gluckman, P. D., Hanson, M. A., & Spencer, H. G. (2005). Predictive adaptive responses and human evolution. Trends in Ecology & Evolution, 20, 527–533. doi:10.1016/j.tree.2005.08.001.

    Article  Google Scholar 

  • Glynn, L. M., Dunkel-Schetter, C., Chicz-DeMet, A., Hobel, C. J., & Sandman, C. A. (2007). Ethnic differences in adrenocorticotropic hormone, cortisol and corticotropin-releasing hormone during pregnancy. Peptides, 28, 1155–1161. doi:10.1016/j.peptides.2007.04.005.

    Article  PubMed  Google Scholar 

  • Glynn, L. M., Dunkel-Schetter, C., Hobel, C. J., & Sandman, C. A. (2008). Pattern of perceived stress and anxiety in pregnancy predicts preterm birth. Health Psychology, 27, 43–51. doi:10.1037/0278-6133.27.1.43.

    Article  PubMed  Google Scholar 

  • Glynn, L. M., Dunkel-Schetter, C., Wadhwa, P. D., & Sandman, C. A. (2004). Pregnancy affects appraisal of negative life events. Journal of Psychosomatic Research, 56, 47–52. doi:10.1016/S0022-3999(03)00133-8.

    Article  PubMed  Google Scholar 

  • Glynn, L. M., & Sandman, C. A. (2011). Prenatal origins of neurological development: A critical period for fetal and mother. Current Directions in Psychological Science, 20, 384–389. doi:10.1177/0963721411422056.

    Article  Google Scholar 

  • Glynn, L. M., & Sandman, C. A. (2012). Sex moderates associations between prenatal glucocorticoid exposure and human fetal neurological development. Developmental Science, 15, 601–610. doi:10.1111/j.1467-7687.2012.01159.x.

    Article  PubMed  Google Scholar 

  • Glynn, L. M., Wadhwa, P. D., Dunkel-Schetter, C., Chicz-DeMet, A., & Sandman, C. A. (2001). When stress happens matters: Effects of earthquake timing on stress responsivity in pregnancy. American Journal of Obstetrics and Gynecology, 184, 637–642. doi:10.1067/mob.2001.111066.

    Article  PubMed  Google Scholar 

  • Goland, R. S., Conwell, I. M., Warren, W. B., & Wardlaw, S. L. (1992). Placental corticotropin-releasing hormone and pituitary-adrenal function during pregnancy. Neuroendocrinology, 56(5), 742–749. doi:10.1159/000126302.

    Article  PubMed  Google Scholar 

  • Groome, L. J., Swiber, M. J., Holland, S. B., Bentz, L. S., Atterbury, J. L., & Trimm, R. F. (1999). Spontaneous motor activity in the perinatal infant before and after birth: Stability in individual differences. Developmental Psychobiology, 35, 15–24. doi:10.1002/(SICI)1098-2302(199907)35:1<15::AID-DEV3>3.0.CO;2-U.

    Article  PubMed  Google Scholar 

  • Haig, D. (1993). Genetic conflicts in human pregnancy. Quarterly Review of Biology, 68, 495–532.

    Google Scholar 

  • Hall, J. G. (2007). The importance of the fetal origins of adult disease for geneticists. Clinical Genetics, 72, 67–73. doi:10.1111/j.1399-0004.2007.00842.x.

    Article  PubMed  Google Scholar 

  • Hellemans, K. G., Sliwowska, J., Verma, P., & Weinberg, J. (2010). Prenatal alcohol exposure: Fetal programming and later life vulnerability to stress, depression and anxiety disorders. Neuroscience and Biobehavioral Reviews, 34, 791–807. doi:10.1016/j.neubiorev.2009.06.004.

    Article  PubMed  Google Scholar 

  • Hepper, P. G. (1995). The behavior of the fetus as an indicator of neural functioning. In J. Lecanuet, W. Fifer, N. Krasnegor, & W. Smotherman (Eds.), Fetal development: A psychobiological perspective (pp. 405–417). Hillsdale, MI: Lawrence Erlbaum Associates.

    Google Scholar 

  • Herman, J. P., & Cullinan, W. E. (1997). Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends in Neurosciences, 20, 78–84. doi:10.1016/S0166-2236(96)10069-2.

    Article  PubMed  Google Scholar 

  • Hilmert, C. J., Dunkel-Schetter, C., Dominguez, T. P., Abdou, C., Hobel, C. J., Glynn, L., & Sandman, C. (2008). Stress and blood pressure during pregnancy: racial differences and associations with birthweight. Psychosomatic Medicine, 70, 57–64. doi:10.1097/PSY.0b013e31815c6d96.

    Google Scholar 

  • Ho, J. T., Lewis, J. G., O'Loughlin, P., Bagley, C. J., Romero, R., Dekker, G. A., & Torpy, D. J. (2007). Reduced maternal corticosteroid-binding globulin and cortisol levels in pre-eclampsia and gamete recipient pregnancies. Clinical Endocrinology, 66, 869–877. doi:10.1111/j.1365-2265.2007.02826.x.

    Google Scholar 

  • Hobel, C. J. (2004). Stress and preterm birth. Clinical Obstetrics and Gynecology, 47(4), 856–880.

    Article  PubMed  Google Scholar 

  • Hobel, C. J., Arora, C. P., & Korst, L. M. (1999). Corticotrophin-releasing hormone and CRH-binding protein. Differences between patients at risk for preterm birth and hypertension. Annals of the New York Academy of Sciences, 897, 54–65. doi:10.1111/j.1749-6632.1999.tb07878.x.

    Article  PubMed  Google Scholar 

  • Hogue, C. J., Hoffman, S., & Hatch, M. C. (2001). Stress and preterm birth: A conceptual framework. Paediatric and Perinatal Epidemiology journal, 15, 30–40. doi:10.1046/j.1365-3016.2001.00006.x.

    Article  Google Scholar 

  • Holzman, C., Jetton, J., Siler-Khodr, T., Fisher, R., & Rip, T. (2001). Second trimester corticotropin-releasing hormone levels in relation to preterm delivery and ethnicity. Obstetrics and Gynecology, 97(5), 657–663.

    PubMed  Google Scholar 

  • Huizink, A. C., Dick, D. M., Sihvola, E., Pulkkinen, L., Rose, R. J., & Kaprio, J. (2007). Chernobyl exposure as stressor during pregnancy and behaviour in adolescent offspring. Acta Psychiatrica Scandinavica, 116, 438–446. doi:10.1111/j.1600-0447.2007.01050.x.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hunt, P. A., & Hassold, T. J. (2002). Sex matters in meiosis. Science, 296, 2181–2183. doi:10.1126/science.1071907.

    Article  PubMed  Google Scholar 

  • Huttenlocher, P. R., & Dabholkar, A. S. (1997). Regional differences in synaptogenesis in human cerebral cortex. Journal of Comparative Neurology, 387, 167–178. doi:10.1002/(SICI)1096-9861(19971020)387:2<167::AID-CNE1>3.0.CO;2-Z.

    Article  PubMed  Google Scholar 

  • Huttenlocher, P. R., de Courten, C., Garey, L. J., & Van der Loos, H. (1982). Synaptogenesis in human visual cortex--evidence for synapse elimination during normal development. Neuroscience Letters, 33, 247–252. doi:10.1016/0304-3940(82)90379-2.

    Article  PubMed  Google Scholar 

  • 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. Behavior Genetics, 31, 209–217. doi:10.1023/A:1010257512183.

    Google Scholar 

  • Joels, M., & Baram, T. Z. (2009). The neuro-symphony of stress. Nature Reviews Neuroscience, 10, 459–466. doi:10.1038/nrn2632.

    PubMed  PubMed Central  Google Scholar 

  • Kagan, J., Snidman, N., & Arcus, D. (1998). Childhood derivatives of high and low reactivity in infancy. Child Development, 69, 1483–1493. doi:10.1111/j.1467-8624.1998.tb06171.x.

    Article  PubMed  Google Scholar 

  • Kane, H. S., Dunkel-Schetter, C., Glynn, L. M., Hobel, C. J., & Sandman, C. A. (2014). Pregnancy anxiety and prenatal cortisol trajectories. Biological Psychology, 100, 13–19. doi:10.1016/j.biopsycho.2014.04.003.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kaplan, J., & Land, S. (2005). Influence of maternal-fetal histocompatibility and MHC zygosity on maternal microchimerism. Journal of Immunology, 174, 7123–7128. doi:10.4049/jimmunol.174.11.7123.

    Article  Google Scholar 

  • Kapoor, A., Dunn, E., Kostaki, A., Andrews, M. H., & Matthews, S. G. (2006). Fetal programming of the hypothalamic-pituitary-adrenal function: Prenatal stress and glucocorticoids. Journal of Physiology, 572, 31–44. doi:10.1113/jphysiol.2006.105254.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kapoor, A., Petropoulos, S., & Matthews, S. G. (2008). Fetal programming of hypothalamic–pituitary–adrenal (HPA) axis function and behavior by synthetic glucocorticoids. Brain Research Reviews, 57, 586–595. doi:10.1016/j.brainresrev.2007.06.013.

    Article  PubMed  Google Scholar 

  • Kim, D. J., Davis, E. P., Sandman, C. A., Sporns, O., O'Donnell, B. F., Buss, C., & Hetrick, W. P. (2014). Longer gestation is associated with more efficient brain networks in preadolescent children. Neuroimage, 100C, 619–627. doi:10.1016/j.neuroimage.2014.06.048.

    Google Scholar 

  • King, S., & Laplante, D. P. (2005). The effects of prenatal maternal stress on children's cognitive development: Project ice storm. Stress, 8, 35–45. doi:10.1080/10253890500108391.

    Article  PubMed  Google Scholar 

  • Kisilevsky, B. S., Fearon, I., & Muir, D. W. (1998). Fetuses differentiate vibroacoustic stimuli. Infant Behavior and Development, 21, 25–46.

    Article  Google Scholar 

  • Kisilevsky, B. S., & Muir, D. W. (1991). Human fetal and subsequent newborn responses to sound and vibration. Infant Behavior and Development, 14, 1–26. doi:10.1016/0163-6383(91)90051-S.

    Article  Google Scholar 

  • Korhonen, M., Luoma, I., Salmelin, R., & Tamminen, T. (2012). A longitudinal study of maternal prenatal, postnatal and concurrent depressive symptoms and adolescent well-being. Journal of Affective Disorders, 136, 680–692. doi:10.1016/j.jad.2011.10.007.

    Article  PubMed  Google Scholar 

  • Kostovic, I., Judas, M., Rados, M., & Hrabac, P. (2002). Laminar organization of the human fetal cerebrum revealed by histochemical markers and magnetic resonance imaging. Cerebral Cortex, 12, 536–544. doi:10.1093/cercor/12.5.536.

    Article  PubMed  Google Scholar 

  • Kramer, M. S., Goulet, L., Lydon, J., Seguin, L., & McNamara, H. (2001). Socio-economic disparities in preterm birth: Causal pathways and mechanisms. Paediatric and Perinatal Epidemiology journal, 15, 104–123. doi:10.1046/j.1365-3016.2001.00012.x.

    Article  Google Scholar 

  • Kurstjens, S., & Wolke, D. (2001). Effects of maternal depression on cognitive development of children over the first 7 years of life. Journal of Child Psychology and Psychiatry, 42, 623–636. doi:10.1017/S0021963001007296.

    Article  PubMed  Google Scholar 

  • Laatikainen, T., Virtanen, T., Kaaja, R., & Salminen-Lappalainen, K. (1991). Corticotropin-releasing hormone in maternal and cord plasma in pre-eclampsia. European Journal of Obstetrics, Gynecology, and Reproductive Biology, 39, 19–24. doi:10.1016/0028-2243(91)90136-9.

    Article  PubMed  Google Scholar 

  • Lange, C., & Irle, E. (2004). Enlarged amygdala volume and reduced hippocampal volume in young women with major depression. Psychological Medicine, 34, 1059–1064. doi:10.1017/S0033291703001806.

    Article  PubMed  Google Scholar 

  • Laplante, D. P., Barr, R. G., Brunet, A., Du Fort, G. G., Meaney, M. L., Saucier, J., …, King, S. (2004). Stress during pregnancy affects general intellectual and language functioning in human toddlers. Pediatric Research, 56, 400–410. doi:10.1203/01.PDR.0000136281.34035.44.

    Google Scholar 

  • Laplante, D. P., 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. Journal of the American Academy of Child and Adolescent Psychiatry, 47, 1063–1072. doi:10.1097/CHI.0b013e31817eec80.

    Article  PubMed  Google Scholar 

  • Lazarus, R. S. (1966). Psychological stress and the coping process. Ann Arbor, MI: McGraw-Hill.

    Google Scholar 

  • Lazarus, R. S. (1968). Emotions and adaptation: Conceptual and empirical relations. Nebraska Symposium on Motivation, 16, 175–266.

    Google Scholar 

  • Lazarus, R. S., & Folkman, S. (1984). Stress, appraisal, and coping. New York, NY: Springer Publishing Company.

    Google Scholar 

  • Leader, L. R., Baillie, P., Martin, B., & Vermeulen, E. (1982). The assessment and significance of habituation to a repeated stimulus by the human fetus. Early Human Development, 7, 211–219. doi:10.1016/0378-3782(82)90084-6.

    Article  PubMed  Google Scholar 

  • Levitt, P. (2003). Structural and functional maturation of the developing primate brain. Journal of Pediatrics, 143, S35–S45. doi:10.1067/S0022-3476(03)00400-1.

    Article  PubMed  Google Scholar 

  • Lewis, G., Rice, F., Harold, G. T., Collishaw, S., & Thapar, A. (2011). Investigating environmental links between parent depression and child depressive/anxiety symptoms using an assisted conception design. Journal of the American Academy of Child and Adolescent Psychiatry, 50, 451–459.e1. doi:10.1016/j.jaac.2011.01.015.

    Google Scholar 

  • Li, J., Olsen, J., Vestergaard, M., Obel, C., Baker, J. L., & Sorensen, T. I. (2010). Prenatal stress exposure related to maternal bereavement and risk of childhood overweight. PLoS One, 5, e11896. doi:10.1371/journal.pone.0011896.

    Article  PubMed  PubMed Central  Google Scholar 

  • Linton, E. A., Perkins, A. V., Woods, R. J., Eben, F., Wolfe, C. D., Behan, D. P., …, Lowry, P. J. (1993). Corticotropin releasing hormone-binding protein (CRH-BP): Plasma levels decrease during the third trimester of normal human pregnancy. The Journal of Clinical Endocrinology and Metabolism, 76(1), 260–262. doi:10.1210/jcem.76.1.8421097.

    Google Scholar 

  • Lobel, M. (1994). Conceptualizations, measurement, and effects of prenatal maternal stress on birth outcomes. Journal of Behavioral Medicine, 17, 225–272. doi:10.1007/BF01857952.

    Article  PubMed  Google Scholar 

  • Lu, M. C., & Halfon, N. (2003). Racial and ethnic disparities in birth outcomes: A life-course perspective. Maternal and Child Health Journal, 7, 13–30. doi:1092-7875/03/0300-0013/0

    Google Scholar 

  • Lupien, S. J., Parent, S., Evans, A. C., Tremblay, R. E., Zelazo, P. D., Corbo, V., …, Séguin, J. R. (2011). Larger amygdala but no change in hippocampal volume in 10-year-old children exposed to maternal depressive symptomatology since birth. Proceedings of the National Academy of Sciences, 108, 14324–14329. doi:10.1073/pnas.1105371108.

    Google Scholar 

  • Lyons, D. M., & Parker, K. J. (2007). Stress inoculation-induced indications of resilience in monkeys. Trauma Stress, 20(4), 423–433. doi:10.1002/jts.20265.

    Article  Google Scholar 

  • Ma, X. H., Wu, W. X., & Nathanielsz, P. W. (2003). Gestation-related and betamethasone-induced changes in 11beta-hydroxysteroid dehydrogenase types 1 and 2 in the baboon placenta. American Journal of Obstetrics and Gynecology, 188, 13–21. doi:10.1067/mob.2003.62.

    Article  PubMed  Google Scholar 

  • Mairesse, J., Lesage, J., Breton, C., Breant, B., Hahn, T., Darnaudery, M., …, Viltart, O. (2007). Maternal stress alters endocrine function of the feto-placental unit in rats. American journal of physiology. Endocrinology and Metabolism, 292, E1526–E1533. doi:10.1152/ajpendo.00574.2006.

    Google Scholar 

  • Mathews, T. J., & Hamilton, B. E. (2005). Trend analysis of the sex ratio at birth in the United States. National Vital Statistics Reports, 53(20), 1–17.

    Google Scholar 

  • McCool, W. F., Dorn, L. D., & Susman, E. J. (1994). The relation of cortisol reactivity and anxiety to perinatal outcome in primiparous adolescents. Research in Nursing and Health, 17, 411–420. doi:10.1002/nur.4770170604.

    Article  PubMed  Google Scholar 

  • McCormack, V. A., Dos Santos Silva, I., De Stavola, B. L., Mohsen, R., Leon, D. A., & Lithell, H. O. (2003). Fetal growth and subsequent risk of breast cancer: Results from long term follow up of Swedish cohort. British Medical Journal, 326, 248. doi:10.1136/bmj.326.7383.248.

    Article  PubMed  PubMed Central  Google Scholar 

  • McEwen, B. S. (1998). Protective and damaging effects of stress mediators. New England Journal of Medicine, 338, 171–179. doi:10.1056/NEJM199801153380307.

    Article  PubMed  Google Scholar 

  • McGrath, S., McLean, M., Smith, D., Bisito, A., Giles, W., & Smith, R. (2002). Maternal plasma coricotropin-releasing hormone trajectories vary depending on the etiology of preterm birth. American Journal of Obstetrics and Gynecology, 186, 257–260. doi:10.1067/mob.2002.119635.

    Article  PubMed  Google Scholar 

  • McLean, M., Bisits, A., Davies, J., Woods, R., Lowry, P., & Smith, R. (1995). A placental clock controlling the length of human pregnancy. Nature Medicine, 1, 460–463. doi:10.1038/nm0595-460.

    Article  PubMed  Google Scholar 

  • McLean, M., & Smith, R. (2001). Corticotrophin-releasing hormone and human parturition. Reproduction, 121, 493–501. doi:10.1530/rep.0.1210493.

    Article  PubMed  Google Scholar 

  • Mehta, M. A., Golembo, N. I., Nosarti, C., Colvert, E., Mota, A., Williams, S. C., …, Sonuga-Barke, E. J. (2009). Amygdala, hippocampal and corpus callosum size following severe early institutional deprivation: The English and Romanian adoptees study pilot. Journal of Child Psychology and Psychiatry, 50, 943–951. doi:10.1111/j.1469-7610.2009.02084.x.

    Google Scholar 

  • Melnick, M., Myrianthopoulos, N. C., & Christian, J. C. (1978). The effects of chorion type on variation in IQ in the NCPP twin population. American Journal of Human Genetics, 30(4), 425–433.

    PubMed  PubMed Central  Google Scholar 

  • Misra, D. P., Guyer, B., & Allston, A. (2003). Integrated perinatal health framework: A multiple determinants model with a life span approach. American Journal of Preventive Medicine, 25, 65–75. doi:10.1016/S0749-3797(03)00090-4.

    Article  PubMed  Google Scholar 

  • Moehler, E., Kagan, J., Parzer, P., Brunner, R., Reck, C., Wiebel, A., …, Resch, F. (2007). Childhood behavioral inhibition and maternal symptoms of depression. Psychopathology, 40, 446–452. doi:10.1159/000107429.

    Google Scholar 

  • Moldow, R. L., Kastin, A. J., Hollander, C. S., Coy, D. H., & Sandman, C. A. (1981). Brain beta-endorphin-like immunoreactivity in adult rats given beta-endorphin neonatally. Brain Research Bulletin, 7, 683–686. doi:10.1016/0361-9230(81)90118-0.

    Article  PubMed  Google Scholar 

  • Mueller, B. R., & Bale, T. L. (2008). Sex-specific programming of offspring emotionality after stress early in pregnancy. Journal of Neuroscience, 28, 9055–9065. doi:10.1523/JNEUROSCI.1424-08.2008.

    Article  PubMed  PubMed Central  Google Scholar 

  • Murphy, V. E., & Clifton, V. L. (2003). Alterations in human placental 11beta-hydroxysteroid dehydrogenase type 1 and 2 with gestational age and labour. Placenta, 24, 739–744. doi:10.1016/S0143-4004(03)00103-6.

    Article  PubMed  Google Scholar 

  • O’Connor, T. G., Bergman, K., Sarkar, P., & Glover, V. (2013). Prenatal cortisol exposure predicts infant cortisol response to acute stress. Developmental Psychobiology, 55, 145–155. doi:10.1002/dev.21007.

    Article  PubMed  PubMed Central  Google Scholar 

  • O’Connor, T. G., Heron, J., Golding, J., & Glover, V. (2003). Maternal antenatal anxiety and behavioural/emotional problems in children: A test of a programming hypothesis. Journal of Child Psychology and Psychiatry, 44, 1025–1036. doi:10.1111/1469-7610.00187.

    Article  PubMed  Google Scholar 

  • Orth, D. N., & Mount, C. D. (1987). Specific high-affinity binding protein for human corticotropin-releasing hormone in normal human plasma. Biochemical and Biophysical Research Communications, 143, 411–417. doi:10.1016/0006-291X(87)91369-6.

    Article  PubMed  Google Scholar 

  • Paarlberg, K. M., Vingerhoets, A. J., Passchier, J., Dekker, G. A., & Van Geijn, H. P. (1995). Psychosocial factors and pregnancy outcome: a review with emphasis on methodological issues. Journal of Psychosomatic Research, 39, 563–595. doi:10.1016/0022-3999(95)00018-6.

    Article  PubMed  Google Scholar 

  • Peacock, J. L., Marston, L., Marlow, N., Calvert, S. A., & Greenough, A. (2012). Neonatal and infant outcome in boys and girls born very prematurely. Pediatric Research, 71, 305–310. doi:10.1038/pr.2011.50.

    Article  PubMed  Google Scholar 

  • Peterson, B. S., Warner, V., Bansal, R., Zhu, H., Hao, X., Liu, J., …, Weissman, M. M. (2009). Cortical thinning in persons at increased familial risk for major depression. Proceedings of the National Academy of Sciences, 106, 6273–6278. doi:10.1073/pnas.0805311106.

    Google Scholar 

  • Peterson, B. S., & Weissman, M. M. (2011). A brain-based endophenotype for major depressive disorder. Annual Review of Medicine, 62, 461–474. doi:10.1146/annurev-med-010510-095632.

    Article  PubMed  PubMed Central  Google Scholar 

  • Petraglia, F., Florio, P., Nappi, C., & Genazzani, A. R. (1996). Peptide signaling in human placenta and membranes: Autocrine, paracrine, and endocrine mechanisms. Endocrine Reviews, 17, 156–186. doi:10.1210/edrv-17-2-156.

    PubMed  Google Scholar 

  • Petraglia, F., Hatch, M. C., Lapinski, R., Stomati, M., Reis, F. M., Cobellis, L., & Berkowitz, G. S. (2001). Lack of effect of psychosocial stress on maternal corticotropin-releasing factor and catecholamine levels at 28 weeks' gestation. Journal of the Society for Gynecologic Investigation, 8, 83–88. doi:10.1177/107155760100800204.

    Google Scholar 

  • Petraglia, F., Potter, E., Cameron, V. A., Sutton, S., Behan, D. P., Woods, R. J., …, Vale, W. (1993). Corticotropin-releasing factor-binding protein is produced by human placenta and intrauterine tissues. Journal of Clinical Endocrinology and Metabolism, 77, 919–924. doi:10.1210/jcem.77.4.8408466.

    Google Scholar 

  • Petraglia, F., Sutton, S., & Vale, W. (1989). Neurotransmitters and peptides modulate the release of immunoreactive corticotropin-releasing factor from cultured human placental cells. American Journal of Obstetrics and Gynecology, 160(1), 247–251. doi:10.1016/0002-9378(89)90130-0.

    Article  PubMed  Google Scholar 

  • Pfeifer, M., Goldsmith, H. H., Davidson, R. J., & Rickman, M. (2002). Continuity and change in inhibited and uninhibited children. Child Development, 73, 1474–1485. doi:10.1111/1467-8624.00484.

    Article  PubMed  Google Scholar 

  • Rice, F., Harold, G. T., 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(02), 335–345. doi:10.1017/S0033291709005911.

    Article  PubMed  PubMed Central  Google Scholar 

  • Richards, M., Hardy, R., Kuh, D., & Wadsworth, M. E. J. (2001). Birth weight and cognitive function in the British 1946 birth cohort: Longitudinal population based study. British Medical Journal, 322, 199–203. doi:10.1136/bmj.322.7280.199.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rini, C. K., Dunkel-Schetter, C., Wadhwa, P. D., & Sandman, C. A. (1999). Psychological adaptation and birth outcomes: The role of personal resources, stress, and sociocultural context in pregnancy. Health Psychology, 18, 333–345. doi:10.1037/0278-6133.18.4.333.

    Article  PubMed  Google Scholar 

  • Rodrigues, S. M., LeDoux, J. E., & Sapolsky, R. M. (2009). The influence of stress hormones on fear circuitry. Annual Review of Neuroscience, 32, 289–313. doi:10.1146/annurev.neuro.051508.135620.

    Article  PubMed  Google Scholar 

  • Roseboom, T. J., van der Meulen, J. H., Osmond, C., Barker, D. J., Ravelli, A. C., Schroeder-Tanka, J. M., …, Bleker, O. P. (2000). Coronary heart disease after prenatal exposure to the Dutch famine, 1944–45. Heart, 84, 595–598. doi:10.1136/heart.84.6.595.

    Google Scholar 

  • Rosenblatt, M. I., & Dickerson, I. M. (1997). Endoproteolysis at tetrabasic amino acid sites in procalcitonin gene-related peptide by pituitary cell lines. Peptides, 18, 567–576. doi:10.1016/S0196-9781(97)00055-7.

    Article  PubMed  Google Scholar 

  • Salm, A. K., Pavelko, M., Krouse, E. M., Webster, W., Kraszpulski, M., & Birkle, D. L. (2004). Lateral amygdaloid nucleus expansion in adult rats is associated with exposure to prenatal stress. Brain Research. Developmental Brain Research, 148, 159–167. doi:10.1016/j.devbrainres.2003.11.005.

    Article  PubMed  Google Scholar 

  • Sandman, C. A. (2010). Human fetal heart rate: A unique opportunity to assess the fetal programming hypothesis. Infant and Child Development, 19, 76–79. doi:10.1002/icd.656.

    Article  Google Scholar 

  • Sandman, CA, Buss, C, Head, K, & Davis, EP. Fetal exposure to maternal depressive symptoms is associated with cortical thickness in late childhood. Biological Psychiatry, 2015, 77, 234-334 NIHMS613398.

    Google Scholar 

  • Sandman, C. A., Cordova, C. J., Davis, E. P., Glynn, L. M., & Buss, C. (2011). Patterns of fetal heart rate response at approximately 30 weeks gestation predict size at birth. Journal of Developmental Origins of Health and Disease, 2, 212–217. doi:10.1017/S2040174411000250.

    Article  PubMed  Google Scholar 

  • Sandman, C. A., & Davis, E. P. (2010). Gestational stress influences cognition and behavior. Future Neurology, 5, 675–690. doi:10.2217/fnl.10.35.

    Article  Google Scholar 

  • Sandman, C. A., & Davis, E. P. (2012). Neurobehavioral risk is associated with gestational exposure to stress hormones. Expert Review of Endocrinology and Metabolism, 7, 445–459. doi:10.1586/eem.12.33.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sandman, C. A., Davis, E. P., Buss, C., & Glynn, L. M. (2011a). Exposure to prenatal psychobiological stress exerts programming influences on the mother and her fetus. Neuroendocrinology, 95, 7–21. doi:10.1159/000327017.

    PubMed  Google Scholar 

  • Sandman, C. A., Davis, E. P., Buss, C., & Glynn, L. M. (2011b). Prenatal programming of human neurological function. International Journal of Peptides, 2011, 1–9. doi:10.1155/2011/837596.

    Article  Google Scholar 

  • Sandman, C. A., Davis, E. P., & Glynn, L. M. (2012a). Psychobiological stress and preterm birth. In J. Morrison (Ed.), Preterm birth – Mother and child (pp. 95–124). doi:10.5772/27539

    Google Scholar 

  • Sandman, C. A., Davis, E. P., & Glynn, L. M. (2012b). Prescient human fetuses thrive. Psychological Science, 23, 93–100. doi:10.1177/0956797611422073.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sandman, C. A., Glynn, L., Dunkel-Schetter, C., Wadhwa, P., Garite, T., Chicz-DeMet, A., & Hobel, C. (2006). Elevated maternal cortisol early in pregnancy predicts third trimester levels of placental corticotropin releasing hormone (CRH): Priming the placental clock. Peptides, 27, 1457–1463. doi:10.1016/j.peptides.2005.10.002.

    Google Scholar 

  • Sandman, C. A., Glynn, L., Wadhwa, P. D., Chicz-DeMet, A., Porto, M., & Garite, T. (2003). Maternal hypothalamic-pituitary-adrenal disregulation during the third trimester influences human fetal responses. Developmental Neuroscience, 25, 41–49. doi:10.1159/000071467.

    Article  PubMed  Google Scholar 

  • Sandman, C. A., Glynn, L. M., & Davis, E. P. (2013). Is there a viability-vulnerability tradeoff? Sex differences in fetal programming. Journal of Psychosomatic Research, 75, 327–335. doi:10.1016/j.jpsychores.2013.07.009.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sandman, C. A., & Kastin, A. J. (1981). Intraventricular administration of MSH induces hyperalgesia in rats. Peptides, 2, 231–233. doi:10.1016/S0196-9781(81)80040-X.

    Article  PubMed  Google Scholar 

  • Sandman, C. A., & O'Halloran, J. P. (1986). Pro-opiomelanocortin, learning, memory and attention. In D. DeWied, W. Gispen, & T. van Wimersma-Greidanus (Eds.), Neuropeptides and behavior: CNS effects of ACTH, MSH and opiod peptides (Vol. 1, pp. 397–420). Oxford: Pergamon Press.

    Google Scholar 

  • Sandman, C. A., Wadhwa, P. D., Chicz-DeMet, A., Porto, M., & Garite, T. J. (1999). Maternal corticotropin-releasing hormone and habituation in the human fetus. Developmental Psychobiology, 34, 163–173. doi:10.1002/(SICI)1098-2302(199904)34:3<163::AID-DEV1>3.0.CO;2-9.

    Article  PubMed  Google Scholar 

  • Sandman, C. A., Wadhwa, P. D., Hetrick, W., Porto, M., & Peeke, H. V. (1997). Human fetal heart rate dishabituation between thirty and thirty-two weeks gestation. Child Development, 68, 1031–1040. doi:10.2307/1132289.

    Article  PubMed  Google Scholar 

  • Sandman, C. A., & Yessaian, N. (1986). Persisting subsensitivity of the striatal dopamine system after fetal exposure to beta-endorphin. Life Sciences, 39, 1755–1763. doi:10.1016/0024-3205(86)90095-0.

    Article  PubMed  Google Scholar 

  • Sasaki, A., Shinkawa, O., Margioris, A. N., Liotta, A. S., Sato, S., Murakami, O., …, Yoshinaga, K. (1987). Immunoreactive corticotropin-releasing hormone in human plasma during pregnancy, labor, and delivery. Journal of Clinical Endocrinology Metabolism, 64, 224–229. doi:10.1210/jcem-64-2-224.

    Google Scholar 

  • Sasaki, A., Tempst, P., Liotta, A. S., Margioris, A. N., Hood, L. E., Kent, S. B., …, Krieger, D. T. (1988). Isolation and characterization of a corticotropin-releasing hormone-like peptide from human placenta. Journal of Clinical Endocrinology Metabolism, 67, 768–773. doi:10.1210/jcem-67-4-768.

    Google Scholar 

  • Schulkin, J. (2006). Angst and the amygdala. Dialogues in Clinical Neuroscience, 8(4), 407–416.

    PubMed  PubMed Central  Google Scholar 

  • Schwartz, C. E., Snidman, N., & Kagan, J. (1999). Adolescent social anxiety as an outcome of inhibited temperament in childhood. Journal of the American Academy of Child and Adolescent Psychiatry, 38, 1008–1015. doi:10.1097/00004583-199908000-00017.

    Article  PubMed  Google Scholar 

  • Seckl, J. R., & Meaney, M. J. (2006). Glucocorticoid "programming" and PTSD risk. Annals of the New York Academy of Sciences, 1071, 351–378. doi:10.1196/annals.1364.027.

    Article  PubMed  Google Scholar 

  • Selye, H. (1936). A syndrome produced by diverse nocuous agents. Nature, 138, 32. doi:10.1038/138032a0.

    Article  Google Scholar 

  • Selye, H. (1955). Stress and disease. The Laryngoscope, 65, 500–514. doi:10.1288/00005537-195507000-00002.

    Article  PubMed  Google Scholar 

  • Selye, H. (1956). The stress of life. New York, NY: McGraw-Hill.

    Google Scholar 

  • Selye, H. (1959). Perspectives in stress research. Perspectives in Biology and Medicine, 2, 403–416.

    Article  PubMed  Google Scholar 

  • Sheslow, D., & Adams, W. (2003). Wide range assessment of memory and learning administration and technical manual (2nd ed.). Lutz, FL: Psychological Assessment Resources.

    Google Scholar 

  • Sirianni, R., Rehman, K. S., Carr, B. R., Parker, C. R., & Rainey, W. E. (2005). Corticotropin-releasing hormone directly stimulates cortisol and the cortisol biosynthetic pathway in human fetal adrenal cells. Journal of Clinical Endocrinology and Metabolism, 90, 279–285. doi:10.1210/jc.2004-0865.

    Article  PubMed  Google Scholar 

  • Smith, R., Mesiano, S., & McGrath, S. (2002). Hormone trajectories leading to human birth. Regulatory Peptides, 108, 159–164. doi:0167-0115/02/$.

    Google Scholar 

  • Smith, R., & Nicholson, R. C. (2007). Corticotrophin releasing hormone and the timing of birth. Frontiers in Bioscience, 12, 912–918.

    Article  PubMed  Google Scholar 

  • Smith, R., Smith, J. I., Shen, X., Engel, P. J., Bowman, M. E., McGrath, S. A., …, Smith, D. W. (2009). Patterns of plasma corticotropin-releasing hormone, progesterone, estradiol, and estriol change and the onset of human labor. Journal of Clinical Endocrinology Metabolism, 94, 2066–2074. doi:10.1210/jc.2008-2257.

    Google Scholar 

  • Sokol, D. K., Moore, C. A., Rose, R. J., Williams, C. J., Reed, T., & Christian, J. C. (1995). Intrapair differences in personality and cognitive ability among young monozygotic twins distinguished by chorion type. Behavior Genetics, 25, 457–466. doi:10.1007/BF02253374.

    Article  PubMed  Google Scholar 

  • Spong, C. Y. (2013). Defining "term" pregnancy: Recommendations from the Defining "Term" Pregnancy Workgroup. JAMA, 309, 2445–2446. doi:10.1001/jama.2013.6235.

    Article  PubMed  Google Scholar 

  • Stiles, J., & Jernigan, T. L. (2010). The basics of brain development. Neuropsychology Review, 20, 327–348. doi:10.1007/s11065-010-9148-4.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sun, K., Adamson, S. L., Yang, K., & Challis, J. R. (1999). Interconversion of cortisol and cortisone by 11beta-hydroxysteroid dehydrogenases type 1 and 2 in the perfused human placenta. Placenta, 20, 13–19. doi:10.1053/plac.1998.0352.

    Article  PubMed  Google Scholar 

  • Tottenham, N., Hare, T. A., Quinn, B. T., McCarry, T. W., Nurse, M., Gilhooly, T., …, Casey, B. J. (2010). Prolonged institutional rearing is associated with atypically large amygdala volume and difficulties in emotion regulation. Developmental Science, 13, 46–61. doi:10.1111/j.1467-7687.2009.00852.x.

    Google Scholar 

  • Tu, P. C., Chen, L. F., Hsieh, J. C., Bai, Y. M., Li, C. T., & Su, T. P. (2012). Regional cortical thinning in patients with major depressive disorder: A surface-based morphometry study. Psychiatry Research: Neuroimaging, 20, 206–213. doi:10.1016/j.pscychresns.2011.07.011.

    Article  Google Scholar 

  • Tyson, E. K., Smith, R., & Read, M. (2009). Evidence that corticotropin-releasing hormone modulates myometrial contractility during human pregnancy. Endocrinology, 150, 5617–5625. doi:10.1210/en.2009-0348.

    Article  PubMed  Google Scholar 

  • Vale, W., Spiess, J., Rivier, C., & Rivier, J. (1981). Characterization of a 41-residue ovine hypothalamic peptide that stimulates secretion of corticotropin and beta-endorphin. Science, 213, 1394–1397. doi:10.1126/science.6267699.

    Article  PubMed  Google Scholar 

  • Van den Bergh, B. (1990). The influence of maternal emotion during pregnancy on fetal and neonatal behavior. Prenatal and Perinatal Psychology, 5(2), 119–130.

    Google Scholar 

  • Van den Bergh, B. R., & Marcoen, A. (2004). High antenatal maternal anxiety is related to ADHD symptoms, externalizing problems, and anxiety in 8- and 9-year-olds. Child Development, 75, 1085–1097. doi:10.1111/j.1467-8624.2004.00727.x.

    Article  PubMed  Google Scholar 

  • Van den Bergh, B. R., 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. doi:10.1038/sj.npp.1301450.

    Article  PubMed  Google Scholar 

  • Vlastos, E. J., Tomlinson, T. M., Bildirici, I., Sreenarasimhaiah, S., Yusuf, K., Sadovsky, Y., & Levy, R. (2007). Fetal heart rate accelerations and the risk of cerebral lesions and poor neurodevelopmental outcome in very low birthweight neonates. American Journal of Perinatology, 24, 83–88. doi:10.1055/s-2006-958161.

    Google Scholar 

  • Wadhwa, P. D., Garite, T. J., Porto, M., Glynn, L., Chicz-DeMet, A., Dunkel-Schetter, C., & Sandman, C. A. (2004). Placental corticotropin-releasing hormone (CRH), spontaneous preterm birth, and fetal growth restriction: A prospective investigation. American Journal of Obstetrics and Gynecology, 191, 1063–1069. doi:10.1016/j.ajog.2004.06.070.

    Google Scholar 

  • Wadhwa, P. D., Porto, M., Garite, T. J., Chicz-DeMet, A., & Sandman, C. A. (1998). Maternal corticotropin-releasing hormone levels in the early third trimester predict length of gestation in human pregnancy. American Journal of Obstetrics and Gynecology, 179(4), 1079–1085. doi:10.1016/S0002-9378(98)70219-4.

    Article  PubMed  Google Scholar 

  • Wadhwa, P. D., Sandman, C. A., Porto, M., Dunkel-Schetter, C., & Garite, T. J. (1993). The association between prenatal stress and infant birth weight and gestational age at birth: A prospective investigation. American Journal of Obstetrics and Gynecology, 169, 858–865. doi:10.1016/0002-9378(93)90016-C.

    Article  PubMed  Google Scholar 

  • Walder, D. J., Laplante, D. P., Sousa-Pires, A., Veru, F., Brunet, A., & King, S. (2014). Prenatal maternal stress predicts autism traits in 6½ year-old children: Project Ice Storm. Psychiatry Research, 219, 353–360. doi:10.1016/j.psychres.2014.04.034.

    Article  PubMed  Google Scholar 

  • Wechsler, D. (2002). The Wechsler Preschool and Primary Scale of Intelligence (3rd ed.). San Antonio, TX: The Psychological Corporation.

    Google Scholar 

  • Wells, J. C. (2000). Natural selection and sex differences in morbidity and mortality in early life. Journal of Theoretical Biology, 202, 65–76. doi:10.1006/jtbi.1999.1044.

    Article  PubMed  Google Scholar 

  • Werner, E. A., Myers, M. M., Fifer, W. P., Cheng, B., Fang, Y., Allen, R., & Monk, C. (2007). Prenatal predictors of infant temperament. Developmental Psychobiology, 49, 474–484. doi:10.1002/dev.20232.

    Google Scholar 

  • Wolfe, C. D., Patel, S. P., Linton, E. A., Campbell, E. A., Anderson, J., Dornhorst, A., …, Jones, M. T. (1988). Plasma corticotrophin-releasing factor (CRF) in abnormal pregnancy. British Journal of Obstetrics and Gynaecology, 95, 1003–1006. doi:10.1111/j.1471-0528.1988.tb06504.x.

    Google Scholar 

  • Yim, I. S., Glynn, L. M., Dunkel-Schetter, C., Hobel, C. J., Chicz-DeMet, A., & Sandman, C. A. (2009). Risk of postpartum depressive symptoms with elevated corticotropin-releasing hormone in human pregnancy. Archives of General Psychiatry, 66, 162–169. doi:10.1001/archgenpsychiatry.2008.533.

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This research reported here was supported by National Institute of Health grants NS-41298, HD-51852, HD-28413 HD-40967, HD-50662, HD-65823 and Conte Center award MH-96889.

We are grateful for the expert contributions of Claudia Buss, PhD, Cheryl Crippen, PhD, Kevin Head, BA, Christina Canino-Brown, MA, Kendra Leak, BA, Quetzel Class, PhD, Megan (Blair) Faulkner, BA, Natalie Hernandez, BA, Mariann Howland BA, Amanda Appel, MPH, Christine Dunkel-Schetter, PhD, and Cal Hobel, MD. Our program of research would not be possible without the participation of the families. Special gratitude is expressed especially to the families (mothers and children) who have continued in our longitudinal studies.

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Sandman, C.A., Glynn, L.M., Davis, E.P. (2016). Neurobehavioral Consequences of Fetal Exposure to Gestational Stress. In: Reissland, N., Kisilevsky, B. (eds) Fetal Development. Springer, Cham. https://doi.org/10.1007/978-3-319-22023-9_13

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