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Prenatal Programming in the Fetus and Placenta

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Prenatal Stress and Child Development

Abstract

Individual differences in risk for neuropsychiatric disorders are shaped before the individual is born. In this chapter, we summarize existing evidence from animal and human studies describing prenatal programming in the fetus and placenta in response to prenatal maternal stress, and associated outcomes seen in offspring neurobehavioral development and risk for psychopathology. First, we review fetal neurobehavioral development and assessment, including fetal physiological monitoring and fetal neuroimaging. We then highlight extant research on associations between fetal neurobehavior and later outcomes. Emerging research also points to the involvement of the placenta, which regulates the prenatal environment. We continue by describing how maternal stress can disrupt the placenta’s fundamental functions, highlighting the role of nutrient transfer, placental barrier permeability, serotonin signaling, and epigenetic changes to placental genes. We close by discussing the importance of sex differences in fetal and placental programming as well as developmental timing of exposures, and future directions for research.

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References

  • Aguirre, V., Werner, E. D., Giraud, J., Lee, Y. H., Shoelson, S. E., & White, M. F. (2002). Phosphorylation of Ser307 in insulin receptor substrate-1 blocks interactions with the insulin receptor and inhibits insulin action. Journal of Biological Chemistry, 277(2), 1531–1537.

    Article  Google Scholar 

  • Allister, L., Lester, B. M., Carr, S., & Liu, J. (2001). The effects of maternal depression on fetal heart rate response to vibroacoustic stimulation. Developmental Neuropsychology, 20(3), 639–651.

    Article  Google Scholar 

  • Anderson, A. L., & Thomason, M. E. (2013). Functional plasticity before the cradle: A review of neural functional imaging in the human fetus. Neuroscience and Biobehavioral Reviews, 37(9) Pt B, 2220–2232.

    Article  Google Scholar 

  • Appleton, A. A., Armstrong, D. A., Lesseur, C., Lee, J., Padbury, J. F., Lester, B. M., & Marsit, C. J. (2013). Patterning in placental 11-B hydroxysteroid dehydrogenase methylation according to prenatal socioeconomic adversity. PLoS One, 8(9), e74691.

    Article  Google Scholar 

  • Arck, P. C., & Hecher, K. (2013). Fetomaternal immune cross-talk and its consequences for maternal and offspring’s health. Nature Medicine, 19(5), 548.

    Article  Google Scholar 

  • Ardissone, A. N., Diomel, M., Davis-Richardson, A. G., Rechcigl, K. T., Li, N., Drew, J. C., Murgas-Torrazza, R., Sharma, R., Hudak, M. L., & Triplett, E. W. (2014). Meconium microbiome analysis identifies bacteria correlated with premature birth. PLoS One, 9(3), e90784.

    Article  Google Scholar 

  • Bale, T. L. (2016). The placenta and neurodevelopment: Sex differences in prenatal vulnerability. Dialogues in Clinical Neuroscience, 18(4), 459–464.

    Article  Google Scholar 

  • Bao, X. R., Ong, S.-E., Goldberger, O., Peng, J., Sharma, R., Thompson, D. A., Vafai, S. B., Cox, A. G., Marutani, E., & Ichinose, F. (2016). Mitochondrial dysfunction remodels one-carbon metabolism in human cells. eLife, 5, e10575.

    Article  Google Scholar 

  • Barcroft, J. (1946). Researches on pre-natal life. Oxford: Blackwell Scientific Publications.

    Google Scholar 

  • Basilious, A., Yager, J., & Fehlings, M. G. (2015). Neurological outcomes of animal models of uterine artery ligation and relevance to human intrauterine growth restriction: A systematic review. Developmental Medicine and Child Neurology, 57(5), 420–430.

    Article  Google Scholar 

  • Baskin, R., Hill, B., Jacka, F. N., O’Neil, A., & Skouteris, H. (2015). The association between diet quality and mental health during the perinatal period. A systematic review. Appetite, 91, 41–47.

    Article  Google Scholar 

  • Beijers, R., Buitelaar, J. K., & de Weerth, C. (2014). Mechanisms underlying the effects of prenatal psychosocial stress on child outcomes: Beyond the HPA axis. European Child & Adolescent Psychiatry, 23(10), 943–956.

    Article  Google Scholar 

  • Belkacemi, L., Jelks, A., Chen, C.-H., Ross, M. G., & Desai, M. (2011). Altered placental development in undernourished rats: Role of maternal glucocorticoids. Reproductive Biology and Endocrinology, 9, 1): 1.

    Article  Google Scholar 

  • Benson, P., Little, B. C., Talbert, D. G., Dewhurst, S. J., & Priest, R. G. (1987). Foetal heart rate and maternal emotional state. British Journal of Medical Psychology, 60(2), 151–154.

    Article  Google Scholar 

  • Berger, M., Gray, J. A., & Roth, B. L. (2009). The expanded biology of serotonin. Annual Review of Medicine, 60, 355–366.

    Article  Google Scholar 

  • Bertram, C., Trowern, A., Copin, N., Jackson, A., & Whorwood, C. (2001). The maternal diet during pregnancy programs altered expression of the glucocorticoid receptor and type 2 11β-Hydroxysteroid dehydrogenase: Potential molecular mechanisms underlying the programming of hypertension in utero 1. Endocrinology, 142(7), 2841–2853.

    Article  Google Scholar 

  • Bilbo, S. D. (2011). How cytokines leave their mark: The role of the placenta in developmental programming of brain and behavior. Brain, Behavior, and Immunity, 25(4), 602–603.

    Article  Google Scholar 

  • Bilbo, S. D., Block, C. L., Bolton, J. L., Hanamsagar, R., & Tran, P. K. (2018). Beyond infection-maternal immune activation by environmental factors, microglial development, and relevance for autism spectrum disorders. Experimental Neurology, 299, 241–251.

    Article  Google Scholar 

  • Blakeley, P. M., Capron, L. E., Jensen, A. B., O’Donnell, K. J., & Glover, V. (2013). Maternal prenatal symptoms of depression and down regulation of placental monoamine oxidase a expression. Journal of Psychosomatic Research, 75(4), 341–345.

    Article  Google Scholar 

  • Bonnin, A., Goeden, N., Chen, K., Wilson, M. L., King, J., Shih, J. C., Blakely, R. D., Deneris, E. S., & Levitt, P. (2011). A transient placental source of serotonin for the fetal forebrain. Nature, 472(7343), 347.

    Article  Google Scholar 

  • Bornstein, M. H., DiPietro, J. A., Hahn, C.-S., Painter, K., Haynes, O. M., & Costigan, K. A. (2002). Prenatal cardiac function and postnatal cognitive development: An exploratory study. Infancy, 3(4), 475–494.

    Article  Google Scholar 

  • Brett, K., Ferraro, Z., Yockell-Lelievre, J., Gruslin, A., & Adamo, K. (2014). Maternal–fetal nutrient transport in pregnancy pathologies: The role of the placenta. International Journal of Molecular Sciences, 15(9), 16153–16185.

    Article  Google Scholar 

  • Bromer, C., Marsit, C. J., Armstrong, D. A., Padbury, J. F., & Lester, B. (2013). Genetic and epigenetic variation of the glucocorticoid receptor (NR3C1) in placenta and infant neurobehavior. Developmental Psychobiology, 55(7), 673–683.

    Google Scholar 

  • Bronson, S. L., & Bale, T. L. (2016). The placenta as a mediator of stress effects on neurodevelopmental reprogramming. Neuropsychopharmacology, 41(1), 207–218.

    Article  Google Scholar 

  • Bronson, S. L., Chan, J. C., & Bale, T. L. (2017). Sex-specific neurodevelopmental programming by placental insulin receptors on stress reactivity and sensorimotor gating. Biological Psychiatry, 82(2), 127–138.

    Article  Google Scholar 

  • Brown, R., Diaz, R., Robson, A., Kotelevtsev, Y., Mullins, J., Kaufman, M., & Seckl, J. (1996). The ontogeny of 11 beta-hydroxysteroid dehydrogenase type 2 and mineralocorticoid receptor gene expression reveal intricate control of glucocorticoid action in development. Endocrinology, 137(2), 794–797.

    Article  Google Scholar 

  • Brummelte, S., Mc Glanaghy, E., Bonnin, A., & Oberlander, T. (2017). Developmental changes in serotonin signaling: Implications for early brain function, behavior and adaptation. Neuroscience, 342, 212–231.

    Article  Google Scholar 

  • Brunst, K. J., Sanchez Guerra, M., Gennings, C., Hacker, M., Jara, C., Bosquet Enlow, M., Wright, R. O., Baccarelli, A., & Wright, R. J. (2017). Maternal lifetime stress and prenatal psychological functioning and decreased placental mitochondrial DNA copy number in the PRISM study. American Journal of Epidemiology, 186(11), 1227–1236.

    Article  Google Scholar 

  • Brunst, K. J., Sanchez-Guerra, M., Chiu, Y.-H. M., Wilson, A., Coull, B. A., Kloog, I., Schwartz, J., Brennan, K. J., Bosquet Enlow, M., Wright, R. O., Baccarelli, A. A., & Wright, R. J. (2018). Prenatal particulate matter exposure and mitochondrial dysfunction at the maternal-fetal interface: Effect modification by maternal lifetime trauma and child sex. Environment International, 112, 49–58.

    Article  Google Scholar 

  • Burchard, E. G., Oh, S. S., Foreman, M. G., & Celedon, J. C. (2015). Moving toward true inclusion of racial/ethnic minorities in federally funded studies. A key step for achieving respiratory health equality in the United States. American Journal of Respiratory and Critical Care Medicine, 191(5), 514–521.

    Article  Google Scholar 

  • Bushman, F. D. (2019). De-discovery of the placenta microbiome. American Journal of Obstetrics and Gynecology, 220(3), 213–214.

    Article  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(1), 141–153.

    Article  Google Scholar 

  • Canetta, S. E., & Brown, A. S. (2012). Prenatal infection, maternal immune activation, and risk for schizophrenia. Translational Neuroscience, 3(4), 320–327.

    Article  Google Scholar 

  • Careaga, M., Murai, T., & Bauman, M. D. (2017). Maternal immune activation and autism spectrum disorder: From rodents to nonhuman and human primates. Biological Psychiatry, 81(5), 391–401.

    Article  Google Scholar 

  • Clouchoux, C., Kudelski, D., Gholipour, A., Warfield, S. K., Viseur, S., Bouyssi-Kobar, M., Mari, J. L., Evans, A. C., du Plessis, A. J., & Limperopoulos, C. (2012). Quantitative in vivo MRI measurement of cortical development in the fetus. Brain Structure & Function, 217(1), 127–139.

    Article  Google Scholar 

  • Collado, M. C., Rautava, S., Aakko, J., Isolauri, E., & Salminen, S. (2016). Human gut colonisation may be initiated in utero by distinct microbial communities in the placenta and amniotic fluid. Scientific Reports, 6, 23129.

    Article  Google Scholar 

  • Conradt, E., Lester, B. M., Appleton, A. A., Armstrong, D. A., & Marsit, C. J. (2013). The roles of DNA methylation of NR3C1 and 11β-HSD2 and exposure to maternal mood disorder in utero on newborn neurobehavior. Epigenetics, 8(12), 1321–1329.

    Article  Google Scholar 

  • Copher, D. E., & Huber, C. P. (1967). Heart rate response of the human fetus to induced maternal hypoxia. American Journal of Obstetrics and Gynecology, 98(3), 320–335.

    Article  Google Scholar 

  • Cox, B., Kotlyar, M., Evangelou, A. I., Ignatchenko, V., Ignatchenko, A., Whiteley, K., Jurisica, I., Adamson, S. L., Rossant, J., & Kislinger, T. (2009). Comparative systems biology of human and mouse as a tool to guide the modeling of human placental pathology. Molecular Systems Biology, 5(1), 279.

    Article  Google Scholar 

  • Curran, M. M., Sandman, C. A., Davis, E. P., Glynn, L. M., & Baram, T. Z. (2017). Abnormal dendritic maturation of developing cortical neurons exposed to corticotropin releasing hormone (CRH): Insights into effects of prenatal adversity? PLoS One, 12(6), e0180311.

    Article  Google Scholar 

  • Dalton, K. J., Dawes, G. S., & Patrick, J. E. (1983). The autonomic nervous system and fetal heart rate variability. American Journal of Obstetrics and Gynecology, 146(4), 456–462.

    Article  Google Scholar 

  • de Goede, O. M., Lavoie, P. M., & Robinson, W. P. (2016). Characterizing the hypomethylated DNA methylation profile of nucleated red blood cells from cord blood. Epigenomics, 8(11), 1481–1494.

    Article  Google Scholar 

  • DeGangi, G. A., DiPietro, J. A., Greenspan, S. I., & Porges, S. W. (1991). Psychophysiological characteristics of the regulatory disordered infant. Infant Behavior and Development, 14, 37–50.

    Article  Google Scholar 

  • Deneris, E. S., & Wyler, S. C. (2012). Serotonergic transcriptional networks and potential importance to mental health. Nature Neuroscience, 15(4), 519.

    Article  Google Scholar 

  • Depino, A. M. (2017). Perinatal inflammation and adult psychopathology: From preclinical models to humans. Seminars in Cell & Developmental Biology, 77, 104–114.

    Article  Google Scholar 

  • Deroy, K., Côté, F., Fournier, T., Sanderson, T., & Vaillancourt, C. (2013). Serotonin production by human and mouse trophoblast: Involvement in placental development and function. Placenta, 34(9), A71.

    Article  Google Scholar 

  • Devarshi, P. P., Grant, R. W., Ikonte, C. J., & Hazels Mitmesser, S. (2019). Maternal Omega-3 nutrition, placental transfer and fetal brain development in gestational diabetes and preeclampsia. Nutrients, 11(5), 1107.

    Article  Google Scholar 

  • Dieter, J. N. I., Emory, E. K., Johnson, K. C., & Raynor, B. D. (2008). Maternal depression and anxiety effects on the human fetus: Preliminary findings and clinical implications. Infant Mental Health Journal, 29(5), 420–441.

    Article  Google Scholar 

  • DiPietro, J. A. (2004). The role of prenatal stress in child development. Current Directions in Psychological Science, 13(2), 71–74.

    Article  Google Scholar 

  • DiPietro, J. A., Hodgson, D. M., Costigan, K. A., Hilton, S. C., & Johnson, T. R. (1996a). Development of fetal movement--fetal heart rate coupling from 20 weeks through term. Early Human Development, 44(2), 139–151.

    Article  Google Scholar 

  • DiPietro, J. A., Hodgson, D. M., Costigan, K. A., Hilton, S. C., & Johnson, T. R. (1996b). Fetal neurobehavioral development. Child Development, 67(5), 2553–2567.

    Article  Google Scholar 

  • DiPietro, J. A., Hodgson, D. M., Costigan, K. A., & Johnson, T. R. (1996c). Fetal antecedents of infant temperament. Child Development, 67(5), 2568–2583.

    Article  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(4), 221–228.

    Article  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(6), 1421–1428.

    Article  Google Scholar 

  • DiPietro, J. A., Hilton, S. C., Hawkins, M., Costigan, K. A., & Pressman, E. K. (2002). Maternal stress and affect influence fetal neurobehavioral development. Developmental Psychology, 38(5), 659–668.

    Article  Google Scholar 

  • DiPietro, J. A., Caulfield, L. E., Costigan, K. A., Merialdi, M., Nguyen, R. H., Zavaleta, N., & Gurewitsch, E. D. (2004). Fetal neurobehavioral development: A tale of two cities. Developmental Psychology, 40(3), 445.

    Article  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(6), 1788–1798.

    Article  Google Scholar 

  • DiPietro, J. A., Kivlighan, K. T., Costigan, K. A., & Laudenslager, M. L. (2009). Fetal motor activity and maternal cortisol. Developmental Psychobiology, 51(6), 505–512.

    Article  Google Scholar 

  • DiPietro, J. A., Kivlighan, K. T., Costigan, K. A., Rubin, S. E., Shiffler, D. E., Henderson, J. L., & Pillion, J. P. (2010). Prenatal antecedents of newborn neurological maturation. Child Development, 81(1), 115–130.

    Article  Google Scholar 

  • DiPietro, J. A., Costigan, K. A., & Voegtline, K. M. (2015). Studies in fetal behavior: Revisited, renewed, and reimagined. Monographs of the Society for Research in Child Development, 80(3), vii–94.

    Article  Google Scholar 

  • Doyle, C., Werner, E., Feng, T., Lee, S., Altemus, M., Isler, J. R., & Monk, C. (2015). Pregnancy distress gets under fetal skin: Maternal ambulatory assessment & sex differences in prenatal development. Developmental Psychobiology, 57(5), 607–625.

    Article  Google Scholar 

  • Draganova, R., Eswaran, H., Murphy, P., Lowery, C., & Preissl, H. (2007). Serial magnetoencephalographic study of fetal and newborn auditory discriminative evoked responses. Early Human Development, 83(3), 199–207.

    Article  Google Scholar 

  • Fedorova, I., Alvheim, A. R., Hussein, N., & Salem, N., Jr. (2009). Deficit in prepulse inhibition in mice caused by dietary n-3 fatty acid deficiency. Behavioral Neuroscience, 123(6), 1218.

    Article  Google Scholar 

  • Field, T., Sandberg, D., Garcia, R., Vega-Lahr, N., Goldstein, S., & Guy, L. (1985). Pregnancy problems, postpartum depression, and early mother–infant interactions. Developmental Psychology, 21(6), 1152.

    Article  Google Scholar 

  • Fowden, A., Forhead, A., Coan, P., & Burton, G. (2008). The placenta and intrauterine programming. Journal of Neuroendocrinology, 20(4), 439–450.

    Article  Google Scholar 

  • Fujioka, T., Fujioka, A., Tan, N., Chowdhury, G. M., Mouri, H., Sakata, Y., & Nakamura, S. (2001). Mild prenatal stress enhances learning performance in the non-adopted rat offspring. Neuroscience, 103(2), 301–307.

    Article  Google Scholar 

  • Georgiades, P., Ferguson-Smith, A., & Burton, G. (2002). Comparative developmental anatomy of the murine and human definitive placentae. Placenta, 23(1), 3–19.

    Article  Google Scholar 

  • Glover, V. (2011). Annual research review: Prenatal stress and the origins of psychopathology: An evolutionary perspective. Journal of Child Psychology and Psychiatry, 52(4), 356–367.

    Article  Google Scholar 

  • Glover, V. (2015). Prenatal stress and its effects on the fetus and the child: Possible underlying biological mechanisms. Advance Neurobiology, 10, 269–283.

    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(5), 601–610.

    Article  Google Scholar 

  • Goeden, N., Velasquez, J., Arnold, K. A., Chan, Y., Lund, B. T., Anderson, G. M., & Bonnin, A. (2016). Maternal inflammation disrupts fetal neurodevelopment via increased placental output of serotonin to the fetal brain. Journal of Neuroscience, 36(22), 6041–6049.

    Article  Google Scholar 

  • Goland, R. S., Jozak, S., Warren, W. B., Conwell, I. M., Stark, R. I., & Tropper, P. J. (1993). Elevated levels of umbilical cord plasma corticotropin-releasing hormone in growth-retarded fetuses. The Journal of Clinical Endocrinology and Metabolism, 77(5), 1174–1179.

    Google Scholar 

  • Gopnik, A., Meltzoff, A. N., & Kuhl, P. K. (1999). The scientist in the crib: Minds, brains, and how children learn. New York, NY, US: William Morrow & Co.

    Google Scholar 

  • Greenough, W. T., Black, J. E., & Wallace, C. S. (1987). Experience and brain development. Child Development, 58(3), 539–559.

    Article  Google Scholar 

  • Groome, L. J., Gotlieb, S. J., Neely, C. L., & Waters, M. D. (1993). Developmental trends in fetal habituation to vibroacoustic stimulation. American Journal of Perinatology, 10(01), 46–49.

    Article  Google Scholar 

  • Groome, L. J., Swiber, M. J., Bentz, L. S., Holland, S. B., & Atterbury, J. L. (1995). Maternal anxiety during pregnancy: Effect on fetal behavior at 38 to 40 weeks of gestation. Journal of Developmental and Behavioral Pediatrics, 16(6), 391–396.

    Article  Google Scholar 

  • Hepper, P. (1992). Fetal psychology: An embryonic science. In J. G. Nijhuis (Ed.), Fetal behaviour: Developmental and perinatal aspects (p. 28). Oxford: Oxford University Press.

    Google Scholar 

  • Higgins, J., Vaughan, O., de Liger, E. F., Fowden, A. L., & Sferruzzi-Perri, A. N. (2016). Placental phenotype and resource allocation to fetal growth are modified by the timing and degree of hypoxia during mouse pregnancy. The Journal of Physiology, 594(5), 1341–1356.

    Article  Google Scholar 

  • Huang, H., & Vasung, L. (2014). Gaining insight of fetal brain development with diffusion MRI and histology. International Journal of Developmental Neuroscience, 32, 11–22.

    Article  Google Scholar 

  • Hvizdošová-Kleščová, A., Uhlik, J., Malina, M., Vulterinova, H., Novotný, T., & Vajner, L. (2013). Remodeling of fetoplacental arteries in rats due to chronic hypoxia. Experimental and Toxicologic Pathology, 65(1–2), 97–103.

    Article  Google Scholar 

  • Jakab, A. (2019). Developmental pathoconnectomics and advanced fetal MRI. Topics in Magnetic Resonance Imaging, 28(5), 275–284.

    Article  Google Scholar 

  • Jansson, T., & Powell, T. L. (2006). Human placental transport in altered fetal growth: Does the placenta function as a nutrient sensor?–a review. Placenta, 27, 91–97.

    Article  Google Scholar 

  • Jansson, T., & Powell, T. L. (2007). Role of the placenta in fetal programming: Underlying mechanisms and potential interventional approaches. Clinical Science, 113(1), 1–13.

    Article  Google Scholar 

  • Jarvie, E., Hauguel-de-Mouzon, S., Nelson, S. M., Sattar, N., Catalano, P. M., & Freeman, D. J. (2010). Lipotoxicity in obese pregnancy and its potential role in adverse pregnancy outcome and obesity in the offspring. Clinical Science, 119(3), 123–129.

    Article  Google Scholar 

  • Jašarević, E., Morrison, K. E., & Bale, T. L. (2016). Sex differences in the gut microbiome–brain axis across the lifespan. Philosophical Transactions of the Royal Society, B: Biological Sciences, 371(1688), 20150122.

    Article  Google Scholar 

  • Jiang, X., Yan, J., West, A. A., Perry, C. A., Malysheva, O. V., Devapatla, S., Pressman, E., Vermeylen, F., & Caudill, M. A. (2012). Maternal choline intake alters the epigenetic state of fetal cortisol-regulating genes in humans. The FASEB Journal, 26(8), 3563–3574.

    Article  Google Scholar 

  • Karin, J., Hirsch, M., & Akselrod, S. (1993). An estimate of fetal autonomic state by spectral analysis of fetal heart rate fluctuations. Pediatric Research, 34(2), 134–138.

    Article  Google Scholar 

  • Khashan, A. S., Abel, K. M., McNamee, R., Pedersen, M. G., Webb, R. T., Baker, P. N., Kenny, L. C., & Mortensen, P. B. (2008). Higher risk of offspring schizophrenia following antenatal maternal exposure to severe adverse life events. Archives of General Psychiatry, 65(2), 146–152.

    Article  Google Scholar 

  • Kim, S., Kim, H., Yim, Y. S., Ha, S., Atarashi, K., Tan, T. G., Longman, R. S., Honda, K., Littman, D. R., Choi, G. B., & Huh, J. R. (2017). Maternal gut bacteria promote neurodevelopmental abnormalities in mouse offspring. Nature, 549(7673), 528–532.

    Article  Google Scholar 

  • Kisilevsky, B. S., Muir, D. W., & Low, J. A. (1992). Maturation of human fetal responses to vibroacoustic stimulation. Child Development, 63, 1497–1508.

    Article  Google Scholar 

  • Lager, S., & Powell, T. L. (2012). Regulation of nutrient transport across the placenta. Journal of Pregnancy, 2012, 1–14.

    Article  Google Scholar 

  • Lambertini, L., Chen, J., & Nomura, Y. (2015). Mitochondrial gene expression profiles are associated with maternal psychosocial stress in pregnancy and infant temperament. PLoS One, 10(9), e0138929.

    Article  Google Scholar 

  • Lane, R. H., Ramirez, R. J., Tsirka, A. E., Kloesz, J. L., McLaughlin, M. K., Gruetzmacher, E. M., & Devaskar, S. U. (2001). Uteroplacental insufficiency lowers the threshold towards hypoxia-induced cerebral apoptosis in growth-retarded fetal rats. Brain Research, 895(1–2), 186–193.

    Article  Google Scholar 

  • Lewis, M., Wilson, C. D., Ban, P., & Baumel, M. H. (1970). An exploratory study of resting cardiac rate and variability from the last trimester of prenatal life through the first year of postnatal life. Child Development, 41(3), 799–811.

    Article  Google Scholar 

  • Lewis, R., Doherty, C., James, L., Burton, G., & Hales, C. (2001). Effects of maternal iron restriction on placental vascularization in the rat. Placenta, 22(6), 534–539.

    Article  Google Scholar 

  • Lindegaard, M. L., Wassif, C. A., Vaisman, B., Amar, M., Wasmuth, E. V., Shamburek, R., Nielsen, L. B., Remaley, A. T., & Porter, F. D. (2008). Characterization of placental cholesterol transport: ABCA1 is a potential target for in utero therapy of Smith–Lemli–Opitz syndrome. Human Molecular Genetics, 17(23), 3806–3813.

    Article  Google Scholar 

  • Madore, C., Nadjar, A., Delpech, J.-C., Sere, A., Aubert, A., Portal, C., Joffre, C., & Layé, S. (2014). Nutritional n-3 PUFAs deficiency during perinatal periods alters brain innate immune system and neuronal plasticity-associated genes. Brain, Behavior, and Immunity, 41, 22–31.

    Article  Google Scholar 

  • Mairesse, J., Lesage, J., Breton, C., Bréant, B., Hahn, T., Darnaudéry, M., Dickson, S. L., Seckl, J., Blondeau, B., & Vieau, D. (2007). Maternal stress alters endocrine function of the feto-placental unit in rats. American Journal of Physiology. Endocrinology and Metabolism, 292(6), E1526–E1533.

    Article  Google Scholar 

  • Malassine, A., Frendo, J. L., & Evain-Brion, D. (2003). A comparison of placental development and endocrine functions between the human and mouse model. Human Reproduction Update, 9(6), 531–539.

    Article  Google Scholar 

  • Marsit, C. J., Maccani, M. A., Padbury, J. F., & Lester, B. M. (2012). Placental 11-beta hydroxysteroid dehydrogenase methylation is associated with newborn growth and a measure of neurobehavioral outcome. PLoS One, 7(3), e33794.

    Article  Google Scholar 

  • Martin, C. B., Jr. (1978). Regulation of the fetal heart rate and genesis of FHR patterns. Seminars in Perinatology, 2(2), 131–146.

    Google Scholar 

  • McCarthy, M. M. (2019). Sex differences in neuroimmunity as an inherent risk factor. Neuropsychopharmacology, 44(1), 38.

    Article  Google Scholar 

  • McQuaid, G. A., Darcey, V. L., Avalos, M. F., Fishbein, D. H., & VanMeter, J. W. (2019). Altered cortical structure and psychiatric symptom risk in adolescents exposed to maternal stress in utero: A retrospective investigation. Behavioural Brain Research, 375, 112145.

    Article  Google Scholar 

  • Meehl, P. E. (1978). Theoretical risks and tabular asterisks: Sir Karl, sir Ronald, and the slow progress of soft psychology. Journal of Consulting and Clinical Psychology, 46(4), 806–834.

    Article  Google Scholar 

  • Miller, A. H., & Raison, C. L. (2016). The role of inflammation in depression: From evolutionary imperative to modern treatment target. Nature Reviews Immunology, 16(1), 22.

    Article  Google Scholar 

  • Monk, C., Fifer, W. P., Myers, M. M., Sloan, R. P., Trien, L., & Hurtado, A. (2000). Maternal stress responses and anxiety during pregnancy: Effects on fetal heart rate. Developmental Psychobiology, 36(1), 67–77.

    Article  Google Scholar 

  • Monk, C., Myers, M. M., Sloan, R. P., Ellman, L. M., & Fifer, W. P. (2003). Effects of women’s stress-elicited physiological activity and chronic anxiety on fetal heart rate. Journal of Developmental and Behavioral Pediatrics, 24(1), 32–38.

    Article  Google Scholar 

  • Monk, C., Sloan, R. P., Myers, M. M., Ellman, L., Werner, E., Jeon, J., Tager, F., & Fifer, W. P. (2004). Fetal heart rate reactivity differs by women’s psychiatric status: An early marker for developmental risk? Journal of the American Academy of Child and Adolescent Psychiatry, 43(3), 283–290.

    Article  Google Scholar 

  • Monk, C., Georgieff, M. K., & Osterholm, E. A. (2013). Maternal prenatal distress and poor nutrition – Mutually influencing risk factors affecting infant neurocognitive development. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 54(2), 115–130.

    Article  Google Scholar 

  • Monk, C., Feng, T., Lee, S., Krupska, I., Champagne, F. A., & Tycko, B. (2016). Distress during pregnancy: Epigenetic regulation of placenta glucocorticoid-related genes and fetal neurobehavior. American Journal of Psychiatry, 7, 705–713.

    Article  Google Scholar 

  • Monk, C., Lugo-Candelas, C., & Trumpff, C. (2019). Prenatal developmental origins of future psychopathology: Mechanisms and pathways. Annual Review of Clinical Psychology, 15, 317–344.

    Article  Google Scholar 

  • Morishima, H. O., Pedersen, H., & Finster, M. (1978). The influence of maternal psychological stress on the fetus. American Journal of Obstetrics and Gynecology, 131(3), 286–290.

    Article  Google Scholar 

  • Morrison, K. E., Epperson, C. N., & Bale, T. L. (2020). Sex differences in the programming of stress resilience. In Stress resilience (pp. 81–94). Elsevier.

    Google Scholar 

  • Mueller, B. R., & Bale, T. L. (2008). Sex-specific programming of offspring emotionality after stress early in pregnancy. Journal of Neuroscience, 28(36), 9055–9065.

    Article  Google Scholar 

  • Myatt, L. (2006). Placental adaptive responses and fetal programming. The Journal of Physiology, 572(1), 25–30.

    Article  Google Scholar 

  • Myers, R. E. (1975). Maternal psychological stress and fetal asphyxia: A study in the monkey. American Journal of Obstetrics and Gynecology, 122(1), 47–59.

    Article  Google Scholar 

  • Nguyen, T., Tseng, Y., McGonnigal, B., Stabila, J., Worrell, L., Saha, S., & Padbury, J. (1999). Placental biogenic amine transporters: In vivo function, regulation and pathobiological significance. Placenta, 20(1), 3–11.

    Article  Google Scholar 

  • Niculescu, M. D., & Zeisel, S. H. (2002). Diet, methyl donors and DNA methylation: Interactions between dietary folate, methionine and choline. The Journal of Nutrition, 132(8), 2333S–2335S.

    Article  Google Scholar 

  • Nijhuis, I. J., ten Hof, J., Nijhuis, J. G., Mulder, E. J., Narayan, H., Taylor, D. J., & Visser, G. H. (1999). Temporal organization of fetal behavior from 24-weeks gestation onwards in normal and complicated pregnancies. Developmental Psychobiology, 34(4), 257–268.

    Article  Google Scholar 

  • Nijhuis, I. J., ten Hof, J., Mulder, E. J., Nijhuis, J. G., Narayan, H., Taylor, D. J., & Visser, G. H. (2000). Fetal heart rate in relation to its variation in normal and growth retarded fetuses. European Journal of Obstetrics, Gynecology, and Reproductive Biology, 89(1), 27–33.

    Article  Google Scholar 

  • Nugent, B. M., O’Donnell, C. M., Epperson, C. N., & Bale, T. L. (2018). Placental H3K27me3 establishes female resilience to prenatal insults. Nature Communications, 9(1), 2555.

    Article  Google Scholar 

  • O’Connor, T. G., Monk, C., & Fitelson, E. M. (2014). Practitioner review: Maternal mood in pregnancy and child development–implications for child psychology and psychiatry. Journal of Child Psychology and Psychiatry, 55(2), 99–111.

    Article  Google Scholar 

  • O’Donnell, K. J., Jensen, A. B., Freeman, L., Khalife, N., O’Connor, T. G., & Glover, V. (2012). Maternal prenatal anxiety and downregulation of placental 11β-HSD2. Psychoneuroendocrinology, 37(6), 818–826.

    Article  Google Scholar 

  • Oberlander, T. F. (2012). Fetal serotonin signaling: Setting pathways for early childhood development and behavior. Journal of Adolescent Health, 51(2), S9–S16.

    Article  Google Scholar 

  • Oh, S. S., Galanter, J., Thakur, N., Pino-Yanes, M., Barcelo, N. E., White, M. J., de Bruin, D. M., Greenblatt, R. M., Bibbins-Domingo, K., Wu, A. H. B., Borrell, L. N., Gunter, C., Powe, N. R., & Burchard, E. G. (2015). Diversity in clinical and biomedical research: A promise yet to be fulfilled. PLoS Medicine, 12(12), e1001918.

    Article  Google Scholar 

  • Ohta, T., Okamura, K., Kimura, Y., Suzuki, T., Watanabe, T., Yasui, T., Yaegashi, N., & Yajima, A. (1999). Alteration in the low-frequency domain in power spectral analysis of fetal heart beat fluctuations. Fetal Diagnosis and Therapy, 14(2), 92–97.

    Article  Google Scholar 

  • Padula, A. M., Monk, C., Brennan, P. A., Borders, A., Barrett, E. S., McEvoy, C. T., Foss, S., Desai, P., Alshawabkeh, A., & Wurth, R. (2019). A review of maternal prenatal exposures to environmental chemicals and psychosocial stressors—Implications for research on perinatal outcomes in the ECHO program. Journal of Perinatology, 40, 1–15.

    Google Scholar 

  • Paquette, A. G., & Marsit, C. J. (2014). The developmental basis of epigenetic regulation of HTR2A and psychiatric outcomes. Journal of Cellular Biochemistry, 115(12), 2065–2072.

    Article  Google Scholar 

  • Paquette, A. G., Lesseur, C., Armstrong, D. A., Koestler, D. C., Appleton, A. A., Lester, B. M., & Marsit, C. J. (2013). Placental HTR2A methylation is associated with infant neurobehavioral outcomes. Epigenetics, 8(8), 796–801.

    Article  Google Scholar 

  • Paquette, A. G., Lester, B. M., Koestler, D. C., Lesseur, C., Armstrong, D. A., & Marsit, C. J. (2014). Placental FKBP5 genetic and epigenetic variation is associated with infant neurobehavioral outcomes in the RICHS cohort. PLoS One, 9(8), e104913.

    Article  Google Scholar 

  • Partanen, E., Kujala, T., Naatanen, R., Liitola, A., Sambeth, A., & Huotilainen, M. (2013). Learning-induced neural plasticity of speech processing before birth. Proceedings of the National Academy of Sciences of the United States of America, 110(37), 15145–15150.

    Article  Google Scholar 

  • Patterson, P. H. (2011). Maternal infection and immune involvement in autism. Trends in Molecular Medicine, 17(7), 389–394.

    Article  Google Scholar 

  • Peña, C. J., Monk, C., & Champagne, F. A. (2012). Epigenetic effects of prenatal stress on 11β-hydroxysteroid dehydrogenase-2 in the placenta and fetal brain. PLoS One, 7(6), e39791.

    Article  Google Scholar 

  • Perez-Muñoz, M. E., Arrieta, M.-C., Ramer-Tait, A. E., & Walter, J. (2017). A critical assessment of the “sterile womb” and “in utero colonization” hypotheses: Implications for research on the pioneer infant microbiome. Microbiome, 5(1), 48.

    Article  Google Scholar 

  • Picard, M., Zhang, J., Hancock, S., Derbeneva, O., Golhar, R., Golik, P., O’Hearn, S., Levy, S., Potluri, P., & Lvova, M. (2014). Progressive increase in mtDNA 3243A> G heteroplasmy causes abrupt transcriptional reprogramming. Proceedings of the National Academy of Sciences, 111(38), E4033–E4042.

    Article  Google Scholar 

  • Pillai, M., & James, D. (1991). Human fetal mouthing movements: A potential biophysical variable for distinguishing state 1F from abnormal fetal behaviour; report of 4 cases. European Journal of Obstetrics & Gynecology and Reproductive Biology, 38(2), 151–156.

    Article  Google Scholar 

  • Porges, S., McCabe, P., & Yongue, B. (1982). Respiratory-heart rate interactions: Psychophysiological implications for pathophysiology and behavior. Perspectives in Cardiovascular Psychophysiology, 223–264.

    Google Scholar 

  • Porges, S. W., Doussard-Roosevelt, J. A., Portales, A. L., & Greenspan, S. I. (1996). Infant regulation of the vagal "brake" predicts child behavior problems: A psychobiological model of social behavior. Developmental Psychobiology, 29(8), 697–712.

    Article  Google Scholar 

  • Posner, J., Cha, J., Roy, A. K., Peterson, B. S., Bansal, R., Gustafsson, H. C., Raffanello, E., Gingrich, J., & Monk, C. (2016). Alterations in amygdala-prefrontal circuits in infants exposed to prenatal maternal depression. Translational Psychiatry, 6(11), e935.

    Article  Google Scholar 

  • Prayer, D., Kasprian, G., Krampl, E., Ulm, B., Witzani, L., Prayer, L., & Brugger, P. C. (2006). MRI of normal fetal brain development. European Journal of Radiology, 57(2), 199–216.

    Article  Google Scholar 

  • Prechtl, H. F. R. (1984). Continuity and change in early neural development. Clinics in Developmental Medicine, 94, 1–15.

    Google Scholar 

  • Pressman, E., DiPietro, J., Costigan, K., Shupe, A., & Johnson, T. (1998). Fetal neurobehavioral development: Associations with socioeconomic class and fetal sex. Developmental Psychobiology, 33(1), 79–91.

    Article  Google Scholar 

  • Reid, M. V., Murray, K. A., Marsh, E. D., Golden, J. A., Simmons, R. A., & Grinspan, J. B. (2012). Delayed myelination in an intrauterine growth retardation model is mediated by oxidative stress upregulating bone morphogenetic protein 4. Journal of Neuropathology and Experimental Neurology, 71(7), 640–653.

    Article  Google Scholar 

  • Reynolds, R. M., Labad, J., Buss, C., Ghaemmaghami, P., & Raikkonen, K. (2013). Transmitting biological effects of stress in utero: Implications for mother and offspring. Psychoneuroendocrinology, 38(9), 1843–1849.

    Article  Google Scholar 

  • Roberts, C., Sohlstrom, A., Kind, K., Earl, R., Khong, T., Robinson, J., Owens, P., & Owens, J. (2001). Maternal food restriction reduces the exchange surface area and increases the barrier thickness of the placenta in the Guinea-pig. Placenta, 22(2–3), 177–185.

    Article  Google Scholar 

  • Robinson, B. G., Emanuel, R. L., Frim, D. M., & Majzoub, J. A. (1988). Glucocorticoid stimulates expression of corticotropin-releasing hormone gene in human placenta. Proceedings of the National Academy of Sciences of the United States of America, 85(14), 5244–5248.

    Article  Google Scholar 

  • Rossant, J., & Cross, J. C. (2001). Placental development: lessons from mouse mutants. Nature Reviews Genetics, 2(7), 538.

    Article  Google Scholar 

  • Rutland, C., Latunde-Dada, A., Thorpe, A., Plant, R., Langley-Evans, S., & Leach, L. (2007). Effect of gestational nutrition on vascular integrity in the murine placenta. Placenta, 28(7), 734–742.

    Article  Google Scholar 

  • Sachis, P. N., Armstrong, D. L., Becker, L. E., & Bryan, A. C. (1982). Myelination of the human vagus nerve from 24 weeks postconceptional age to adolescence. Journal of Neuropathology & Experimental Neurology, 41(4), 466–472.

    Article  Google Scholar 

  • Sánchez-Villegas, A., Verberne, L., De Irala, J., Ruíz-Canela, M., Toledo, E., Serra-Majem, L., & Martínez-González, M. A. (2011). Dietary fat intake and the risk of depression: The SUN project. PLoS One, 6(1), e16268.

    Article  Google Scholar 

  • Sánchez-Villegas, A., Toledo, E., de Irala, J., Ruiz-Canela, M., Pla-Vidal, J., & Martínez-González, M. A. (2012). Fast-food and commercial baked goods consumption and the risk of depression. Public Health Nutrition, 15(3), 424–432.

    Article  Google Scholar 

  • Sandman, C. A., Wadhwa, P., Glynn, L., Chicz-Demet, A., Porto, M., & Garite, T. J. (1999a). Corticotrophin-releasing hormone and fetal responses in human pregnancy. Annals of the New York Academy of Sciences, 897, 66–75.

    Article  Google Scholar 

  • Sandman, C. A., Wadhwa, P. D., Chicz-DeMet, A., Porto, M., & Garite, T. J. (1999b). Maternal corticotropin-releasing hormone and habituation in the human fetus. Developmental Psychobiology, 34(3), 163–173.

    Article  Google Scholar 

  • Sandman, C. A., Buss, C., Head, K., & Davis, E. P. (2015). Fetal exposure to maternal depressive symptoms is associated with cortical thickness in late childhood. Biological Psychiatry, 77(4), 324–334.

    Article  Google Scholar 

  • Sandman, C. A., Curran, M. M., Davis, E. P., Glynn, L. M., Head, K., & Baram, T. Z. (2018). Cortical thinning and neuropsychiatric outcomes in children exposed to prenatal adversity: A role for placental CRH? American Journal of Psychiatry, 175(5), 471–479.

    Article  Google Scholar 

  • Sarkar, S., Craig, M. C., Dell’Acqua, F., O’Connor, T. G., Catani, M., Deeley, Q., Glover, V., & Murphy, D. G. (2014). Prenatal stress and limbic-prefrontal white matter microstructure in children aged 6-9 years: A preliminary diffusion tensor imaging study. The World Journal of Biological Psychiatry, 15(4), 346–352.

    Article  Google Scholar 

  • Saunders, R. (2005). Static magnetic fields: Animal studies. Progress in Biophysics and Molecular Biology, 87(2–3), 225–239.

    Article  Google Scholar 

  • Schroeder, D. I., Blair, J. D., Lott, P., Yu, H. O. K., Hong, D., Crary, F., Ashwood, P., Walker, C., Korf, I., & Robinson, W. P. (2013). The human placenta methylome. Proceedings of the National Academy of Sciences, 110(15), 6037–6042.

    Article  Google Scholar 

  • Schulz, L. C., Schlitt, J. M., Caesar, G., & Pennington, K. A. (2012). Leptin and the placental response to maternal food restriction during early pregnancy in mice. Biology of Reproduction, 87(5), 120, 121–120, 129.

    Article  Google Scholar 

  • Scorza, P., Duarte, C. S., Hipwell, A. E., Posner, J., Ortin, A., Canino, G., & Monk, C. (2019). Research review: Intergenerational transmission of disadvantage: Epigenetics and parents’ childhoods as the first exposure. Journal of Child Psychology and Psychiatry, 60(2), 119–132.

    Article  Google Scholar 

  • Seckl, J. R., & Holmes, M. C. (2007). Mechanisms of disease: Glucocorticoids, their placental metabolism and fetal ‘programming’ of adult pathophysiology. Nature Reviews Endocrinology, 3(6), 479.

    Article  Google Scholar 

  • Shah, R., Courtiol, E., Castellanos, F. X., & Teixeira, C. M. (2018). Abnormal serotonin levels during perinatal development lead to behavioral deficits in adulthood. Frontiers in Behavioral Neuroscience, 12, 114.

    Article  Google Scholar 

  • Sheridan, C. J., Matuz, T., Draganova, R., Eswaran, H., & Preissl, H. (2010). Fetal magnetoencephalography – Achievements and challenges in the study of prenatal and early postnatal brain responses: A review. Infant and Child Development, 19(1), 80–93.

    Article  Google Scholar 

  • Sies, H. (2000). What is oxidative stress? In Oxidative stress and vascular disease (pp. 1–8). Berlin: Springer.

    Google Scholar 

  • Sjostrom, K., Valentin, L., Thelin, T., & Marsal, K. (2002). Maternal anxiety in late pregnancy: Effect on fetal movements and fetal heart rate. Early Human Development, 67(1–2), 87–100.

    Article  Google Scholar 

  • Snidman, N., Kagan, J., Riordan, L., & Shannon, D. C. (1995). Cardiac function and behavioral reactivity during infancy. Psychophysiology, 32(3), 199–207.

    Article  Google Scholar 

  • Sontag, L. W. (1941). The significance of fetal environmental differences. American Journal of Obstetrics and Gynecology, 42(6), 996–1003.

    Article  Google Scholar 

  • Sontag, L. W., & Richards, T. W. (1938). Studies in fetal behavior: I. Fetal heart rate as a behavioral indicator. Monographs of the Society for Research in Child Development, 3(4), i–72.

    Article  Google Scholar 

  • Sontag, L., & Wallace, R. F. (1934). Preliminary report of the fels fund: Study of fetal activity. American Journal of Diseases of Children, 48(5), 1050–1057.

    Article  Google Scholar 

  • Soo, P. S., Hiscock, J., Botting, K. J., Roberts, C. T., Davey, A. K., & Morrison, J. L. (2012). Maternal undernutrition reduces P-glycoprotein in Guinea pig placenta and developing brain in late gestation. Reproductive Toxicology, 33(3), 374–381.

    Article  Google Scholar 

  • Sykiotis, G. P., & Papavassiliou, A. G. (2001). Serine phosphorylation of insulin receptor substrate-1: A novel target for the reversal of insulin resistance. Molecular Endocrinology, 15(11), 1864–1869.

    Google Scholar 

  • Takahashi, E., Folkerth, R. D., Galaburda, A. M., & Grant, P. E. (2012). Emerging cerebral connectivity in the human fetal brain: An MR tractography study. Cerebral Cortex, 22(2), 455–464.

    Article  Google Scholar 

  • Tanti, J.-F., & Jager, J. (2009). Cellular mechanisms of insulin resistance: Role of stress-regulated serine kinases and insulin receptor substrates (IRS) serine phosphorylation. Current Opinion in Pharmacology, 9(6), 753–762.

    Article  Google Scholar 

  • Tau, G. Z., & Peterson, B. S. (2010). Normal development of brain circuits. Neuropsychopharmacology, 35(1), 147–168.

    Article  Google Scholar 

  • Thomas, P. W., Haslum, M. N., MacGillivray, I., & Golding, M. J. (1989). Does fetal heart rate predict subsequent heart rate in childhood? Early Human Development, 19(2), 147–152.

    Article  Google Scholar 

  • Thomason, M. E., Dassanayake, M. T., Shen, S., Katkuri, Y., Alexis, M., Anderson, A. L., Yeo, L., Mody, S., Hernandez-Andrade, E., Hassan, S. S., Studholme, C., Jeong, J. W., & Romero, R. (2013). Cross-hemispheric functional connectivity in the human fetal brain. Science Translational Medicine, 5(173), 173ra124.

    Article  Google Scholar 

  • Thomason, M. E., Hect, J., Waller, R., Manning, J. H., Stacks, A. M., Beeghly, M., Boeve, J. L., Wong, K., van den Heuvel, M. I., Hernandez-Andrade, E., Hassan, S. S., & Romero, R. (2018). Prenatal neural origins of infant motor development: Associations between fetal brain and infant motor development. Development and Psychopathology, 30(3), 763–772.

    Article  Google Scholar 

  • Van den Bergh, B. R., Mulder, E. J., Visser, G. H., Poelmann-Weesjes, G., Bekedam, D. J., & Prechtl, H. F. (1989). The effect of (induced) maternal emotions on fetal behaviour: A controlled study. Early Human Development, 19(1), 9–19.

    Article  Google Scholar 

  • van den Bergh, B. R. H., van den Heuvel, M. I., Lahti, M., Braeken, M., de Rooij, S. R., Entringer, S., Hoyer, D., Roseboom, T., Raikkonen, K., King, S., & Schwab, M. (2017). Prenatal developmental origins of behavior and mental health: The influence of maternal stress in pregnancy. Neuroscience and Biobehavioral Reviews. https://doi.org/10.1016/j.neubiorev.2017.07.003.

  • Vermeulen, E., Stronks, K., Snijder, M. B., Schene, A. H., Lok, A., de Vries, J. H., Visser, M., Brouwer, I. A., & Nicolaou, M. (2017). A combined high-sugar and high-saturated-fat dietary pattern is associated with more depressive symptoms in a multi-ethnic population: The HELIUS (healthy life in an urban setting) study. Public Health Nutrition, 20(13), 2374–2382.

    Article  Google Scholar 

  • Vrba, J., Robinson, S., McCubbin, J., Murphy, P., Eswaran, H., Wilson, J., Preissl, H., & Lowery, C. (2004). Human fetal brain imaging by magnetoencephalography: Verification of fetal brain signals by comparison with fetal brain models. NeuroImage, 21(3), 1009–1020.

    Article  Google Scholar 

  • Walker, R. W., Clemente, J. C., Peter, I., & Loos, R. J. F. (2017). The prenatal gut microbiome: Are we colonized with bacteria in utero? Pediatric Obesity, 12(Suppl 1), 3–17.

    Article  Google Scholar 

  • Walton, A., & Hammond, J. (1938). The maternal effects on growth and conformation in shire horse-shetland pony crosses. Proceedings of the Royal Society of London, Series B: Biological Sciences, 125(840), 311–335.

    Google Scholar 

  • Watson, E. D., & Cross, J. C. (2005). Development of structures and transport functions in the mouse placenta. Physiology, 20(3), 180–193.

    Article  Google Scholar 

  • Werner, E. A., Myers, M. M., Fifer, W. P., Cheng, B., Fang, Y., Allen, R., & Monk, C. (2007a). Prenatal predictors of infant temperament. Developmental Psychobiology, 49(5), 474–484.

    Article  Google Scholar 

  • Werner, E. A., Myers, M. M., Fifer, W. P., Cheng, B., Fang, Y., Allen, R., Monk, C., Gorenstein, E. E., Tager, F. A., Shapiro, P. A., Monk, C., & Sloan, R. P. (2007b). Prenatal predictors of infant temperament Cognitive-behavior therapy for reduction of persistent anger. Developmental Psychobiology, 49(5), 474–484.

    Article  Google Scholar 

  • Werner, E. A., Gustafsson, H. C., Lee, S., Feng, T., Jiang, N., Desai, P., & Monk, C. (2016). PREPP: Postpartum depression prevention through the mother–infant dyad. Archives of Women’s Mental Health, 19(2), 229–242.

    Article  Google Scholar 

  • Yoshida, S., & Wada, Y. (2005). Transfer of maternal cholesterol to embryo and fetus in pregnant mice. Journal of Lipid Research, 46(10), 2168–2174.

    Article  Google Scholar 

  • Yoshizato, T., Koyanagi, T., Takashima, T., Satoh, S., Akazawa, K., & Nakano, H. (1994). The relationship between age-related heart rate changes and developing brain function: A model of anencephalic human fetuses in utero. Early Human Development, 36(2), 101–112.

    Article  Google Scholar 

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Scorza, P., Doyle, C., Monk, C. (2021). Prenatal Programming in the Fetus and Placenta. In: Wazana, A., Székely, E., Oberlander, T.F. (eds) Prenatal Stress and Child Development. Springer, Cham. https://doi.org/10.1007/978-3-030-60159-1_4

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