Skip to main content
SpringerLink
Log in

Navigating Transitions in Hypothalamic–Pituitary–Adrenal Function from Pregnancy Through Lactation: Implications for Maternal Health and Infant Brain Development

  • Chapter
  • First Online:
Building Babies

Part of the book series: Developments in Primatology: Progress and Prospects ((DIPR,volume 37))

Abstract

Despite the tremendous interest in understanding the effects of prenatal stress on fetal health and the programming of adult disease risk, the adaptive functions of hypothalamic–pituitary–adrenal (HPA) axis activity in healthy pregnancies and during lactation have been less widely considered. Existing research has addressed the influence of glucocorticoids on altered patterns of fetal growth and development in humans (Kuzawa and Sweet 2009; Seckl and Holmes 2007; Sloboda et al. 2005; 2009a, b) and the effects of prenatal stress in animal models, particularly with respect to offspring birth weight and stress reactivity (Drake et al. 2005; Neumann 2001; Seckl and Meaney 2004). With several important exceptions, the majority of this research has invoked the concept of “maternal stress” to encapsulate the premise that maternal activation of the HPA axis is associated with adverse birth outcomes, without the simultaneous acknowledgment that progressive elevation of the maternal HPA activity across the course of pregnancy is part of an anthropoid-typical pattern of neuroendocrine activity (Bowman et al. 2001; Smith et al. 1999). Even less is known about the HPA dynamics of pregnancy in non-Western populations with distinct infectious disease ecologies and marginal energetic status (Nyberg 2012). Given the human reproductive strategy of giving birth to secondarily altricial infants (Martin 2007), basal glucocorticoids may play a pivotal role in facilitating parturition and accelerating fetal tissue maturation in coordination with the timing of birth (Power and Schulkin 2006; Pike 2005; Smith et al. 2001). These constraints on the duration of gestation may be imposed, in part, by the metabolic demands of pregnancy (Ellison 2001, 2003; Martin 1996) and are further impacted by the obstetrical dilemma, imposed by the “tight fit” between fetal head circumference and the maternal pelvis that occurred as a result our hominin transition to obligate bipedalism (Rosenberg 2001; Rosenberg and Trevathan 1996). As a result, human birth is physiologically stressful, even by primate standards (Leigh 2004; Martin 1996; Rosenberg 2001; Rosenberg and Trevathan 1996).

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Akers (2002) Lactation and the mammary gland. Iowa State Press: Ames

    Google Scholar 

  • Albers EM, Riksen-Walraven JM, Sweep FC, de Weerth C (2008) Maternal behavior predicts infant cortisol recovery from a mild everyday stressor. J Child Psychol Psychiatry 49(1):97–103

    PubMed  Google Scholar 

  • Allolio B, Gunther RW, Benker G, Reinwein D, Winkelmann W, Schulte HM (1990) A multihormonal response to corticotropin-releasing hormone in inferior petrosal sinus blood of patients with Cushing’s disease. J Clin Endocrinol Metab 71(5):1195–1201

    PubMed  CAS  Google Scholar 

  • Altemus M, Deuster PA, Galliven E, Carter CS, Gold PW (1995) Suppression of hypothalamic-pituitary-adrenal axis responses to stress in lactating women. J Clin Endocrinol Metab 80(10):2954–2959

    PubMed  CAS  Google Scholar 

  • Altemus M, Redwine LS, Leong YM, Frye CA, Porges SW, Carter CS (2001) Responses to laboratory psychosocial stress in postpartum women. Psychosom Med 63(5):814–821

    PubMed  CAS  Google Scholar 

  • Anacker C, Zunszain PA, Carvalho LA, Pariante CM (2010) The glucocorticoid receptor: pivot of depression and of antidepressant treatment? Psychoneuroendocrinology 36(3):415–425

    Google Scholar 

  • Beck CT (1995) The effects of postpartum depression on maternal-infant interaction: a meta-analysis. Nurs Res 44(5):298–304

    PubMed  CAS  Google Scholar 

  • Belsky J, Houts RM, Fearon RM (2010a) Infant attachment security and the timing of puberty: testing an evolutionary hypothesis. Psychol Sci 21(9):1195–1201

    PubMed  Google Scholar 

  • Belsky J, Steinberg L, Houts RM, Halpern-Felsher BL (2010b) The development of reproductive strategy in females: early maternal harshness –  >  earlier menarche –  >  increased sexual risk taking. Dev Psychol 46(1):120–128

    PubMed  Google Scholar 

  • Benediktsson R, Calder AA, Edwards CR, Seckl JR (1997) Placental 11 beta-hydroxysteroid dehydrogenase: a key regulator of fetal glucocorticoid exposure. Clin Endocrinol (Oxf) 46(2):161–166

    CAS  Google Scholar 

  • Bergant AM, Kirchler H, Heim K, Daxenbichler G, Herold M, Schrocksnadel H (1998) Childbirth as a biological model for stress? Associations with endocrine and obstetric factors. Gynecol Obstet Invest 45(3):181–185

    PubMed  CAS  Google Scholar 

  • Bloch M, Daly RC, Rubinow DR (2003) Endocrine factors in the etiology of postpartum depression. Compr Psychiatry 44(3):234–246

    PubMed  Google Scholar 

  • Bowman ME, Lopata A, Jaffe RB, Golos TG, Wickings J, Smith R (2001) Corticotropin-releasing hormone-binding protein in primates. Am J Primatol 53(3):123–130

    PubMed  CAS  Google Scholar 

  • Brummelte S, Galea LA (2010) Depression during pregnancy and postpartum: contribution of stress and ovarian hormones. Prog Neuropsychopharmacol Biol Psychiatry 34(5):766–776

    PubMed  CAS  Google Scholar 

  • Brunson KL, Eghbal-Ahmadi M, Bender R, Chen Y, Baram TZ (2001) Long-term, progressive hippocampal cell loss and dysfunction induced by early-life administration of corticotropin-releasing hormone reproduce the effects of early-life stress. Proc Natl Acad Sci USA 98(15):8856–8861

    PubMed  CAS  Google Scholar 

  • Brunton PJ, Russell JA (2008) Attenuated hypothalamo-pituitary-adrenal axis responses to immune challenge during pregnancy: the neurosteroid opioid connection. J Physiol 586(2):369–375

    PubMed  CAS  Google Scholar 

  • Buske-Kirschbaum A, Krieger S, Wilkes C, Rauh W, Weiss S, Hellhammer DH (2007) Hypothalamic-pituitary-adrenal axis function and the cellular immune response in former preterm children. J Clin Endocrinol Metab 92(9):3429–3435

    PubMed  CAS  Google Scholar 

  • Campbell B (2011) Adrenarche in comparative perspective. Am J Hum Biol 23(1):44–52

    PubMed  Google Scholar 

  • Cannon WB (1932) Wisdom of the body. W. W. Norton & Company, New York, p 312

    Google Scholar 

  • Carter CS, Altemus M, Chrousos GP (2001) Neuroendocrine and emotional changes in the post-partum period. Prog Brain Res 133:241–249

    PubMed  CAS  Google Scholar 

  • Challis JR, Sloboda D, Matthews SG, Holloway A, Alfaidy N, Patel FA, Whittle W, Fraser M, Moss TJ, Newnham J (2001) The fetal placental hypothalamic-pituitary-adrenal (HPA) axis, parturition and post natal health. Mol Cell Endocrinol 185(1–2):135–144

    PubMed  CAS  Google Scholar 

  • Champagne F, Meaney MJ (2001) Like mother, like daughter: evidence for non-genomic transmission of parental behavior and stress responsivity. Prog Brain Res 133:287–302

    PubMed  CAS  Google Scholar 

  • Chatterton RT Jr, Hill PD, Aldag JC, Hodges KR, Belknap SM, Zinaman MJ (2000) Relation of plasma oxytocin and prolactin concentrations to milk production in mothers of preterm infants: influence of stress. J Clin Endocrinol Metab 85(10):3661–3668

    PubMed  CAS  Google Scholar 

  • Chen E, Miller GE, Kobor MS, Cole SW (2010) Maternal warmth buffers the effects of low early-life socioeconomic status on pro-inflammatory signaling in adulthood. Mol Psychiatry 16(7):729–737

    PubMed  Google Scholar 

  • Chisholm JS, Coall DA (2008) Not by bread alone: the role of psychosocial stress in age at first reproduction and health inequalities. In: Trevathan W, Smith EO, McKenna JJ (eds) Evolutionary medicine and health: new perspectives. Oxford University Press, Oxford, pp 134–148

    Google Scholar 

  • Chrousos GP (2000) The HPA axis and the stress response. Endocr Res 26(4):513–514

    PubMed  CAS  Google Scholar 

  • Clancy KBH (2012) Inflammation, reproduction, and the Goldilocks Principle. In: Clancy KBH, Hinde K, Rutherford JN (eds) Building babies: primate development in proximate and ultimate perspectives. Springer, New York

    Google Scholar 

  • Cohen S, Janicki-Deverts D, Miller GE (2007) Psychological stress and disease. JAMA 298(14):1685–1687

    PubMed  CAS  Google Scholar 

  • Cohn J, Campbell S, Matias R, Hopkins J (2011) Face-to-face interactions of postpartum depressed and nondepressed mother-infant pairs at 2 months. Dev Psychol 26:15–23

    Google Scholar 

  • Cole SW (2008) Social regulation of leukocyte homeostasis: the role of glucocorticoid sensitivity. Brain Behav Immun 22(7):1049–1055

    PubMed  CAS  Google Scholar 

  • Crespi EJ, Denver RJ (2005) Ancient origins of human developmental plasticity. Am J Hum Biol 17(1):44–54

    PubMed  Google Scholar 

  • Crocker I, Lawson N, Fletcher J. (2002) Effect of pregnancy and obstructive jaundice on inflammatory diseases: the work of P S Hench revisited. Ann Rheum Dis. 61(4):307–10

    Google Scholar 

  • Cushing H. (1932) Further concerning a parasympathetic center in the brain VII. The effect of intraventricullary-injected histamine. Proc Natl Acad Sci U S A. 18(7):500–10.

    Google Scholar 

  • Dallman MF, Strack AM, Akana SF, Bradbury MJ, Hanson ES, Scribner KA, Smith M (1993) Feast and famine: critical role of glucocorticoids with insulin in daily energy flow. Front Neuroendocrinol 14(4):303–347

    PubMed  CAS  Google Scholar 

  • de Kloet ER, Sarabdjitsingh RA (2008) Everything has rhythm: focus on glucocorticoid pulsatility. Endocrinology 149(7):3241–3243

    PubMed  Google Scholar 

  • DeSilva JM. (2011) A shift toward birthing relatively large infants early in human evolution. Proc Natl Acad Sci U S A. 108(3):1022–7

    Google Scholar 

  • de Weerth C, Buitelaar JK (2005a) Cortisol awakening response in pregnant women. Psychoneuroendocrinology 30(9):902–907

    PubMed  Google Scholar 

  • de Weerth C, Buitelaar JK (2005b) Physiological stress reactivity in human pregnancy–a review. Neurosci Biobehav Rev 29(2):295–312

    PubMed  Google Scholar 

  • de Weerth C, Zijl RH, Buitelaar JK (2003) Development of cortisol circadian rhythm in infancy. Early Hum Dev 73(1–2):39–52

    PubMed  Google Scholar 

  • de Weerth C, Wied CC, Jansen LM, Buitelaar JK (2007) Cardiovascular and cortisol responses to a psychological stressor during pregnancy. Acta Obstet Gynecol Scand:1–12

    Google Scholar 

  • Del Giudice M, Ellis BJ, Shirtcliff EA (2011) The Adaptive Calibration Model of stress responsivity. Neurosci Biobehav Rev 35(7):1562–1592

    PubMed  Google Scholar 

  • Devlin AM, Brain U, Austin J, Oberlander TF (2011) Prenatal exposure to maternal depressed mood and the MTHFR C677T variant affect SLC6A4 methylation in infants at birth. PLoS One 5(8):e12201

    Google Scholar 

  • Drake AJ, Walker BR, Seckl JR (2005) Intergenerational consequences of fetal programming by in utero exposure to glucocorticoids in rats. Am J Physiol Regul Integr Comp Physiol 288(1):R34–R38

    PubMed  CAS  Google Scholar 

  • Ellison P (2001) On fertile ground: a natural history of human reproduction. Harvard University Press, Cambridge.

    Google Scholar 

  • Ellison PT (2010) Fetal programming and fetal psychology. Infant and Child Development 19:6–20

    Google Scholar 

  • Entringer S, Kumsta R, Hellhammer DH, Wadhwa PD, Wust S (2009) Prenatal exposure to maternal psychosocial stress and HPA axis regulation in young adults. Horm Behav 55(2):292–298

    PubMed  CAS  Google Scholar 

  • Entringer S, Buss C, Shirtcliff EA, Cammack AL, Yim IS, Chicz-DeMet A, Sandman CA, Wadhwa PD (2011) Attenuation of maternal psychophysiological stress responses and the maternal cortisol awakening response over the course of human pregnancy. Stress 13(3):258–268

    Google Scholar 

  • Feldman R, Weller A, Zagoory-Sharon O, Levine A (2007) Evidence for a neuroendocrinological foundation of human affiliation: plasma oxytocin levels across pregnancy and the postpartum period predict mother-infant bonding. Psychol Sci 18(11):965–970

    PubMed  Google Scholar 

  • Fish EW, Shahrokh D, Bagot R, Caldji C, Bredy T, Szyf M, Meaney MJ (2004) Epigenetic programming of stress responses through variations in maternal care. Ann N Y Acad Sci 1036:167–180

    PubMed  Google Scholar 

  • Flinn MV, Nepomnaschy PA, Muehlenbein MP, Ponzi D (2011) Evolutionary functions of early social modulation of hypothalamic-pituitary-adrenal axis development in humans. Neurosci Biobehav Rev 35(7):1611–1629

    PubMed  CAS  Google Scholar 

  • Flykt M, Kanninen K, Sinkonnen J, Punamakki R (2010) Maternal depression and dyadic interaction: the role of maternal attachment style. Infant Child Dev 19(5):530–550

    Google Scholar 

  • Freemark M (1999) The fetal adrenal and the maturation of the growth hormone and prolactin axes. Endocrinology 140(5):1963–1965

    PubMed  CAS  Google Scholar 

  • Galeeva A, Pelto-Huikko M, Pivina S, Ordyan N (2010) Postnatal ontogeny of the glucocorticoid receptor in the hippocampus. Vitam Horm 82:367–389

    PubMed  CAS  Google Scholar 

  • Garbrecht MR, Klein JM, Schmidt TJ, Snyder JM (2006) Glucocorticoid metabolism in the human fetal lung: implications for lung development and the pulmonary surfactant system. Biol Neonate 89(2):109–119

    PubMed  CAS  Google Scholar 

  • Garbrecht MR, Klein JM, McCarthy TA, Schmidt TJ, Krozowski ZS, Snyder JM (2007) 11-Beta hydroxysteroid dehydrogenase type 2 in human adult and fetal lung and its regulation by sex steroids. Pediatr Res 62(1):26–31

    PubMed  CAS  Google Scholar 

  • Gettler LT, McDade TW, Feranil AB, Kuzawa CW (2011) Longitudinal evidence that fatherhood decreases testosterone in human males. Proc Natl Acad Sci USA 108(39):16194–16199

    PubMed  CAS  Google Scholar 

  • Giedd JN, Vaituzis AC, Hamburger SD, Lange N, Rajapakse JC, Kaysen D, Vauss YC, Rapoport JL (1996) Quantitative MRI of the temporal lobe, amygdala, and hippocampus in normal human development: ages 4–18 years. J Comp Neurol 366(2):223–230

    PubMed  CAS  Google Scholar 

  • Giesbrecht GF, Campbell T, Letourneau N, Kooistra L, APrON Study Team (2012) Psychological distress and salivary cortisol covary within persons during pregnancy. Psychoneuroendocrinology 37(2):270–279

    PubMed  CAS  Google Scholar 

  • Glover V, O’Connor TG, O’Donnell K (2010) Prenatal stress and the programming of the HPA axis. Neurosci Biobehav Rev 35(1):17–22

    PubMed  CAS  Google Scholar 

  • Gluckman PD, Hanson MA, Mitchell MD (2010) Developmental origins of health and disease: reducing the burden of chronic disease in the next generation. Genome Med 2(2):14

    PubMed  Google Scholar 

  • Gould SJ, Lewontin RC (1979) The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc R Soc Lond B Biol Sci 205(1161):581–598

    PubMed  CAS  Google Scholar 

  • Groer MW, Davis MW, Hemphill J (2002) Postpartum stress: current concepts and the possible protective role of breastfeeding. J Obstet Gynecol Neonatal Nurs 31(4):411–417

    PubMed  Google Scholar 

  • Groschl M, Rauh M, Dorr HG (2003) Circadian rhythm of salivary cortisol, 17alpha-hydroxyprogesterone, and progesterone in healthy children. Clin Chem 49(10):1688–1691

    PubMed  Google Scholar 

  • Gunnar MR (1998) Quality of early care and buffering of neuroendocrine stress reactions: potential effects on the developing human brain. Prev Med 27(2):208–211

    PubMed  CAS  Google Scholar 

  • Gunnar MR, Donzella B (2002) Social regulation of the cortisol levels in early human development. Psychoneuroendocrinology 27(1–2):199–220

    PubMed  CAS  Google Scholar 

  • Gunnar MR, Brodersen L, Krueger K, Rigatuso J (1996) Dampening of adrenocortical responses during infancy: normative changes and individual differences. Child Dev 67(3):877–889

    PubMed  CAS  Google Scholar 

  • Gurven M, Kaplan H, Supa AZ (2007) Mortality experience of Tsimane Amerindians of Bolivia: regional variation and temporal trends. Am J Hum Biol 19(3):376–398

    PubMed  Google Scholar 

  • Harris A, Seckl J (2010) Glucocorticoids, prenatal stress and the programming of disease. Horm Behav 59(3):279–289

    PubMed  Google Scholar 

  • Hauner KK, Adam EK, Mineka S, Doane LD, DeSantis AS, Zinbarg R, Craske M, Griffith JW (2008) Neuroticism and introversion are associated with salivary cortisol patterns in adolescents. Psychoneuroendocrinology 33(10):1344–1356

    PubMed  CAS  Google Scholar 

  • Heinrichs M, Meinlschmidt G, Neumann I, Wagner S, Kirschbaum C, Ehlert U, Hellhammer DH (2001) Effects of suckling on hypothalamic-pituitary-adrenal axis responses to psychosocial stress in postpartum lactating women. J Clin Endocrinol Metab 86(10):4798–4804

    PubMed  CAS  Google Scholar 

  • Heinrichs M, Baumgartner T, Kirschbaum C, Ehlert U (2003) Social support and oxytocin interact to suppress cortisol and subjective responses to psychosocial stress. Biol Psychiatry 54(12):1389–1398

    PubMed  CAS  Google Scholar 

  • Hench PS, Kendall EC, Slocumb CH, Polley HF (1949a) Adrenocortical hormone in arthritis: preliminary report. Ann Rheum Dis 8(2):97–104

    PubMed  CAS  Google Scholar 

  • Hench PS, Slocumb CH et al (1949b) The effects of the adrenal cortical hormone 17-hydroxy-11-dehydrocorticosterone (Compound E) on the acute phase of rheumatic fever; preliminary report. Mayo Clin Proc 24(11):277–297

    CAS  Google Scholar 

  • Hinde K (2012) Lactational programming of infant behavioral phenotype. In: Clancy KBH, Hinde K, Rutherford JN (eds) Building babies: primate development in proximate and ultimate perspectives. Springer, New York

    Google Scholar 

  • Hinde K, Milligan LA (2011) Primate milk: proximate mechanisms and ultimate perspectives. Evol Anthropol 20(1):9–23

    Google Scholar 

  • Hipwell AE, Goossens FA, Melhuish EC, Kumar R (2000) Severe maternal psychopathology and infant-mother attachment. Dev Psychopathol 12(2):157–175

    PubMed  CAS  Google Scholar 

  • Holmes MC, Sangra M, French KL, Whittle IR, Paterson J, Mullins JJ, Seckl JR (2006) 11beta-Hydroxysteroid dehydrogenase type 2 protects the neonatal cerebellum from deleterious effects of glucocorticoids. Neuroscience 137(3):865–873

    PubMed  CAS  Google Scholar 

  • Hruschka DJ, Kohrt BA, Worthman CM (2005) Estimating between- and within-individual variation in cortisol levels using multilevel models. Psychoneuroendocrinology 30(7):698–714

    PubMed  CAS  Google Scholar 

  • Huanca T (2006) Tsimane’ oral tradition, landscape, and identity in tropical forest

    Google Scholar 

  • Jansen J, Beijers R, Riksen-Walraven M, de Weerth C (2011) Cortisol reactivity in young infants. Psychoneuroendocrinology 35(3):329–338

    Google Scholar 

  • Jessop DS, Turner-Cobb JM (2008) Measurement and meaning of salivary cortisol: a focus on health and disease in children. Stress 11(1):1–14

    PubMed  CAS  Google Scholar 

  • Jones A, Godfrey KM, Wood P, Osmond C, Goulden P, Phillips DI (2006) Fetal growth and the adrenocortical response to psychological stress. J Clin Endocrinol Metab 91(5):1868–1871

    PubMed  CAS  Google Scholar 

  • Kajantie E, Phillips DI, Andersson S, Barker DJ, Dunkel L, Forsen T, Osmond C, Tuominen J, Wood PJ, Eriksson J (2002) Size at birth, gestational age and cortisol secretion in adult life: foetal programming of both hyper- and hypocortisolism? Clin Endocrinol (Oxf) 57(5):635–641

    Google Scholar 

  • Kajantie E, Feldt K, Raikkonen K, Phillips DI, Osmond C, Heinonen K, Pesonen AK, Andersson S, Barker DJ, Eriksson JG (2007) Body size at birth predicts hypothalamic-pituitary-adrenal axis response to psychosocial stress at age 60 to 70 years. J Clin Endocrinol Metab 92(11):4094–4100

    PubMed  CAS  Google Scholar 

  • Kammerer M, Adams D, Castelberg BV, Glover V (2002) Pregnant women become insensitive to cold stress. BMC Pregnancy Childbirth 2(1):8

    PubMed  Google Scholar 

  • Kammerer M, Taylor A, Glover V (2006) The HPA axis and perinatal depression: a hypothesis. Arch Womens Ment Health 9(4):187–196

    PubMed  CAS  Google Scholar 

  • Kapoor A, Dunn E, Kostaki A, Andrews MH, Matthews SG (2006) Fetal programming of hypothalamo-pituitary-adrenal function: prenatal stress and glucocorticoids. J Physiol 572(Pt 1):31–44

    PubMed  CAS  Google Scholar 

  • Kern S, Oakes TR, Stone CK, McAuliff EM, Kirschbaum C, Davidson RJ (2008) Glucose metabolic changes in the prefrontal cortex are associated with HPA axis response to a psychosocial stressor. Psychoneuroendocrinology 33(4):517–529

    PubMed  CAS  Google Scholar 

  • Kirschbaum C, Hellhammer DH (1994) Salivary cortisol in psychoneuroendocrine research: recent developments and applications. Psychoneuroendocrinology 19(4):313–333

    PubMed  CAS  Google Scholar 

  • Kivlighan KT, DiPietro JA, Costigan KA, Laudenslager ML (2008) Diurnal rhythm of cortisol during late pregnancy: associations with maternal psychological well-being and fetal growth. Psychoneuroendocrinology 33(9):1225–1235

    PubMed  CAS  Google Scholar 

  • Kramer KL (2011) The evolution of human parental care and recruitment of juvenile help. Trends Ecol Evol 26(10):533–540

    PubMed  Google Scholar 

  • Kramer MS, Lydon J, Seguin L, Goulet L, Kahn SR, McNamara H, Genest J, Dassa C, Chen MF, Sharma S et al (2009) Stress pathways to spontaneous preterm birth: the role of stressors, psychological distress, and stress hormones. Am J Epidemiol 169(11):1319–1326

    PubMed  Google Scholar 

  • Kulski JK, Hartmann PE (1981) Changes in the concentration of cortisol in milk during different stages of human lactation. Aust J Exp Biol Med Sci 59(Pt 6):769–778

    PubMed  CAS  Google Scholar 

  • Kuzawa CW, Quinn EA (2009) Developmental origins of adult function and health: evolutionary hypotheses. Annu Rev Anthropol 38:131–147

    Google Scholar 

  • Kuzawa CW, Sweet E (2009) Epigenetics and the embodiment of race: developmental origins of US racial disparities in cardiovascular health. Am J Hum Biol 21(1):2–15

    PubMed  Google Scholar 

  • Kuzawa CW, Thayer ZM (2011) Timescales of human adaptation: the role of epigenetic processes. Epigenomics 3(2):221–234

    PubMed  CAS  Google Scholar 

  • Laatikainen TJ, Raisanen IJ, Salminen KR (1988) Corticotropin-releasing hormone in amniotic fluid during gestation and labor and in relation to fetal lung maturation. Am J Obstet Gynecol 159(4):891–895

    PubMed  CAS  Google Scholar 

  • Leigh SR (2004) Brain growth, life history, and cognition in primate and human evolution. Am J Primatol 62(3):139–164

    PubMed  CAS  Google Scholar 

  • Leonard WR, Godoy R (2008) Tsimane’ Amazonian Panel Study (TAPS): the first 5 years (2002–2006) of socioeconomic, demographic, and anthropometric data available to the public. Econ Hum Biol 6(2):299–301

    PubMed  Google Scholar 

  • Levine J, Wolfe LG, Schiebinger RJ, Loriaux DL, Cutler GB Jr (1982) Rapid regression of fetal adrenal zone and absence of adrenal reticular zone in the marmoset. Endocrinology 111(6):1797–1802

    PubMed  CAS  Google Scholar 

  • Levine A, Zagoory-Sharon O, Feldman R, Weller A (2007) Oxytocin during pregnancy and early postpartum: individual patterns and maternal-fetal attachment. Peptides 28(6):1162–1169

    PubMed  CAS  Google Scholar 

  • Liggins GC (1974) Parturition in the sheep and the human. Basic Life Sci 4(Pt B):423–443

    PubMed  CAS  Google Scholar 

  • Liggins GC, Thorburn GD (1994) Initiation of parturition. In: Lamming GE (ed) Marshall’s physiology of reproduction. Chapman and Hall, London, pp 863–1002

    Google Scholar 

  • Lightman SL, Windle RJ, Wood SA, Kershaw YM, Shanks N, Ingram CD (2001) Peripartum plasticity within the hypothalamo-pituitary-adrenal axis. Prog Brain Res 133:111–129

    PubMed  CAS  Google Scholar 

  • Lillycrop KA, Slater-Jefferies JL, Hanson MA, Godfrey KM, Jackson AA, Burdge GC (2007) Induction of altered epigenetic regulation of the hepatic glucocorticoid receptor in the offspring of rats fed a protein-restricted diet during pregnancy suggests that reduced DNA methyltransferase-1 expression is involved in impaired DNA methylation and changes in histone modifications. Br J Nutr 97(6):1064–73

    Google Scholar 

  • Linden W, Earle TL, Gerin W, Christenfeld N (1997) Physiological stress reactivity and recovery: conceptual siblings separated at birth? J Psychosom Res 42(2):117–135

    PubMed  CAS  Google Scholar 

  • Lockwood CJ (2004) The initiation of parturition at term. Obstet Gynecol Clin North Am. 31(4):935–47

    Google Scholar 

  • Lupien SJ, King S, Meaney MJ, McEwen BS (2000) Child’s stress hormone levels correlate with mother’s socioeconomic status and depressive state. Biol Psychiatry 48(10):976–980

    PubMed  CAS  Google Scholar 

  • Lupien SJ, McEwen BS, Gunnar MR, Heim C (2009) Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 10(6):434–445

    PubMed  CAS  Google Scholar 

  • Magiakou MA, Mastorakos G, Webster E, Chrousos GP (1997) The hypothalamic-pituitary-adrenal axis and the female reproductive system. Ann N Y Acad Sci 816:42–56

    PubMed  CAS  Google Scholar 

  • Martin RD (1996) Scaling of the mammalian brain: the maternal energy hypothesis. News Physiol Sci 11:149–156

    Google Scholar 

  • Martin RD (2007) The evolution of human reproduction: a primatological perspective. Am J Phys Anthropol Suppl 45:59–84

    PubMed  Google Scholar 

  • Mastorakos G, Ilias I (2003) Maternal and fetal hypothalamic-pituitary-adrenal axes during pregnancy and postpartum. Ann N Y Acad Sci 997:136–149

    PubMed  CAS  Google Scholar 

  • McEwen BS (1999) Stress and hippocampal plasticity. Annu Rev Neurosci 22:105–122

    PubMed  CAS  Google Scholar 

  • McEwen BS (2009) The brain is the central organ of stress and adaptation. Neuroimage 47(3):911–3

    Google Scholar 

  • McEwen BS, Wingfield JC (2003) The concept of allostasis in biology and biomedicine. Horm Behav 43(1):2–15

    PubMed  Google Scholar 

  • McLean M, Smith R (2001) Corticotropin-releasing hormone and human parturition. Reproduction 121(4):493–501

    PubMed  CAS  Google Scholar 

  • McNamara JP, Harrison JH, Kincaid RL, Waltner SS (1995) Lipid metabolism in adipose tissue of cows fed high fat diets during lactation. J Dairy Sci. 78(12):2782–96

    Google Scholar 

  • Meaney MJ (2010) Epigenetics and the biological definition of gene x environment interactions. Child Dev 81(1):41–79

    PubMed  Google Scholar 

  • Mesiano S, Jaffe RB (1997) Developmental and functional biology of the primate fetal adrenal cortex. Endocr Rev 18(3):378–403

    PubMed  CAS  Google Scholar 

  • Miller G (2010) Epigenetics. The seductive allure of behavioral epigenetics. Science 329(5987):24–27

    PubMed  CAS  Google Scholar 

  • Miller GE, Cohen S, Ritchey AK (2002) Chronic psychological stress and the regulation of pro-inflammatory cytokines: a glucocorticoid-resistance model. Health Psychol 21(6):531–541

    PubMed  Google Scholar 

  • Miller G, Chen E, Cole SW (2009) Health psychology: developing biologically plausible models linking the social world and physical health. Annu Rev Psychol 60:501–524

    PubMed  Google Scholar 

  • Nepomnaschy PA, Welch KB, McConnell DS, Low BS, Strassmann BI, England BG (2006) Cortisol levels and very early pregnancy loss in humans. Proc Natl Acad Sci USA 103(10):3938–3942

    PubMed  CAS  Google Scholar 

  • Neumann ID (2001) Alterations in behavioral and neuroendocrine stress coping strategies in pregnant, parturient and lactating rats. Prog Brain Res 133:143–152

    PubMed  CAS  Google Scholar 

  • Nguyen AD, Mapes SM, Corbin CJ, Conley AJ (2008) Morphological adrenarche in rhesus macaques: development of the zona reticularis is concurrent with fetal zone regression in the early neonatal period. J Endocrinol 199(3):367–378

    PubMed  CAS  Google Scholar 

  • Nyberg CH (2009) Market integration, stress, and health: an exploration of hypothalamic-pituitary-adrenal axis dynamics among the Tsimane’ of the Bolivian Amazon. Dissertation. Northwestern University, 339 pp

    Google Scholar 

  • Nyberg CH (2012) Diurnal cortisol rhythms in Tsimane’ Amazonian foragers: new insights into ecological HPA axis research. Psychoneuroendocrinology 37(2):178–190

    PubMed  CAS  Google Scholar 

  • Nyberg CH (in preparation) HPA activity in pregnant and lactating Tsimane’ women

    Google Scholar 

  • Oates M, Woodside B, Walker CD (2000) Chronic leptin administration in developing rats reduces stress responsiveness partly through changes in maternal behavior. Horm Behav 37(4):366–376

    PubMed  CAS  Google Scholar 

  • Obel C, Hedegaard M, Henriksen TB, Secher NJ, Olsen J, Levine S (2005) Stress and salivary cortisol during pregnancy. Psychoneuroendocrinology 30(7):647–656

    PubMed  CAS  Google Scholar 

  • Oberlander TF, Weinberg J, Papsdorf M, Grunau R, Misri S, Devlin AM (2008) Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics 3(2):97–106

    PubMed  Google Scholar 

  • O’Donnell K, O’Connor TG, Glover V (2009) Prenatal stress and neurodevelopment of the child: focus on the HPA axis and role of the placenta. Dev Neurosci 31(4):285–292

    PubMed  Google Scholar 

  • O’Keane V, Lightman S, Marsh M, Pawlby S, Papadopoulos AS, Taylor A, Moore R, Patrick K (2011) Increased pituitary-adrenal activation and shortened gestation in a sample of depressed pregnant women: a pilot study. J Affect Disord 130(1–2):300–5

    Google Scholar 

  • Paulson JF, Dauber S, Leiferman JA (2006) Individual and combined effects of postpartum depression in mothers and fathers on parenting behavior. Pediatrics 118(2):659–668

    PubMed  Google Scholar 

  • Pepe GJ, Albrecht ED (1990) Regulation of the primate fetal adrenal cortex. Endocr Rev 11(1):151–176

    PubMed  CAS  Google Scholar 

  • Petherick A (2010) Development: mother’s milk: a rich opportunity. Nature 468(7327):S5–S7

    PubMed  CAS  Google Scholar 

  • Phillips DI (2007) Programming of the stress response: a fundamental mechanism underlying the long-term effects of the fetal environment? J Intern Med 261(5):453–460

    PubMed  CAS  Google Scholar 

  • Pike IL (2005) Maternal stress and fetal responses: evolutionary perspectives on preterm delivery. Am J Hum Biol 17(1):55–65

    PubMed  Google Scholar 

  • Power ML, Schulkin J (2006) Functions of corticotropin-releasing hormone in anthropoid primates: from brain to placenta. Am J Hum Biol 18(4):431–447

    PubMed  Google Scholar 

  • Pruessner JC, Dedovic K, Pruessner M, Lord C, Buss C, Collins L, Dagher A, Lupien SJ (2010) Stress regulation in the central nervous system: evidence from structural and functional neuroimaging studies in human populations - 2008 Curt Richter Award Winner. Psychoneuroendocrinology 35(1):179–191

    PubMed  Google Scholar 

  • Quesnell RR, Han X, Schultz BD (2007) Glucocorticoids stimulate ENaC upregulation in bovine mammary epithelium. Am J Physiol Cell Physiol 292(5):C1739–45

    Google Scholar 

  • Rebuffé-Scrive M, Enk L, Crona N, Lönnroth P, Abrahamsson L, Smith U, Björntorp P (1985) Fat cell metabolism in different regions in women. Effect of menstrual cycle, pregnancy, and lactation. J Clin Invest 75(6):1973–6

    Google Scholar 

  • Reck C, Hunt A, Fuchs T, Weiss R, Noon A, Moehler E, Downing G, Tronick EZ, Mundt C (2004) Interactive regulation of affect in postpartum depressed mothers and their infants: an overview. Psychopathology 37(6):272–280

    PubMed  Google Scholar 

  • Roberts D, Dalziel S (2006a) Antenatal corticosteroids for accelerating fetal lung maturation for women at risk of preterm birth. Cochrane Database Syst Rev 3:CD004454

    PubMed  Google Scholar 

  • Roberts D, Dalziel S (2006b) Antenatal corticosteroids for accelerating fetal lung maturation for women at risk of preterm birth. Cochrane Database Syst Rev 3:CD004454

    PubMed  Google Scholar 

  • Romero LM, Dickens MJ, Cyr NE (2009) The Reactive Scope Model—a new model integrating homeostasis, allostasis, and stress. Horm Behav 55(3):375–389

    PubMed  Google Scholar 

  • Rosenberg KR, Trevathan WR (2001) The evolution of human birth. Sci Am 285(5):72–77

    PubMed  CAS  Google Scholar 

  • Roth TL, David SJ (2011) Annual research review: Epigenetic mechanisms and environmental shaping of the brain during sensitive periods of development. J Child Psychol Psychiatry 52(4):398–408

    PubMed  Google Scholar 

  • Russell JA, Douglas AJ, Ingram CD (2001) Brain preparations for maternity–adaptive changes in behavioral and neuroendocrine systems during pregnancy and lactation. An overview. Prog Brain Res 133:1–38

    PubMed  CAS  Google Scholar 

  • Rutherford JN (2009) Fetal signaling through placental structure and endocrine function: illustrations and implications from a nonhuman primate model. Am J Hum Biol 21(6):745–753

    PubMed  Google Scholar 

  • Rutherford JN (2012) The primate placenta as an agent of developmental and health trajectories across the lifecourse. In: Clancy KBH, Hinde K, Rutherford JN (eds) Building babies: primate development in proximate and ultimate perspectives. Springer, New York

    Google Scholar 

  • Sapolsky RM (2003) Stress and plasticity in the limbic system. Neurochem Res 28(11):1735–1742

    PubMed  CAS  Google Scholar 

  • Schulkin J (2003) Allostasis: a neural behavioral perspective. Horm Behav 43(1):21–27 (discussion 28–30)

    PubMed  Google Scholar 

  • Schulkin J, Schmidt L, Erickson E (2005) Glucocorticoids facilitation of corticotropin-releasing hormone in the placenta and brain: functional impact on birth and behavior. In: Power ML, Schulkin J (eds) Birth, distress, and disease: placenta-brain interactions. Cambridge University Press, Cambridge, pp 235–268

    Google Scholar 

  • Schulte HM, Weisner D, Allolio B (1990) The corticotropin releasing hormone test in late pregnancy: lack of adrenocorticotropin and cortisol response. Clin Endocrinol (Oxf) 33(1):99–106

    CAS  Google Scholar 

  • Seckl JR (2004) Prenatal glucocorticoids and long-term programming. Eur J Endocrinol 151(Suppl 3):U49–U62

    PubMed  CAS  Google Scholar 

  • Seckl JR, Holmes MC (2007) Mechanisms of disease: glucocorticoids, their placental metabolism and fetal ‘programming’ of adult pathophysiology. Nat Clin Pract Endocrinol Metab 3(6):479–488

    PubMed  CAS  Google Scholar 

  • Seckl JR, Meaney MJ (2004) Glucocorticoid programming. Ann N Y Acad Sci 1032:63–84

    PubMed  CAS  Google Scholar 

  • Seyle H (1956) The stress of life. McGraw-Hill, New York. 324p.

    Google Scholar 

  • Sloboda D, Moss TJ, Newnham J, Challis JR (2005) Fetal HPA activation, preterm birth, and postnatal programming. In: Power ML, Schulkin J (eds) Birth, distress, and disease: placenta-brain interactions. Cambridge, Cambridge

    Google Scholar 

  • Sloboda DM, Beedle AS, Cupido CL, Gluckman PD, Vickers MH (2009) Impaired perinatal growth and longevity: a life history perspective. Curr Gerontol Geriatr Res:608740

    Google Scholar 

  • Sloboda DM, Howie GJ, Pleasants A, Gluckman PD, Vickers MH (2009b) Pre- and postnatal nutritional histories influence reproductive maturation and ovarian function in the rat. PLoS One 4(8):e6744

    PubMed  Google Scholar 

  • Smith R, Nicholson RC (2007) Corticotrophin releasing hormone and the timing of birth. Front Biosci 12:912–918

    PubMed  CAS  Google Scholar 

  • Smith R, Wickings EJ, Bowman ME, Belleoud A, Dubreuil G, Davies JJ, Madsen G (1999) Corticotropin-releasing hormone in chimpanzee and gorilla pregnancies. J Clin Endocrinol Metab 84(8):2820–2825

    PubMed  CAS  Google Scholar 

  • Sterling R, Eyer J (1988) Allostasis: a new paradigm to explain arousal pathology. In: Fisher S, Reason J (eds) Handbook of life stress, cognition, and health. Wiley, New York, pp 629–649

    Google Scholar 

  • Stetler C, Miller GE (2005) Blunted cortisol response to awakening in mild to moderate depression: regulatory influences of sleep patterns and social contacts. J Abnorm Psychol 114(4):697–705

    PubMed  Google Scholar 

  • Stetler C, Dickerson SS, Miller GG (2004) Uncoupling of social zeitgebers and diurnal cortisol secretion in clinical depression. Psychoneuroendocrinology 29(10):1250–1259

    PubMed  CAS  Google Scholar 

  • Sullivan EC, Hinde K, Mendoza SP, Capitanio JP (2011) Cortisol concentrations in the milk of rhesus monkey mothers are associated with confident temperament in sons, but not daughters. Dev Psychobiol 53(1):96–104

    PubMed  CAS  Google Scholar 

  • Sun K, Adamson SL, Yang K, Challis JR (1999) Interconversion of cortisol and cortisone by 11beta-hydroxysteroid dehydrogenases type 1 and 2 in the perfused human placenta. Placenta 20(1):13–19

    PubMed  Google Scholar 

  • Szyf M, Weaver IC, Champagne FA, Diorio J, Meaney MJ (2005) Maternal programming of steroid receptor expression and phenotype through DNA methylation in the rat. Front Neuroendocrinol 26(3–4):139–162

    PubMed  CAS  Google Scholar 

  • Taylor A (2011) The endocrinology of pregnancy. In: Greenspan F, Baxter D (eds) Basic and clinical endocrinology. Prentice Hall, Hartford, pp 575–602

    Google Scholar 

  • Thayer Z, Kuzawa C (2012) Diurnal cortisol profiles in pregnancy: evidence for interpopulation variation (in preparation)

    Google Scholar 

  • Tottenham N, Sheridan MA (2009) A review of adversity, the amygdala and the hippocampus: a consideration of developmental timing. Front Hum Neurosci 3:68

    Google Scholar 

  • Tronick E, Reck C (2009) Infants of depressed mothers. Harv Rev Psychiatry 17(2):147–156

    PubMed  Google Scholar 

  • Tu MT, Lupien SJ, Walker CD (2006) Diurnal salivary cortisol levels in postpartum mothers as a function of infant feeding choice and parity. Psychoneuroendocrinology 31(7):812–824

    PubMed  CAS  Google Scholar 

  • Vieau D, Sebaai N, Leonhardt M, Dutriez-Casteloot I, Molendi-Coste O, Laborie C, Breton C, Deloof S, Lesage J (2007) HPA axis programming by maternal undernutrition in the male rat offspring. Psychoneuroendocrinology 32(Suppl 1):S16–S20

    PubMed  CAS  Google Scholar 

  • Wadhwa PD (2005) Psychoneuroendocrine processes in human pregnancy influence fetal development and health. Psychoneuroendocrinology 30(8):724–743

    PubMed  CAS  Google Scholar 

  • Wadhwa PD, Buss C, Entringer S, Swanson JM (2009) Developmental origins of health and disease: brief history of the approach and current focus on epigenetic mechanisms. Semin Reprod Med 27(5):358–368

    PubMed  CAS  Google Scholar 

  • Walker CD, Naef L, d’Asti E, Long H, Xu Z, Moreau A, Azeddine B (2008a) Perinatal maternal fat intake affects metabolism and hippocampal function in the offspring: a potential role for leptin. Ann N Y Acad Sci 1144:189–202

    PubMed  Google Scholar 

  • Walker CD (2010) Maternal touch and feed as critical regulators of behavioral and stress responses in the offspring. Dev Psychobiol 52(7):638–650

    PubMed  Google Scholar 

  • Weaver IC, Cervoni N, Champagne FA, D’Alessio AC, Sharma S, Seckl JR, Dymov S, Szyf M, Meaney MJ (2004) Epigenetic programming by maternal behavior. Nat Neurosci 7(8):847–854

    PubMed  CAS  Google Scholar 

  • Weinberg MK, Tronick EZ (1998) Emotional characteristics of infants associated with maternal depression and anxiety. Pediatrics 102(5 Suppl E):1298–1304

    PubMed  CAS  Google Scholar 

  • Windle RJ, Kershaw YM, Shanks N, Wood SA, Lightman SL, Ingram CD (2004) Oxytocin attenuates stress-induced c-fos mRNA expression in specific forebrain regions associated with modulation of hypothalamo-pituitary-adrenal activity. J Neurosci 24(12):2974–2982

    PubMed  CAS  Google Scholar 

  • Windle RJ, Wood SA, Kershaw YM, Lightman SL, Ingram CD (2011) Reduced stress responsiveness in pregnancy: relationship with pattern of forebrain c-fos mRNA expression. Brain Res 1358:102–109

    Google Scholar 

  • Worthman CM, Kuzara J (2005) Life history and the early origins of health differentials. Am J Hum Biol 17(1):95–112

    PubMed  Google Scholar 

  • Wust S, Entringer S, Federenko IS, Schlotz W, Hellhammer DH (2005) Birth weight is associated with salivary cortisol responses to psychosocial stress in adult life. Psychoneuroendocrinology 30(6):591–598

    PubMed  Google Scholar 

  • Young EA, Vazquez D (1996) Hypercortisolemia, hippocampal glucocorticoid receptors, and fast feedback. Mol Psychiatry 1(2):149–159

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anthropology, University of Massachusetts Boston, 100 Morrissey Boulevard, Boston, MA, 02125, USA

    Colleen H. Nyberg

Authors
  1. Colleen H. Nyberg
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Colleen H. Nyberg .

Editor information

Editors and Affiliations

  1. , Department of Anthropology, University of Illinois, 109 Davenport Hall, M/C 148, Urbana, 61801, Illinois, USA

    Kathryn B.H. Clancy

  2. , Department of HUman Evolutionary Biology, Harvard University, 11 Divinity Ave, Cambridge, 02138, Massachusetts, USA

    Katie Hinde

  3. , Comparative Primate Biology Laboratory, University of Illinois at Chicago, Chicago, 60612, Illinois, USA

    Julienne N. Rutherford

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Science+Business Media New York

About this chapter

Cite this chapter

Nyberg, C.H. (2013). Navigating Transitions in Hypothalamic–Pituitary–Adrenal Function from Pregnancy Through Lactation: Implications for Maternal Health and Infant Brain Development. In: Clancy, K., Hinde, K., Rutherford, J. (eds) Building Babies. Developments in Primatology: Progress and Prospects, vol 37. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-4060-4_6

Download citation

Publish with us

Policies and ethics

Search

Navigation