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Ontogeny of Stress Reactivity in the Human Child: Phenotypic Flexibility, Trade-Offs, and Pathology

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Adaptive and Maladaptive Aspects of Developmental Stress

Part of the book series: Current Topics in Neurotoxicity ((Current Topics Neurotoxicity,volume 3))

Abstract

We humans are highly sensitive to our social environments. Our brains have special abilities such as empathy and social foresight that allow us to understand each other’s feelings and communicate in ways that are unique among all living organisms. Our extraordinary social minds, however, come with some significant strings attached. Our emotional states can be strongly influenced by what others say and do. Our hearts can soar, but they also can be broken. Our bodies use internal chemical messengers—hormones and neurotransmitters—to help guide responses to our social worlds. From romantic daydreams to jealous rage, from orgasm to lactation and parent–child bonding, the powerful molecules produced and released by tiny and otherwise seemingly insignificant cells and glands help orchestrate our thoughts and actions. Understanding this chemical language is important for many research questions in human health. Here we focus on the question of why social relationships can affect health—why it is that words can hurt children. Stress hormones appear to play important roles in this puzzle.

The hypothalamic–pituitary–adrenal axis (HPAA) is highly responsive to traumatic experiences including social challenges. For the past 23 years we have conducted a field study of child stress and family environment in a rural community in Dominica. The primary objective is to document hormonal responses of children to everyday interactions with their parents and other care providers, concomitant with longitudinal assessment of developmental and health outcomes. Results indicate that difficult family environments and traumatic social events are associated with temporal elevations of cortisol and elevated morbidity. The long-term effects of traumatic early experiences on cortisol profiles are complex and indicate domain-­specific effects, with normal recovery from physical stressors, but some heightened response to negative-affect social challenges. These results are consistent with the hypothesis that developmental programming of the HPAA and other neuroendocrine systems associated with stress responses may facilitate cognitive targeting to salient social challenges in specific environmental contexts.

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References

  • Ademec RE, Blundell J, Burton P (2005) Neural circuit changes mediating lasting brain and behavioral response to predator stress. Neurosci Biobehav Rev 29:1225–1241

    PubMed  CAS  Google Scholar 

  • Adolphs R (2003) Cognitive neuroscience of human social behavior. Nat Rev Neurosci 4:165–179

    PubMed  CAS  Google Scholar 

  • Agrawal AA (2001) Phenotypic plasticity in the interactions and evolution of species. Science 294:321–326

    PubMed  CAS  Google Scholar 

  • Agrawal AA (2007) Macroevolution of plant defense strategies. Trends Ecol Evol 22(2):103–109. doi:10.1016/j.tree.2006.10.012

    PubMed  CAS  Google Scholar 

  • Agrawal AA, Laforsch C, Tollrian R (1999) Transgenerational induction of defences in animals and plants. Nature 401(6748):60–63

    PubMed  CAS  Google Scholar 

  • Alexander RD (1990) How did humans evolve? Special Publication No. 1. Museum of Zoology, The University of Michigan, Ann Arbor

    Google Scholar 

  • Allman J (1999) Evolving brains. Scientific American Library, New York

    Google Scholar 

  • Amaral DG (2003) The amygdala, social behavior, and danger detection. Ann N Y Acad Sci 1000:337–347

    Google Scholar 

  • Amodio DM, Frith CD (2006) Meeting of minds: the medial frontal cortex and social cognition. Nat Rev Neurosci 7(4):268–277

    Google Scholar 

  • Anderson S, Lyss P, Dumont PN, Teicher M (1999) Enduring neurochemical effects of early maternal separation on limbic structures. Ann N Y Acad Sci 877:756–759

    Google Scholar 

  • Ashman S, Dawson G, Panagiotides H, Yamada E, Wilkinson C (2002) Stress hormone levels of children of depressed mothers. Dev Psychopathol 14:333–349

    PubMed  Google Scholar 

  • Baron-Cohen S (1995) Mindblindness: an essay on autism and theory of mind. MIT Press/Bradford Books, Boston

    Google Scholar 

  • Battaglia M, Ogliari A, Zanoni A, Villa F, Citterio A, Binaghi F et al (2004) Children’s discrimination of expressions of emotion: relationship with indices of social anxiety and shyness. J Am Acad Child Adolesc Psychiatry 43:358–365

    Google Scholar 

  • Berman CM (1996) An animal model for the intergenerational transmission of maternal style? Fam Syst 3:125–140

    Google Scholar 

  • Bogin B (1999) Patterns of human growth, 2nd edn. Cambridge University Press, Cambridge

    Google Scholar 

  • Brand S, Wilhelm FH, Kossowsky J, Holsboer-Trachsler E, Schneider S (2011) Children suffering from separation anxiety disorder (SAD) show increased HPA axis activity compared to healthy controls. J Psychiatr Res 45:452–459

    PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Brunson K, Sarit Avishai-Eliner S, Hatalski C, Baram T (2001) Neurobiology of the stress response early in life: evolution of a concept and the role of corticotropin releasing hormone. Mol Psychiatry 6:647–656

    PubMed  CAS  Google Scholar 

  • Bugental DB (2000) Acquisition of the algorithms of social life: a domain-based approach. Psychol Bull 126:187–219

    PubMed  CAS  Google Scholar 

  • Byrne G, Suomi S (2002) Cortisol reactivity and its relation to homecage behavior and personality ratings in tufted capuchin (Cebus paella) juveniles from birth to six years of age. Psychoneuroendocrinology 27:139–154

    PubMed  CAS  Google Scholar 

  • Caldji C, Tannenbaum B, Sharma S, Francis D, Plotsky P, Meaney MJ (1998) Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Neurobiology 95:5335–5340

    CAS  Google Scholar 

  • Carter CS (2005) Biological perspectives on social attachment and bonding. In: Carter CS et al (eds) Attachment and bonding: a new synthesis. The MIT Press, Cambridge

    Google Scholar 

  • Champagne F (2008) Epigenetic mechanisms and the transgenerational effects of maternal care. Front Neuroendocrinol 29:386–397

    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 

  • Champagne F, Meaney MJ (2006) Stress during gestation alters postpartum maternal care and the development of the offspring in a rodent model. Biol Psychiatry 59:1227–1235

    PubMed  CAS  Google Scholar 

  • Clarke AS, Schneider M (1993) Prenatal stress has long-term effects on behavioral responses to stress in juvenile rhesus monkeys. Dev Psychobiol 26:293–304

    PubMed  CAS  Google Scholar 

  • Clarke AS, Wittwer D, Abbott D, Schneider M (1994) Long-term effects of prenatal stress on HPA activity in juvenile rhesus monkeys. Dev Psychobiol 27:257–269

    PubMed  CAS  Google Scholar 

  • Coplan J, Trost R, Owens M, Cooper T, Gorman J, Nemeroff C, Rosenblum L (1998) Cerebrospinal fluid concentrations of somatostatin and biogenic amines in grown primates reared by mothers exposed to manipulated foraging conditions. Arch Gen Psychiatry 55:473–477

    PubMed  CAS  Google Scholar 

  • D’Amato FR, Ammassari-Teule M, Oliverio A (1988) Prenatal antagonism of stress by naltexone administration: early and long-lasting effects on emotional behaviors in mice. Dev Psychobiol 21:283–292

    PubMed  Google Scholar 

  • Deater-Deckard K, Atzaba-Poria N, Pike A (2004) Mother- and father-child mutuality in Anglo and Indian British families: a link with lower externalizing behaviors. J Abnorm Child Psychol 32(6):609–620

    PubMed  Google Scholar 

  • Del Giudice M (2012) Fetal programming by maternal stress: insights from a conflict perspective. Psychoneuroendocrinology 37:1614–1629

    PubMed  Google Scholar 

  • Dickerson SS, Kemeny ME (2004) Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychol Bull 130:355–391

    PubMed  Google Scholar 

  • Dunbar RIM (1997) Gossip, grooming, and evolution of language. Harvard University Press, Cambridge, MA

    Google Scholar 

  • Dunbar RIM, Schultz S (2007) Evolution in the social brain. Science 317:1344–1347

    Google Scholar 

  • Essex M, Klein M, Cho E, Kalin N (2002) Maternal stress beginning in infancy may sensitize children to later stress exposure: effects on cortisol and behavior. Biol Psychiatry 52:776–784

    PubMed  CAS  Google Scholar 

  • Essex MJ, Boyce WT, Hertzman C, Lam LL, Armstrong JM, Neumann SMA, Kobor MS (2012) Epigenetic vestiges of early developmental adversity: childhood stress exposure and DNA methylation in adolescence. Child Dev, published online: 1 SEP 2011. doi:10.1111/j.1467-8624.2011.01641

  • Fairbanks L (1989) Early experience and cross-generational continuity of mother-infant contact in vervet monkeys. Dev Psychobiol 22:669–681

    PubMed  CAS  Google Scholar 

  • Fairbanks L, McGuire M (1988) Long-term effects of early mothering behavior on responsiveness to the environment in vervet monkeys. Dev Psychobiol 21:711–724

    PubMed  CAS  Google Scholar 

  • Feldman R, Gordon I, Zagoory-Sharon O (2011) Maternal and paternal plasma, salivary, and urinary oxytocin and parent–infant synchrony: considering stress and affiliation components of human bonding. Dev Sci 14(4):752–761. doi:10.1111/j.1467-7687.2010.01021.x

    PubMed  CAS  Google Scholar 

  • Feldman R, Zagoory-Sharon O, Weisman O, Schneiderman I, Gordon I, Maoz R, Shalev I, Ebstein RP (2012) Sensitive parenting is associated with plasma oxytocin and polymorphisms in the OXTR and CD38 genes. Biol Psychiatry 72:175–181. doi:10.1016/j.biopsych.2011.12.025

    PubMed  CAS  Google Scholar 

  • Felitti VJ, Anda RF, Nordenberg D, Williamson DF, Spitz AM et al (1998) Relationship of childhood abuse and household dysfunction to many of the leading causes of death in adults—The Adverse Childhood Experiences (ACE) Study. Am J Prev Med 14:245–258

    PubMed  CAS  Google Scholar 

  • Fleming A (2005) Plasticity of innate behavior: experiences throughout life affect maternal behavior and its neurobiology. In: Carter CS et al (eds) Attachment and bonding: a new synthesis. The MIT Press, Cambridge

    Google Scholar 

  • Fleming A, O’Day D, Kraemer GW (1999) Neurobiology of mother-infant interactions: ­experience and central nervous system plasticity across development and generations. Neurosci Biobehav Rev 23:673–685

    PubMed  CAS  Google Scholar 

  • Flinn MV (1999) Family environment, stress, and health during childhood. In: Panter-Brick C, Worthman C (eds) Health, hormones, and behavior. Cambridge University Press, Cambridge

    Google Scholar 

  • Flinn MV (2004) Culture and developmental plasticity: evolution of the social brain. In: MacDonald K, Burgess RL (eds) Evolutionary perspectives on child development. Sage, Thousand Oaks, CA

    Google Scholar 

  • Flinn MV (2006a) Evolution and ontogeny of stress response to social challenge in the human child. Dev Rev 26:138–174

    Google Scholar 

  • Flinn MV (2006b) Evolution of stress response to social-evaluative threat. In: Barrett L, Dunbar R (eds) Oxford handbook of evolutionary psychology. Oxford University Press, Oxford

    Google Scholar 

  • Flinn MV (2006c) Cross-cultural universals and variations: the evolutionary paradox of informational novelty. Psychol Inq 17(2):118–123

    Google Scholar 

  • Flinn MV (2007) Social relationships and health. In: Trevathan W, Smith EO, McKenna J (eds) Evolutionary medicine & health. Oxford University Press, Oxford

    Google Scholar 

  • Flinn MV (2011) Evolutionary anthropology of the human family. In: Salmon C, Shackleford T (eds) Oxford handbook of evolutionary family psychology, (chapter 2). Oxford University Press, Oxford, pp 12–32

    Google Scholar 

  • Flinn MV, Alexander RD (2007) Runaway social selection. In: Gangestad SW, Simpson JA (eds) The evolution of mind. Guilford Press, New York

    Google Scholar 

  • Flinn MV, Coe MK (2007) The linked red queens of human cognition, reciprocity, and culture. In: Gangestad SW, Simpson JA (eds) The evolution of mind. Guilford Press, New York

    Google Scholar 

  • Flinn MV, England B (1997) Social economics of childhood glucocorticoid stress response and health. Am J Phys Anthropol 102:33–53

    PubMed  CAS  Google Scholar 

  • Flinn MV, England BG (2003) Childhood stress: endocrine and immune responses to psychosocial events. In: Wilce JM (ed) Social & cultural lives of immune systems. Routledge Press, London, pp 107–147

    PubMed  CAS  Google Scholar 

  • Flinn MV, Leone DV (2006) Early trauma and the ontogeny of glucocorticoid stress response in the human child: grandmother as a secure base. J Dev Processes 1(1):31–68

    Google Scholar 

  • Flinn MV, Leone DV (2009) Alloparental care and the ontogeny of glucocorticoid stress response among stepchildren. In: Bentley G, Mace R (eds) Alloparental care in human societies. Biosocial Society Symposium Series. Berghahn Books, Oxford

    Google Scholar 

  • Flinn MV, Ward CV (2005) Evolution of the social child. In: Ellis B, Bjorklund D (eds) Origins of the social mind: evolutionary psychology and child development. Guilford Press, London

    Google Scholar 

  • Flinn MV, Quinlan RJ, Turner MT, Decker SA, England BG (1996) Male–female differences in effects of parental absence on glucocorticoid stress response. Hum Nat 7:125–162

    Google Scholar 

  • Flinn MV, Geary D, Ward CV (2005a) Ecological dominance, social competition, and coalitionary arms races: why humans evolved extraordinary intelligence. Evol Hum Behav 26:10–46

    Google Scholar 

  • Flinn MV, Ward CV, Noone R (2005b) Hormones and the human family. In: Buss D (ed) Handbook of evolutionary psychology. Wiley, New York

    Google Scholar 

  • Flinn MV, Quinlan R, Ward CV, Coe MK (2007) Evolution of the human family: cooperative males, long social childhoods, smart mothers, and extended kin networks. In: Salmon C, Shackelford T (eds) Evolutionary family psychology. Oxford University Press, Oxford

    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 35:1611–1629

    PubMed  CAS  Google Scholar 

  • Flinn MV, Duncan C, Quinlan RL, Leone DV, Decker SA, Ponzi D (2012a) Hormones in the wild: monitoring the endocrinology of family relationships. Parent Sci Pract 12(2):124–133. doi:10.1080/15295192.2012.683338

    Google Scholar 

  • Flinn MV, Ponzi D, Muehlenbein MP (2012b) Hormonal mechanisms for regulation of aggression in human coalitions. Hum Nat 22(1):68–88. doi:10.1007/s12110-012-9135-y

    Google Scholar 

  • Fox S, Levitt P, Nelson CA (2010) How the timing and quality of early experiences influence the development of brain architecture. Child Dev 81:28–40

    PubMed  CAS  Google Scholar 

  • Francis D, Meaney M (2002) Maternal care and the development of stress responses. In: Cacioppo J et al (eds) Foundations in social neuroscience. The MIT Press, Cambridge, MA

    Google Scholar 

  • Francis D, Diorio J, Liu D, Meaney MJ (1999) Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286:1155–1158

    PubMed  CAS  Google Scholar 

  • Francis D, Diorio J, Plotsky P, Meaney M (2002) Environmental enrichment reverses the effects of maternal separation on stress reactivity. J Neurosci 22:7840–7843

    PubMed  CAS  Google Scholar 

  • Fride E, Weinstock M (1988) Prenatal stress increases anxiety-related behavior and alters cerebral laterization of dopamine activity. Life Sci 42:1059–1065

    PubMed  CAS  Google Scholar 

  • Fride E, Dan Y, Gavish M, Weinstock M (1985) Prenatal stress impairs maternal behavior in a conflict situation and reduces hippocampal benzodiazepine receptors. Life Sci 36:2103–2109

    PubMed  CAS  Google Scholar 

  • Gallese V, Keysers C, Rizzolatti G (2004) A unifying view of the basis of social cognition. Trends Cogn Sci 8:396–403

    Google Scholar 

  • Geary D, Flinn MV (2001) Evolution of human parental behavior and the human family. Parent Pract Sci 1:5–61

    Google Scholar 

  • Gilbert P (2001) Evolutionary approaches to psychopathology: the role of natural defences. Aust N Z J Psychiatry 35:17–27

    Google Scholar 

  • Gilbert P (2005) Social mentalities: a biopsychosocial and evolutionary approach to social relationships. In: Baldwin MW (ed) Interpersonal cognition. Guilford, New York, pp 299–333

    Google Scholar 

  • Glover V (2011) Prenatal stress and the origins of psychopathology: an evolutionary perspective. J Child Psychol Psychiatry 52:356–367

    PubMed  Google Scholar 

  • Glover V, O’Connor T (2002) Effects of antenatal stress and anxiety: implications for development and psychiatry. Br J Psychiatry 180:389–391

    PubMed  Google Scholar 

  • Gluckman PD, Hanson MA (2006) Developmental origins of health and disease. Cambridge University Press, Cambridge

    PubMed  Google Scholar 

  • Gopnik A, Meltzoff AN, Kuhl PK (1999) The scientist in the crib: minds, brains, and how children learn. William Morrow & Co., New York

    PubMed  Google Scholar 

  • Grimm V, Frieder B (1987) The effects of mild maternal stress during pregnancy on the behavior of rat pups. Int J Neurosci 35:65–72

    PubMed  CAS  Google Scholar 

  • Grossman A, Churchill J, McKinney B, Kodish I, Otte S, Greenough W (2003) Experience effects on brain development: possible contributions to psychopathology. J Child Psychol Psychiatry 44:33–63

    PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Halligan S, Herbert J, Goodyer I, Murray L (2004) Exposure to postnatal depression predicts elevated cortisol in adolescent offspring. Biol Psychiatry 55:376–381

    PubMed  CAS  Google Scholar 

  • Hanazato T (1990) Induction of helmet development by a Chaoborus factor in Daphnia ambigua during juvenile stages. J Plankton Res 12:1287–1294

    PubMed  CAS  Google Scholar 

  • Harkness K, Monroe S (2002) Childhood adversity and the endogenous versus nonendogenous distinction in women with major depression. Am J Psychiatry 159:387–393

    PubMed  Google Scholar 

  • Harkonmaki K, Korkeila K, Vahtera J, Kivimaki M, Suominen S et al (2007) Childhood adversities as a predictor of disability retirement. J Epidemiol Community Health 61:479–484

    PubMed  Google Scholar 

  • Hatzinger M, Brand S, Perren S, von Wyl A, Standelmann S et al (2012) Pre-schoolers suffering from psychiatric disorders show increased cortisol secretion and poor sleep compared to healthy controls. J Psychiatr Res 46(5):590–599

    PubMed  Google Scholar 

  • Heim C, Nemeroff C (2001) The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol Psychiatry 49:1023–1039

    PubMed  CAS  Google Scholar 

  • Heim C, Newport D, Wagner D, Wilcox M, Miller A, Nemeroff C (2002) The role of early adverse experience and adulthood stress in the prediction of neuroendocrine stress reactivity in women: a multiple regression analysis. Depress Anxiety 15:117–125

    PubMed  Google Scholar 

  • Hess NH, Hagen EH (2006) Sex differences in indirect aggression: psychological evidence from young adults. Evol Hum Behav 27:231–245

    PubMed  CAS  Google Scholar 

  • Hrdy SB (2005) Evolutionary context of human development: the cooperative breeding model. In: Carter CS, Ahnert L (Eds.) Attachment and bonding: a new synthesis. Dahlem Workshop 92. MIT Press, Cambridge, MA

    PubMed  CAS  Google Scholar 

  • Hucklebridge F, Hussain T, Evans P, Clow A (2005) The diurnal patterns of the adrenal steroids cortisol and dehydroepiandrosterone (DHEA) in relation to awakening. Psychoneuroendocrinology 30:51–57

    PubMed  CAS  Google Scholar 

  • Huether G (1996) The central adaptation syndrome: psychosocial stress as a trigger for adaptive modifications of brain structure and brain function. Prog Neurobiol 48:569–612

    PubMed  CAS  Google Scholar 

  • Huether G (1998) Stress and the adaptive self organization of neuronal connectivity during early childhood. Int J Dev Neurosci 16:297–306

    PubMed  CAS  Google Scholar 

  • Huot R, Gonzalez C, Ladd C, Thrivikraman K, Plotsky P (2004) Foster litters prevent ­hypothalamic-pituitary-adrenal axis sensitization mediated by neonatal maternal separation. Psychoneuroendocrinology 29:279–289

    PubMed  CAS  Google Scholar 

  • Insel T, Kinsley C, Mann P, Bridges R (1990) Prenatal stress has long-term effects on brain opiate receptors. Brain Res 511:93–97

    PubMed  CAS  Google Scholar 

  • Kaplan H, Lancaster J, Robson A (2003) Embodied capital and the evolutionary economics of the human life span. Population Dev Rev 29:152–182

    Google Scholar 

  • Kaufman J, Plotsky P, Nemeroff C, Charney D (2000) Effects of early adverse experiences on brain structure and function: clinical implications. Biol Psychiatry 48:778–790

    PubMed  CAS  Google Scholar 

  • Kerr M, Bowen M (1988) Family evaluation. W.W. Norton, New York

    Google Scholar 

  • Kinsley C, Bridges R (1988) Prenatal stress and maternal behavior in intact virgin rats: response latencies are decreased in males and increased in females. Horm Behav 22:76–89

    PubMed  CAS  Google Scholar 

  • Kinsley C, Svare B (1986) Prenatal stress reduces intermale aggression in mice. Physiol Behav 36:783–786

    PubMed  CAS  Google Scholar 

  • Konner M (2010) The evolution of childhood: relationships, emotion, mind. Harvard University Press, Cambridge, MA

    Google Scholar 

  • Kraemer G (1992) A psychobiological theory of attachment. Behav Brain Sci 15:493–511

    Google Scholar 

  • Krpan K, Coombs R, Zinga D, Steiner M, Fleming A (2005) Experiential and hormonal correlates of maternal behavior in teen and adult mothers. Horm Behav 47:112–122

    PubMed  CAS  Google Scholar 

  • Laakso M, Porkka-Heiskanen T, Alila A, Stenberg O, Johansson G (1994) 24-hour rhythms in relation to the natural photoperiod: a field study in humans. J Biol Rhythms 9:283–293

    PubMed  CAS  Google Scholar 

  • Ladd C, Huot R, Thrivikraman K, Nemeroff C, Meaney M, Plotsky P (2000) Long-term behavioral and neuroendocrine adaptations to adverse early experience. In: Mayer E, Super C (eds) Progress in brain research. Elsevier Science, Amsterdam, pp 81–103

    Google Scholar 

  • Laplante DP, Barr RG, Brunet A, Galbaud du Fort G, Meaney MJ et al (2004) Stress during ­pregnancy affects general intellectual and leanguage functioning in human toddlers. Pediatr Res 56:400–410

    PubMed  Google Scholar 

  • LeDoux J (1996) The emotional brain. Simon and Schuster, New York

    Google Scholar 

  • Leslie AM, Friedmann O, German TP (2004) Core mechanisms in ‘theory of mind’. Trends Cogn Sci 8:529–533

    Google Scholar 

  • Liu D, Diorio J, Tannenbaum B, Caldji C, Francis D, Freedman A, Sharma S, Pearson D, Plotsky P, Meaney MJ (1997) Maternal care, hippocampal glucocorticoid receptors and HPA responses to stress. Science 277:1659–1662

    PubMed  CAS  Google Scholar 

  • Long B, Ungpakorn G, Harrison GA (1993) Home-school differences in stress hormone levels in a group of Oxford primary school children. J Biosoc Sci 25:73–78

    PubMed  CAS  Google Scholar 

  • Lupien S, McEwen BS (1997) The acute effects of corticosteroids on cognition: integration of animal and human model studies. Brain Res Rev 24:1–27

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Maccari S, Piazza P, Kabbaj M, Barbazanges A, Simon H, Le Moal M (1995) Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress. J Neurosci 15:110–115

    PubMed  CAS  Google Scholar 

  • McEwen BS (1998) Protective and damaging effects of stress mediators. N Engl J Med 338:171–179

    PubMed  CAS  Google Scholar 

  • McEwen BS, Magarinos AM (2001) Stress and hippocampal plasticity: implications for the pathophysiology of affective disorders. Hum Psychopharmacol 16:S7–S19

    PubMed  CAS  Google Scholar 

  • McEwen BS (1995) Stressful experience, brain, and emotions: developmental, genetic, and hormonal influences. In: Gazzaniga MS (ed) The cognitive neurosciences. MIT, Cambridge, MA, pp 1117–1135

    PubMed  CAS  Google Scholar 

  • McEwen BS, Seeman T (1999) Protective and damaging effects of mediators of stress: elaborating and testing the concepts of allostasis and allostatic load. Ann N Y Acad Sci 896:30–47

    PubMed  CAS  Google Scholar 

  • McEwen B, Biron C, Brunson K, Bulloch K, Chambers W, Dhabhar F, Goldfarb R, Kitson R, Miller A, Spencer R, Weiss J (1997) The role of adrenocorticoids as modulators of immune function in health and disease: neural, endocrine and immune interactions. Brain Res Rev 23:79–133

    PubMed  CAS  Google Scholar 

  • McGowan PO, Sasaki A, D’Alessio AC, Dymov S, Labonté B, Szyf M, Turecki G, Meaney MJ (2009) Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat Neurosci 12:342–348

    PubMed  CAS  Google Scholar 

  • Mirescu C, Peters J, Gould E (2004) Early life experience alters response of adult neurogenesis to stress. Nat Neurosci 7:841–846

    PubMed  CAS  Google Scholar 

  • Mousseau TA, Fox CW (1998) Maternal effects as adaptations. Oxford University Press, New York

    Google Scholar 

  • Moyer J, Herrenkohl L, Jacobowitz D (1978) Stress during pregnancy: effect on catecholamines in discrete brain regions of offspring as adults. Brain Res 144:173–178

    PubMed  CAS  Google Scholar 

  • Muehlenbein MP, Flinn MV (2011) Patterns and processes of human life history evolution. In: Flatt T, Heyland A (eds) Mechanisms of life history evolution. Oxford University Press, New York, pp 153–168

    PubMed  CAS  Google Scholar 

  • Nepomnaschy P, Flinn MV (2009) Early life influences on the ontogeny of neuroendocrine stress response in the human child. In: Gray P, Ellison P (eds) The endocrinology of social relationships (chapter 16). Harvard University Press, Cambridge, MA

    Google Scholar 

  • Nicolson N (2004) Childhood parental loss and cortisol levels in adult men. Psychoneuroendocrinology 29:1012–1018

    PubMed  CAS  Google Scholar 

  • Noone R (2008) The multigenerational transmission process and the neurobiology of attachment and stress reactivity. Fam Syst 8:21–34

    Google Scholar 

  • O’Connor T, Dunn J, Jenkins J, Pickering K, Rasbash J (2001) Family settings and children’s adjustment: differential adjustment within and across families. Br J Psychiatry 179:110–115

    PubMed  Google Scholar 

  • O’Regan D, Welberg L, Holmes M, Seckl J (2001) Glucocorticoid programming of pituitary-­adrenal function: mechanisms and physiological consequences. Semin Neonatol 6:319–329

    PubMed  Google Scholar 

  • Panksepp J (1998) Affective neuroscience. Oxford University Press, New York

    Google Scholar 

  • Pinker S (1994) The language instinct. William Morrow, New York

    Google Scholar 

  • Pollard I (1984) Effects of stress administered during pregnancy on reproductive capacity and subsequent development of the offspring of rats: prolonged effects on the litters of a second pregnancy. J Endocrinol 100:301–306

    PubMed  CAS  Google Scholar 

  • Quinlan R, Flinn MV (2005) Kinship, sex and fitness in a Caribbean community. Hum Nat 16(1):32–57

    Google Scholar 

  • Quinlan R, Quinlan MB, Flinn MV (2005) Local resource enhancement & sex-biased breastfeeding in a Caribbean community. Curr Anthropol 46(3):471–480

    Google Scholar 

  • Rilling JK, Sanfey AG (2011) The neuroscience of social decision-making. Annu Rev Psychol 62:23–48

    Google Scholar 

  • Roth G, Dicke U (2005) Evolution of the brain and intelligence. Trends Cogn Sci 9:250–257

    Google Scholar 

  • Sabatini MJ, Ebert P, Lewis DA, Levitt P, Cameron JL, Mirnics K (2007) Amygdala gene expression correlates of social behavior in monkeys experiencing maternal separation. J Neurosci 27(12):3295–3304

    Google Scholar 

  • Sapolsky R (1992) Stress, the aging brain, and the mechanisms of neuron death. A Bradford Book, The MIT Press, Cambridge, Massachusetts

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Schneider M (1992) Prenatal stress exposure alters postnatal behavioral expression under conditions of novelty challenge in rhesus monkey infants. Dev Psychobiol 25:529–540

    PubMed  CAS  Google Scholar 

  • Schneider M, Coe C (1993) Repeated social stress during pregnancy impairs neuromotor ­development of the primate infant. J Dev Behav Pediatr 14:81–87

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Shimada M, Takahashi K, Ohkawa T, Segawa M, Higurashi M (1995) Determination of salivary cortisol by ELISA and its application to the assessment of the circadian rhythm in children. Horm Res 44:213–217

    PubMed  CAS  Google Scholar 

  • Simons RL, Chao W, Conger RD, Elder GH (2001) Quality of parenting as mediator of the effect of childhood defiance on adolescent friendship choices and delinquency: a growth curve analysis. J Marriage Fam 63:63–79

    Google Scholar 

  • Suomi S (2002) Attachment in rhesus monkeys. In: Cacioppo J et al (eds) Foundations in social neuroscience. The MIT Press, Cambridge, MA, pp 775–795

    Google Scholar 

  • Suomi S (2003) Social and biological mechanisms underlying impulsive aggressiveness in rhesus monkeys. In: Lahey B, Moffit T, Caspi A (eds) Causes of conduct disorder and juvenile delinquency. Guilford Press, New York, p 2003

    Google Scholar 

  • Suomi S, Mineka S, DeLizio RD (1983) Short- and long-term effects of repetitive mother-infant separations on social development in rhesus monkeys. Dev Psychobiol 19:770–786

    Google Scholar 

  • Swain JE, Lorberbaum JP, Kose S, Strathearn L (2007) Brain basis of early parent–infant interactions: psychology, physiology, and in vivo functional neuroimaging studies. J Child Psychol Psychiatry 48:262–287

    PubMed  Google Scholar 

  • Takahashi LK, Turner JG, Kalin NH (1992) Prenatal stress alters brain catecholaminergic activity and potentiates stress-induced behavior in adult rats. Brain Res 574:131–137

    PubMed  CAS  Google Scholar 

  • Talge NM, Neal C, Glover V (2007) Antenatal maternal stress and long-term effects on child neurodevelopment: how and why? J Child Psychol Psychiatry 48:245–261

    PubMed  Google Scholar 

  • Thomas C, Hypponen E, Power C (2008) Obesity and type 2 diabetes risk in midadult life: the role of childhood adversity. Pediatrics 121:e1240–e1249

    PubMed  Google Scholar 

  • Touitou Y, Haus E (2000) Alterations with aging of the endocrine and neuroendocrine circadian system in humans. Chronobiol Int 17:369–390

    PubMed  Google Scholar 

  • Touitou Y, Sulon J, Bogdan A, Reinberg A, Sodoyez JC, Demey-Ponsart E (1983) Adrenocortical hormones, ageing and mental condition: seasonal and circadian rhythms of plasma 18-hydroxy-11-deoxycorticosterone, total and free cortisol and urinary corticosteroids. J Endocrinol 96:53–64

    PubMed  Google Scholar 

  • Uvnas-Moberg K (1998) Oxytocin may mediate the benefits of positive social interaction and emotions. Psychoneuroendocrinology 23:819–835

    PubMed  CAS  Google Scholar 

  • Van den Bergh BRH, Marcoen A (2004) High antenatal maternal anxiety is related to ADHD symptoms, externalising problems, and anviety in 8- and 9-year-olds. Child Dev 75:1085

    PubMed  Google Scholar 

  • Van den Bergh BRH, Van Calster B, Smits T, Van Huffel S, Lagae L (2008) Antenatal maternal anxiety is related to HPA-axis dusregulation and self-reported depressive symptioms in adolescence: a prospective study on the fetal origins of depressed mood. Neuropsychopharmacology 33:536–545

    PubMed  Google Scholar 

  • van Hulten M, Pelser M, van Loon LC, Pieterse CM, Ton J (2006) Costs and benefits of priming for defense in Arabidopsis. Proc Natl Acad Sci U S A 103(14):5602–5607

    PubMed  Google Scholar 

  • Waddington CH (1956) Principles of embryology. Macmillan, New York

    PubMed  Google Scholar 

  • Walker RS, Flinn MV, Hill K (2010) The evolutionary history of partible paternity in lowland South America. Proc Natl Acad Sci 107(45):19195–19200

    PubMed  Google Scholar 

  • Walker RS, Hill K, Flinn MV, Ellsworth R (2011) Evolutionary history of hunter-gatherer marriage practices. PLoS One 6(4):e19066. doi:10.1371/ journal.pone.0019066

    PubMed  Google Scholar 

  • Weaver I, Cervoni N, Champagne F, Alessio A, Sharma S, Seckl J, Dymov S, Szyl M, Meaney M (2004) Epigenetic programming by maternal behavior. Nat Neurosci 7:847–854

    PubMed  CAS  Google Scholar 

  • Weinstock M (1997) Does prenatal stress impair coping and regulation of hypothalamic-pituitary-adrenal axis? Neurosci Biobehav Rev 21:1–10

    PubMed  CAS  Google Scholar 

  • Weinstock M (2005) The potential influence of maternal stress hormones on development and mental health of the offspring. Brain Behav Immun 19:296–308

    PubMed  CAS  Google Scholar 

  • Weinstock M (2008) The long-term behavioural consequences of prenatal stress. Neurosci Biobehav Rev 32:1073–1086

    PubMed  CAS  Google Scholar 

  • West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, Oxford

    PubMed  CAS  Google Scholar 

  • Yehuda R, Mulherin Engel S, Brand S, Marcus S, Berkowitz G (2005) Transgenerational effects of posttraumatic stress disorder in babies of mothers exposed to the World Trade Center attacks during pregnancy. J Clin Endocrinol Metab 90:4115–4118

    PubMed  CAS  Google Scholar 

  • Zhang T-Y, Meaney MJ (2010) Epigenetics and the environmental regulation of the genome and its function. Annu Rev Psychol 61:439–466

    PubMed  Google Scholar 

  • Zhang T-Y, Bagot R, Parent C, Nesbitt C, Bredy TW, Caldji C, Fish E, Anisman H, Szyf M, Meaney MJ (2006) Maternal programming of defensive responses through sustained effects on gene expression. Biol Psychol 73:72–89

    PubMed  Google Scholar 

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Acknowledgements

The authors thank the editors and reviewers for helpful advice. We also thank Dr. Katrina Salvanteand for aid in the literature review and development of the figures. This chapter has been possible, thanks to the financial support provided by the National Science Foundation (BCS-SBE #0640442, SBR-0136023, SBR-9205373, and BNS-8920569 to MVF) and a CIHR IGH Operating Grant (CIHR #106705), a Simon Fraser University (SFU) President’s Start-up Grant, and a seed grant from the Human Evolutionary Program at SFU (funded by the Simon Fraser University Community Trust Endowment Fund) to PAN.

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Authors and Affiliations

  1. Department of Anthropology, University of Missouri, 107 Swallow Hall, Columbia, MO, 65211, USA

    Mark V. Flinn

  2. Division of Biological Sciences, University of Missouri, Columbia, MO, USA

    Davide Ponzi

  3. Simon Fraser University, Burnaby, BC, Canada

    Pablo Nepomnaschy

  4. Center for Family Consultation, Evanston, IL, USA

    Robert Noone

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  1. Mark V. Flinn
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  2. Davide Ponzi
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Correspondence to Mark V. Flinn .

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  1. Istituto Superiore di Sanità, 299 Viale Regina Elena, Rome, 00161, Italy

    Giovanni Laviola

  2. Istituto Superiore di Sanità, 299 Viale Regina Elena, Rome, 00161, Italy

    Simone Macrì

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Flinn, M.V., Ponzi, D., Nepomnaschy, P., Noone, R. (2013). Ontogeny of Stress Reactivity in the Human Child: Phenotypic Flexibility, Trade-Offs, and Pathology. In: Laviola, G., Macrì, S. (eds) Adaptive and Maladaptive Aspects of Developmental Stress. Current Topics in Neurotoxicity, vol 3. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-5605-6_5

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