Pediatrics & Neonatology
Volume 52, Issue 3 , Pages 122-129 , June 2011

Effects of Early Life Stress on Neuroendocrine and Neurobehavior: Mechanisms and Implications

  • Ming-Chi Lai

      Affiliations

    • Department of Pediatrics, Chi Mei Medical Center, Yong Kang Campus, Tainan, Taiwan
  • ,
  • Li-Tung Huang

      Affiliations

    • Department of Pediatrics, Chang Gung Memorial Hospital—Kaohsiung Medical Center, Chang Gung University College of Medicine, Kaohsiung, Taiwan
    • Corresponding Author InformationCorresponding author. Department of Pediatrics, Chang Gung Memorial Hospital—Kaohsiung Medical Center, 123 Ta Pei Road, Niao Sung Hsiang, Kaohsiung Hsien 833, Taiwan.

Received 10 August 2010 ,Revised 30 November 2010 ,Accepted 23 December 2010.

References 

  1. Buchmann AF, Kopf D, Westphal S, et al. Impact of early parental child-rearing behavior on young adults’ cardiometabolic risk profile: a prospective study. Psychosom Med. 2010;72:156–162
  2. Talge NM, Neal C, Glover V. Antenatal maternal stress and long-term effects on child neurodevelopment: how and why?. J Child Psychol Psychiatry. 2007;48:245–261
  3. Taylor SE. Mechanisms linking early life stress to adult health outcomes. Proc Natl Acad Sci U S A. 2010;107:8507–8512
  4. Meagher MW, Sieve AN, Johnson RR, et al. Neonatal maternal separation alters immune, endocrine, and behavioral responses to acute Theiler’s virus infection in adult mice. Behav Genet. 2010;40:233–249
  5. Joëls M, Baram TZ. The neuro-symphony of stress. Nat Rev Neurosci. 2009;10:459–466
  6. Craft TK, Zhang N, Glasper ER, Hurn PD, Devries AC. Neonatal factors influence adult stroke outcome. Psychoneuroendocrinology. 2006;31:601–613
  7. Francis DD, Diorio J, Plotsky PM, Meaney MJ. Environmental enrichment reverses the effects of maternal separation on stress reactivity. J Neurosci. 2002;22:7840–7843
  8. Levine S. Maternal behavior as a mediator of pup adrenocortical function. Ann NY Acad Sci. 1994;746:260–275
  9. Liu D, Diorio J, Tannenbaum B, et al. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science. 1997;277:1659–1662
  10. Matthews SG. Early programming of the hypothalamo-pituitary-adrenal axis. Trends Endocrinol Metab. 2002;13:373–380
  11. McCormick CM, Kehoe P, Kovacs S. Corticosterone release in response to repeated, short episodes of neonatal isolation: evidence of sensitization. Int J Dev Neurosci. 1998;16:175–185
  12. McEwen BS. Effects of adverse experiences for brain structure and function. Biol Psychiatry. 2000;48:721–731
  13. Meaney MJ. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci. 2001;24:1161–1192
  14. Plotsky PM, Meaney MJ. Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Mol Brain Res. 1993;18:195–200
  15. Roceri M, Cirulli F, Pessina C, Peretto P, Racagni G, Riva MA. Postnatal repeated maternal deprivation produces age-dependent changes of brain-derived neurotrophic factor expression in selected rat brain regions. Biol Psychiatry. 2004;55:708–714
  16. Weaver IC, Cervoni N, Champagne FA, et al. Epigenetic programming by maternal behavior. Nat Neurosci. 2004;7:847–854
  17. Heuser I, Lammers CH. Stress and the brain. Neurobiol Aging. 2003;24(S1):S69–S76
  18. Imaki T, Nahan JL, Rivier C, Sawchenko PE, Vale W. Differential regulation of corticotropin-releasing factor mRNA in rat brain regions by glucocorticoids and stress. J Neurosci. 1991;11:585–599
  19. Plotsky PM, Sawchenko PE. Hypophysial-portal plasma levels, median eminence content, and immunohistochemical staining of corticotropin-releasing factor, arginine vasopressin, and oxytocin after pharmacological adrenalectomy. Endocrinology. 1987;120:1361–1369
  20. Silbernagl S, Despopoulos A. Color Atlas of Physiology (Basic Sciences). 6th edition. Stuttgart/New York: Thieme; 2009;pp. 268–333
  21. von Bardeleben U, Holsboer F. Human corticotropin releasing hormone: clinical studies in patients with affective disorders, alcoholism, panic disorder and in normal controls. Prog Neuropsychopharmacol Biol Psychiatry. 1988;12:S165–S187
  22. Sapolsky RM. Stress, glucocorticoids, and damage to the nervous system: the current state of confusion. Stress. 1996;1:1–19
  23. Eisenberg L. Social policy and child health. Acta Paediatr Suppl. 1994;394:7–13
  24. Eisenberg L, Belfer M. Prerequisites for global child and adolescent mental health. J Child Psychol Psychiatry. 2009;50:26–35
  25. Linnet KM, Dalsgaard S, Obel C, et al. Maternal lifestyle factors in pregnancy risk of attention deficit hyperactivity disorder and associated behaviors: review of the current evidence. Am J Psychiatry. 2003;160:1028–1040
  26. Miller SP, Weiss J, Barnwell A, et al. Seizure-associated brain injury in term newborns with perinatal asphyxia. Neurology. 2002;58:542–548
  27. Scher MS. Neonatal seizures and brain damage. Pediatr Neurol. 2003;29:381–390
  28. Scher MS, Hamid MY, Steppe DA, Beggarly ME, Painter MJ. Ictal and interictal electrographic seizure durations in preterm and term neonates. Epilepsia. 1993;34:284–288
  29. Yeh TF, Lin YJ, Lin HC, et al. Outcomes at school age after postnatal dexamethasone therapy for lung disease of prematurity. N Engl J Med. 2004;350:1304–1313
  30. Barbazanges A, Piazza PV, Le Moal M, Maccari S. Maternal glucocorticoid secretion mediates long-term effects of prenatal stress. J Neurosci. 1996;16:3943–3949
  31. Huang LT, Holmes GL, Lai MC, et al. Maternal deprivation stress exacerbates cognitive deficits in immature rats with recurrent seizures. Epilepsia. 2002;43:1141–1148
  32. Lai MC, Holmes GL, Lee KH, et al. Effect of neonatal isolation on outcome following neonatal seizures in rats: the role of corticosterone. Epilepsy Res. 2006;68:123–136
  33. Lai MC, Lui CC, Yang SN, Wang JY, Huang LT. Epileptogenesis is increased in rats with neonatal isolation and early-life seizure and ameliorated by MK-801: a long-term MRI and histological study. Pediatr Res. 2009;66:441–447
  34. Lai MC, Yang SN, Huang LT. Neonatal isolation enhances anxiety-like behavior following early-life seizure in rats. Pediatr Neonatol. 2008;49:19–25
  35. Sevelinges Y, Sullivan RM, Messaoudi B, Mouly AM. Neonatal odor-shock conditioning alters the neural network involved in odor fear learning at adulthood. Learn Mem. 2008;15:649–656
  36. de Kloet ER. Steroids, stability and stress. Front Neuroendocrinol. 1995;16:416–425
  37. de Kloet ER, Reul JM, Sutanto W. Corticosteroids and the brain. J Steroid Biochem Mol Biol. 1990;37:387–394
  38. Avishai-Eliner S, Brunson KL, Sandman CA, Baram TZ. Stressed-out, or in (utero)?. Trends Neurosci. 2002;25:518–524
  39. Brunson KL, Eghbal-Ahmadi M, Bender R, Chen Y, Baram TZ. 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. 2001;98:8856–8861
  40. Hatalski CG, Guirguis C, Baram TZ. Corticotropin releasing factor mRNA expression in the hypothalamic paraventricular nucleus and the central nucleus of the amygdala is modulated by repeated acute stress in the immature rat. J Neuroendocrinol. 1998;10:663–669
  41. Wadhwa PD, Sandman CA, Garite TJ. The neurobiology of stress in human pregnancy: implications for prematurity and development of the fetal central nervous system. Prog Brain Res. 2001;133:131–142
  42. Sapolsky RM, Meaney MJ. Maturation of the adrenocortical stress response: neuroendocrine control mechanisms and the stress hyporesponsive period. Brain Res. 1986;39:64–76
  43. Grino M, Burgunder JM, Eskay RL, Eiden LE. Onset of glucocorticoid responsiveness of anterior pituitary corticotrophs during development is scheduled by corticotropin-releasing factor. Endocrinology. 1989;124:2686–2692
  44. Walker CD, Akana SF, Cascio CS, Dallman MF. Adrenalectomy in the neonate: adult-like adrenocortical system responses to both removal and replacement of corticosterone. Endocrinology. 1990;127:832–842
  45. Schmidt MV, Enthoven L, van der Mark M, Levine S, de Kloet ER, Oitzl MS. The postnatal development of the hypothalamic-pituitary-adrenal axis in the mouse. Int J Dev Neurosci. 2003;21:125–132
  46. Erdmann G, Schütz G, Berger S. Loss of glucocorticoid receptor function in the pituitary results in early postnatal lethality. Endocrinology. 2008;149:3446–3451
  47. Levine S, Huchton DM, Wiener SG, Rosenfeld P. Time course of the effect of maternal deprivation on the hypothalamic-pituitary-adrenal axis in the infant rat. Dev Psychobiol. 1991;24:547–558
  48. Schmidt MV. Molecular mechanisms of early life stress: lessons from mouse models. Neurosci Biobehav Rev. 2010;34:845–852
  49. Smith MA, Kim SY, van Oers HJ, Levine S. Maternal deprivation and stress induce immediate early genes in the infant rat brain. Endocrinology. 1997;138:4622–4628
  50. Avishai-Eliner S, Hatalski CG, Tabachnik E, Eghbal-Ahmadi M, Baram TZ. Differential regulation of glucocorticoid receptor messenger RNA (GR-mRNA) by maternal deprivation in immature rat hypothalamus and limbic regions. Brain Res Dev Brain Res. 1999;114:265–268
  51. Schmidt MV, Oitzl MS, Levine S, de Kloet ER. The HPA system during the postnatal development of CD1 mice and the effects of maternal deprivation. Brain Res Dev Brain Res. 2002;139:39–49
  52. Weaver IC. Epigenetic effects of glucocorticoids. Semin Fetal Neonatal Med. 2009;14:143–150
  53. Gross KL, Lu NZ, Cidlowski JA. Molecular mechanisms regulating glucocorticoid sensitivity and resistance. Mol Cell Endocrinol. 2009;300:7–16
  54. Coste SC, Kesterson RA, Heldwein KA, et al. Abnormal adaptations to stress and impaired cardiovascular function in mice lacking corticotropin-releasing hormone receptor-2. Nat Genet. 2000;24:403–409
  55. Chen Y, Bender RA, Brunson KL, et al. Modulation of dendritic differentiation by corticotropin-releasing factor in the developing hippocampus. Proc Natl Acad Sci U S A. 2004;101:15782–15787
  56. Chen Y, Bender RA, Frotscher M, Baram TZ. Novel and transient populations of corticotropin-releasing hormone-expressing neurons in developing hippocampus suggest unique functional roles: a quantitative spatiotemporal analysis. J Neurosci. 2001;21:7171–7181
  57. Oitzl MS, Champagne DL, van der Veen R, de Kloet ER. Brain development under stress: hypotheses of glucocorticoid actions revisited. Neurosci Biobehav Rev. 2010;34:853–866
  58. Leuner B, Gould E. Structural plasticity and hippocampal function. Annu Rev Psychol. 2010;61:111–140C1–3
  59. Karst H, Joëls M. Corticosterone slowly enhances miniature excitatory postsynaptic current amplitude in mice CA1 hippocampal cells. J Neurophysiol. 2005;94:3479–3486
  60. Rich MM, Wenner P. Sensing and expressing homeostatic synaptic plasticity. Trends Neurosci. 2007;30:119–125
  61. Fenoglio KA, Brunson KL, Baram TZ. Hippocampal neuroplasticity induced by early-life stress: functional and molecular aspects. Front Neuroendocrinol. 2006;27:180–192
  62. Liu D, Diorio J, Day JC, Francis DD, Meaney MJ. Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nat Neurosci. 2000;3:799–806
  63. Aisa B, Elizalde N, Tordera R, Lasheras B, Del Río J, Ramírez MJ. Effects of neonatal stress on markers of synaptic plasticity in the hippocampus: implications for spatial memory. Hippocampus. 2009;19:1222–1231
  64. Diorio J, Meaney MJ. Maternal programming of defensive responses through sustained effects on gene expression. J Psychiatry Neurosci. 2007;32:275–284
  65. Kim JJ, Yoon KS. Stress: metaplastic effects in the hippocampus. Trends Neurosci. 1998;21:505–509
  66. McGaugh JL. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu Rev Neurosci. 2004;27:1–28
  67. Foster JA, Burman MA. Evidence for hippocampus-dependent contextual learning at postnatal day 17 in the rat. Learn Mem. 2010;17:259–266
  68. Phillips RG, LeDoux JE. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci. 1992;106:274–285
  69. Matsumoto M, Yoshioka M, Togashi H. Early postnatal stress and neural circuit underlying emotional regulation. Int Rev Neurobiol. 2009;85:95–107
  70. Sevelinges Y, Moriceau S, Holman P, et al. Enduring effects of infant memories: infant odor-shock conditioning attenuates amygdala activity and adult fear conditioning. Biol Psychiatry. 2007;62:1070–1079
  71. Musholt K, Cirillo G, Cavaliere C, et al. Neonatal separation stress reduces glial fibrillary acidic protein- and S100 beta-immunoreactive astrocytes in the rat medial precentral cortex. Dev Neurobiol. 2009;69:203–211
  72. Silva AJ, Kogan JH, Frankland PW, Kida S. CREB and memory. Annu Rev Neurosci. 1998;21:127–148
  73. Owen D, Matthews SG. Repeated maternal glucocorticoid treatment affects activity and hippocampal NMDA receptor expression in juvenile guinea pigs. J Physiol. 2007;578:249–257
  74. Son GH, Geum D, Chung S, et al. Maternal stress produces learning deficits associated with impairment of NMDA receptor-mediated synaptic plasticity. J Neurosci. 2006;26:3309–3318
  75. Gross C, Zhuang X, Stark K, et al. Serotonin1A receptor acts during development to establish normal anxiety-like behaviour in the adult. Nature. 2002;416:396–400
  76. Datson NA, van der Perk J, de Kloet ER, Vreugdenhil E. Identification of corticosteroid-responsive genes in rat hippocampus using serial analysis of gene expression. Eur J Neurosci. 2001;14:1–17
  77. Feldker DE, Datson NA, Veenema AH, Meulmeester E, de Kloet ER, Vreugdenhil E. Serial analysis of gene expression predicts structural differences in hippocampus of long attack latency and short attack latency mice. Eur J Neurosci. 2003;17:379–387
  78. Cirulli F, Berry A, Bonsignore LT, et al. Early life influences on emotional reactivity: evidence that social enrichment has greater effects than handling on anxiety-like behaviors, neuroendocrine responses to stress and central BDNF levels. Neurosci Biobehav Rev. 2010;34:808–820
  79. Dubé C, Boyet S, Marescaux C, Nehlig A. Relationship between neuronal loss and interictal glucose metabolism during the chronic phase of the lithium-pilocarpine model of epilepsy in the immature and adult rat. Exp Neurol. 2001;167:227–241
  80. Schmid R, Tandon P, Stafstrom CE, Holmes GL. Effects of neonatal seizures on subsequent seizure-induced brain injury. Neurology. 1999;53:1754–1761
  81. Koe AS, Jones NC, Salzberg MR. Early life stress as an influence on limbic epilepsy: an hypothesis whose time has come?. Front Behav Neurosci. 2009;3:1–16
  82. Nair SM, Werkman TR, Craig J, Finnell R, Joels M, Eberwine JH. Corticosteroid regulation of ion channel conductances and mRNA levels in individual hippocampal CA1 neurons. J Neurosci. 1998;18:2685–2696
  83. Venero C, Borrell J. Rapid glucocorticoid effects on excitatory amino acid levels in the hippocampus: a microdialysis study in freely moving rats. Eur J Neurosci. 1999;11:2465–2473
  84. Lee PR, Brady D, Koenig JI. Corticosterone alters N-methyl-D-aspartate receptor subunit mRNA expression before puberty. Brain Res Mol Brain Res. 2003;115:55–62
  85. Virgin CE, Ha TP, Packan DR, et al. Glucocorticoids inhibit glucose transport and glutamate uptake in hippocampal astrocytes: implications for glucocorticoid neurotoxicity. J Neurochem. 1991;57:1422–1428
  86. Taher TR, Salzberg M, Morris MJ, Rees S, O’Brien TJ. Chronic low-dose corticosterone supplementation enhances acquired epileptogenesis in the rat amygdala kindling model of TLE. Neuropsychopharmacology. 2005;30:1610–1616
  87. Frye CA, Rhodes ME, Raol YH, Brooks-Kayal AR. Early postnatal stimulation alters pregnane neurosteroids in the hippocampus. Psychopharmacology (Berl). 2006;186:343–350
  88. Salzberg M, Kumar G, Supit L, et al. Early postnatal stress confers enduring vulnerability to limbic epileptogenesis. Epilepsia. 2007;48:2079–2085
  89. Karst H, de Kloet ER, Joels M. Episodic corticosterone treatment accelerates kindling epileptogenesis and triggers long-term changes in hippocampal CA1 cells, in the fully kindled state. Eur J Neurosci. 1999;11:889–898
  90. Mulholland PJ, Self RL, Harris BR, Littleton JM, Prendergast MA. (−)-Nicotine ameliorates corticosterone’s potentiation of N-methyl-D-aspartate receptor-mediated cornu ammonis 1 toxicity. Neuroscience. 2004;125:671–682
  91. Stein-Behrens BA, Lin WJ, Sapolsky RM. Physiological elevations of glucocorticoids potentiate glutamate accumulation in the hippocampus. J Neurochem. 1994;63:596–602
  92. Seidel K, Helmeke C, Poeggel G, Braun K. Repeated neonatal separation stress alters the composition of neurochemically characterized interneuron subpopulations in the rodent dentate gyrus and basolateral amygdala. Dev Neurobiol. 2008;68:1137–1152
  93. Anand KJ. Effects of perinatal pain and stress. Prog Brain Res. 2000;122:117–129

PII: S1875-9572(11)00039-8

doi: 10.1016/j.pedneo.2011.03.008

Pediatrics & Neonatology
Volume 52, Issue 3 , Pages 122-129 , June 2011