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Neurobiological Programming of Early Life Stress: Functional Development of Amygdala-Prefrontal Circuitry and Vulnerability for Stress-Related Psychopathology

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Behavioral Neurobiology of PTSD

Part of the book series: Current Topics in Behavioral Neurosciences ((CTBN,volume 38))

Abstract

Early adverse experiences are associated with heighted vulnerability for stress-related psychopathology across the lifespan. While extensive work has investigated the effects of early adversity on neurobiology in adulthood, developmental approaches can provide further insight on the neurobiological mechanisms that link early experiences and long-term mental health outcomes. In the current review, we discuss the role of emotion regulation circuitry implicated in stress-related psychopathology from a developmental and transdiagnostic perspective. We highlight converging evidence suggesting that multiple forms of early adverse experiences impact the functional development of amygdala-prefrontal circuitry. Next, we discuss how adversity-induced alterations in amygdala-prefrontal development are associated with symptoms of emotion dysregulation and psychopathology. Additionally, we discuss potential mechanisms through which protective factors may buffer the effects of early adversity on amygdala-prefrontal development to confer more adaptive long-term outcomes. Finally, we consider limitations of the existing literature and make suggestions for future longitudinal and translational research that can better elucidate the mechanisms linking early adversity, neurobiology, and emotional phenotypes. Together, these findings may provide further insight into the neuro-developmental mechanisms underlying the emergence of adversity-related emotional disorders and facilitate the development of targeted interventions that can ameliorate risk for psychopathology in youth exposed to early life stress.

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References

  1. Green JG, Mclaughlin KA, Berglund PA, Gruber MJ, Sampson NA, Zaslavsky AM, Kessler RC (2010) Childhood adversities and adult psychiatric disorders in the national comorbidity survey replication I: associations with first onset of DSM-IV disorders. Arch Gen Psychiatry 67(2):113–123, http://doi.org/10.1001/archgenpsychiatry.2009.187

    PubMed  PubMed Central  Google Scholar 

  2. Kessler RC, Berglund P, Demler O, Jin R, Merikangas KR, Walters EE (2005) Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Arch Gen Psychiatry 62(6):593–602, http://doi.org/10.1001/archpsyc.62.6.593

    PubMed  Google Scholar 

  3. Kessler RC, McLaughlin KA, Green JG, Gruber MJ, Sampson NA, Zaslavsky AM et al (2010) Childhood adversities and adult psychopathology in the WHO World Mental Health Surveys. Br J Psychiatry 197(5):378–385, http://doi.org/10.1192/bjp.bp.110.080499

    PubMed  PubMed Central  Google Scholar 

  4. Essex MJ, Shirtcliff EA, Burk LR, Ruttle PL, Klein MH, Slattery MJ et al (2011) Influence of early life stress on later hypothalamic-pituitary-adrenal axis functioning and its covariation with mental health symptoms: a study of the allostatic process from childhood into adolescence. Dev Psychopathol 23(4):1039–1058, http://doi.org/10.1017/S0954579411000484

    PubMed  PubMed Central  Google Scholar 

  5. Humphreys KL, Gleason MM, Drury SS, Miron D, Nelson CA, Fox NA, Zeanah CH (2015) Effects of institutional rearing and foster care on psychopathology at age 12 years in Romania: follow-up of an open, randomised controlled trial. Lancet Psychiatry 2(7):625–634, http://doi.org/10.1016/S2215-0366(15)00095-4

    PubMed  PubMed Central  Google Scholar 

  6. Lansford JE, Dodge KA, Pettit GS, Bates JE, Crozier J, Kaplow J (2014) A 12-year prospective study of the long-term effects of early child physical maltreatment on psychological. Arch Pediatr Adolesc Med 156:824–830

    Google Scholar 

  7. Merikangas KR, He J, Burstein M, Swanson SA, Avenevoli S, Cui L et al (2010) Lifetime prevalence of mental disorders in U.S. adolescents: results from the National Comorbidity Survey Replication–Adolescent Supplement (NCS-A). J Am Acad Child Adolesc Psychiatry 49(10):980–989, http://doi.org/10.1016/j.jaac.2010.05.017

    PubMed  PubMed Central  Google Scholar 

  8. Smith LB, Thelen E (2003) Development as a dynamic system. Trends Cogn Sci 7(8):343–348, http://doi.org/10.1016/S1364-6613(03)00156-6

    PubMed  Google Scholar 

  9. Barker DJP (2007) The origins of the developmental origins theory. J Intern Med 261(5):412–417, http://doi.org/10.1111/j.1365-2796.2007.01809.x

    CAS  PubMed  Google Scholar 

  10. Blair C, Raver CC (2012) Child development in the context of adversity: experiential canalization of brain and behavior. Am Psychol 67(4):309–318, http://doi.org/10.1037/a0027493

    PubMed  PubMed Central  Google Scholar 

  11. 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 

  12. Wadhwa P, Buss C, Entringer S, Swanson M (2010) Developmental origins of health and disease: brief history of the approach and current focus on epigenetic mechanisms. Semin Reprod Med 27(5):358–368, http://doi.org/10.1055/s-0029-1237424.Developmental

    Google Scholar 

  13. Callaghan BL, Tottenham N (2016) The stress acceleration hypothesis: effects of early-life adversity on emotion circuits and behavior. Curr Opin Behav Sci 7:76–81, http://doi.org/10.1016/j.cobeha.2015.11.018

    PubMed  Google Scholar 

  14. Tottenham N, Sheridan MA (2009) A review of adversity, the amygdala and the hippocampus: a consideration of developmental timing. Front Hum Neurosci 3:68, http://doi.org/10.3389/neuro.09.068.2009

    PubMed  Google Scholar 

  15. De Bellis MD, Broussard ER, Herring DJ, Wexler S, Moritz G, Benitez JG (2001) Psychiatric co-morbidity in caregivers and children involved in maltreatment: a pilot research study with policy implications. Child Abuse Negl 25(7):923–944, http://doi.org/10.1016/S0145-2134(01)00247-2

    PubMed  Google Scholar 

  16. Hariri AR, Holmes A (2015) Finding translation in stress research. Nat Neurosci 18(10):1347–1352, http://doi.org/10.1038/nn.4111

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Davis M, Whalen PJ (2001) The amygdala: vigilance and emotion. Mol Psychiatry 6(1):13–34. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/11244481

  18. Kim JH, Hamlin AS, Richardson R (2009) Fear extinction across development: the involvement of the medial prefrontal cortex as assessed by temporary inactivation and immunohistochemistry. J Neurosci 29(35):10802–10808, http://doi.org/10.1523/JNEUROSCI.0596-09.2009

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Milad MR, Rauch SL, Pitman RK, Quirk GJ (2006) Fear extinction in rats: implications for human brain imaging and anxiety disorders. Biol Psychol 73:61–71, http://doi.org/10.1016/j.biopsycho.2006.01.008

    PubMed  Google Scholar 

  20. Phelps EA, LeDoux JE (2005) Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 48(2):175–187, http://doi.org/10.1016/j.neuron.2005.09.025

    CAS  PubMed  Google Scholar 

  21. Buhle JT, Silvers JA, Wager TD, Lopez R, Onyemekwu C, Kober H et al (2014) Cognitive reappraisal of emotion: a meta-analysis of human neuroimaging studies. Cereb Cortex 24:2981–2990, http://doi.org/10.1093/cercor/bht154

    PubMed  Google Scholar 

  22. Etkin A, Klemenhagen KC, Dudman JT, Rogan MT, Hen R, Kandel ER, Hirsch J (2004) Individual differences in trait anxiety predict the response of the basolateral amygdala to unconsciously processed fearful faces. Neuron 44(6):1043–1055, http://doi.org/10.1016/j.neuron.2004.12.006

    CAS  PubMed  Google Scholar 

  23. Koenigs M, Grafman J (2009) Posttraumatic stress disorder: the role of medial prefrontal cortex and amygdala. Neuroscientist 15(5):540–548

    PubMed  PubMed Central  Google Scholar 

  24. Murray EA, Wise SP, Drevets WC (2011) Localization of dysfunction in major depressive disorder: prefrontal cortex and amygdala. Biol Psychiatry 69(12):e43–e54, http://doi.org/10.1016/j.biopsych.2010.09.041

    PubMed  Google Scholar 

  25. Morris SE, Cuthbert BN (2012) State of the art. Dialogues Clin Neurosci 14:29–37

    PubMed  PubMed Central  Google Scholar 

  26. Dillon DG, Rosso IM, Pechtel P, Killgore WDS, Rauch SL, Pizzagalli DA (2014) Peril and pleasure: an rdoc-inspired examination of threat responses and reward processing in anxiety and depression. Depress Anxiety 31(3):233–249, http://doi.org/10.1002/da.22202.Peril

    PubMed  Google Scholar 

  27. Gee DG, Humphreys KL, Flannery J, Goff B, Telzer EH, Shapiro M et al (2013) A developmental shift from positive to negative connectivity in human amygdala-prefrontal circuitry. J Neurosci 33(10):4584–4593, http://doi.org/10.1523/JNEUROSCI.3446-12.2013

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Guyer AE, Monk CS, McClure-Tone EB, Nelson EE, Roberson-Nay R, Adler AD et al (2008) A developmental examination of amygdala response to facial expressions. J Cogn Neurosci 20(9):1565–1582, http://doi.org/10.1162/jocn.2008.20114

    PubMed  PubMed Central  Google Scholar 

  29. Hwang S, White SF, Nolan ZT, Sinclair S, Blair RJR (2014) Neurodevelopmental changes in the responsiveness of systems involved in top down attention and emotional responding. Neuropsychologia 62:1–9, http://doi.org/10.1016/j.neuropsychologia.2014.08.003

    Google Scholar 

  30. Swartz JR, Carrasco M, Wiggins JL, Thomason ME, Monk CS (2014) Age-related changes in the structure and function of prefrontal cortex-amygdala circuitry in children and adolescents: a multi-modal imaging approach. Neuroimage 86:212–220, http://doi.org/10.1016/j.neuroimage.2013.08.018

    PubMed  Google Scholar 

  31. Vink M, Derks JM, Hoogendam JM, Hillegers M, Kahn RS (2014) Functional differences in emotion processing during adolescence and early adulthood. Neuroimage 91:70–76, http://doi.org/10.1016/j.neuroimage.2014.01.035

    PubMed  Google Scholar 

  32. Decety J, Michalska KJ, Kinzler KD (2012) The contribution of emotion and cognition to moral sensitivity: a neurodevelopmental study. Cereb Cortex 22(1):209–220, http://doi.org/10.1093/cercor/bhr111

    PubMed  Google Scholar 

  33. Gabard-Durnam LJ, Flannery J, Goff B, Gee DG, Humphreys KL, Telzer E et al (2014) The development of human amygdala functional connectivity at rest from 4 to 23 years: a cross-sectional study. Neuroimage 95:193–207, http://doi.org/10.1016/j.neuroimage.2014.03.038

    PubMed  Google Scholar 

  34. Dougherty LR, Blankenship SL, Spechler PA, Padmala S, Pessoa L (2015) An fMRI pilot study of cognitive reappraisal in children: divergent effects on brain and behavior. J Psychopathol Behav Assess 37(4):634–644, http://doi.org/10.1007/s10862-015-9492-z

    PubMed  PubMed Central  Google Scholar 

  35. McRae K, Gross JJ, Weber J, Robertson ER, Sokol-Hessner P, Ray RD et al (2012) The development of emotion regulation: an fMRI study of cognitive reappraisal in children, adolescents and young adults. Soc Cogn Affect Neurosci 7(1):11–22, http://doi.org/10.1093/scan/nsr093

    PubMed  PubMed Central  Google Scholar 

  36. Silvers JA, Shu J, Hubbard AD, Weber J, Ochsner KN (2015) Concurrent and lasting effects of emotion regulation on amygdala response in adolescence and young adulthood. Dev Sci 18(5):771–784, http://doi.org/10.1111/desc.12260

    PubMed  Google Scholar 

  37. Gaffrey MS, Luby JL, Belden AC, Hirshberg JS, Volsch J, Barch DM (2011) Association between depression severity and amygdala reactivity during sad face viewing in depressed preschoolers: an fMRI study. J Affect Disord 129(1-3):364–370, http://doi.org/10.1016/j.jad.2010.08.031

    PubMed  PubMed Central  Google Scholar 

  38. Garrett AS, Carrion V, Kletter H, Karchemskiy A, Weems CF, Reiss A (2012) Brain activation to facial expressions in youth with PTSD symptoms. Depress Anxiety 29(5):449–459, http://doi.org/10.1002/da.21892

    PubMed  PubMed Central  Google Scholar 

  39. Pagliaccio D, Luby J, Gaffrey M, Belden A, Botteron K, Gotlib IH, Barch DM (2012) Anomalous functional brain activation following negative mood induction in children with pre-school onset major depression. Dev Cogn Neurosci 2(2):256–267, http://doi.org/10.1016/j.dcn.2011.11.008

    PubMed  Google Scholar 

  40. Pine DS, Guyer AE, Leibenluft E (2008) Functional magnetic resonance imaging and pediatric anxiety. J Am Acad 47(11):1217–1221, http://doi.org/10.1097/CHI.0b013e318185dad0.FUNCTIONAL

    Google Scholar 

  41. Roy AK, Fudge JL, Kelly C, Perry JSA, Daniele T, Carlisi C et al (2013) Intrinsic functional connectivity of amygdala-based networks in adolescent generalized anxiety disorder. J Am Acad Child Adolesc Psychiatry 52(3):290–299.e2. http://doi.org/10.1016/j.jaac.2012.12.010

  42. Wolf RC, Herringa RJ (2016) Prefrontal-amygdala dysregulation to threat in pediatric post-traumatic stress disorder. Neuropsychopharmacology 41(3):822–831, http://doi.org/10.1038/npp.2015.209

    PubMed  Google Scholar 

  43. Kujawa A, Wu M, Klump H, Pine DS, Swain JE, Fitzgerald KD et al (2016) Altered development of amygdala-anterior cingulate cortex connectivity in anxious youth and young adults. Biol Psychiatry Cogn Neurosci Neuroimaging 1(4):345–352, http://doi.org/10.1017/CBO9781107415324.004

    PubMed  PubMed Central  Google Scholar 

  44. Callaghan BL, Sullivan RM, Howell B, Tottenham N (2014) The international society for developmental psychobiology Sackler symposium: early adversity and the maturation of emotion circuits-A cross-species analysis. Dev Psychobiol 56(8):1635–1650, http://doi.org/10.1002/dev.21260

    PubMed  PubMed Central  Google Scholar 

  45. Avishai-Eliner S, Yi SJ, Baram TZ (1996) Developmental profile of messenger RNA for the corticotropin-releasing hormone receptor in the rat limbic system. Brain Res Dev Brain Res 91(2):159–163, http://doi.org/0165380695001581

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Hatalski CG, Guirguis C, Baram TZ (2012) 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 10(9):663–669

    Google Scholar 

  47. Moriceau S, Wilson DA, Levine S, Sullivan RM (2006) Dual circuitry for odor-shock conditioning during infancy: corticosterone switches between fear and attraction via amygdala. J Neurosci 26(25):6737–6748, http://doi.org/10.1523/JNEUROSCI.0499-06.2006

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Eiland L, Ramroop J, Hill MN, Manley J, McEwen BS (2012) Chronic juvenile stress produces corticolimbic dendritic architectural remodeling and modulates emotional behavior in male and female rats. Psychoneuroendocrinology 37(1):39–47, http://doi.org/10.1016/j.psyneuen.2011.04.015

    CAS  PubMed  Google Scholar 

  49. Malter Cohen M, Jing D, Yang RR, Tottenham N, Lee FS, Casey BJ (2013) Early-life stress has persistent effects on amygdala function and development in mice and humans. Proc Natl Acad Sci U S A 110(45):18274–18278, http://doi.org/10.1073/pnas.1310163110

    PubMed  PubMed Central  Google Scholar 

  50. Raineki C, Cortés MR, Belnoue L, Sullivan RM (2012) Effects of early-life abuse differ across development: infant social behavior deficits are followed by adolescent depressive-like behaviors mediated by the amygdala. J Neurosci 32(22):7758–7765, http://doi.org/10.1523/JNEUROSCI.5843-11.2012

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Ishikawa J, Nishimura R, Ishikawa A (2015) Early-life stress induces anxiety-like behaviors and activity imbalances in the medial prefrontal cortex and amygdala in adult rats. Eur J Neurosci 41(4):442–453, http://doi.org/10.1111/ejn.12825

    PubMed  Google Scholar 

  52. McLaughlin KA, Sheridan MA, Lambert HHK (2014) Childhood adversity and neural development: deprivation and threat as distinct dimensions of early experience. Neurosci Biobehav Rev 47:578–591, http://doi.org/10.1016/j.neubiorev.2014.10.012

    PubMed  PubMed Central  Google Scholar 

  53. Arata CM, Langhinrichsen-Rohling J, Bowers D, O’Brien N (2007) Differential correlates of multi-type maltreatment among urban youth. Child Abuse Negl 31(4):393–415, http://doi.org/10.1016/j.chiabu.2006.09.006

    PubMed  Google Scholar 

  54. Dannlowski U, Kugel H, Huber F, Stuhrmann A, Redlich R, Grotegerd D et al (2013) Childhood maltreatment is associated with an automatic negative emotion processing bias in the amygdala. Hum Brain Mapp 34(11):2899–2909, http://doi.org/10.1002/hbm.22112

    PubMed  Google Scholar 

  55. van Harmelen A-L, van Tol M-J, Demenescu LR, van der Wee NJA, Veltman DJ, Aleman A et al (2013) Enhanced amygdala reactivity to emotional faces in adults reporting childhood emotional maltreatment. Soc Cogn Affect Neurosci 8(4):362–369, http://doi.org/10.1093/scan/nss007

    PubMed  Google Scholar 

  56. Bogdan R, Williamson DE, Hariri AR (2012) Mineralocorticoid receptor Iso/Val (rs5522) genotype moderates the association between previous childhood emotional neglect and amygdala reactivity. Am J Psychiatry 169:515–522, http://doi.org/10.1176/appi.ajp.2011.11060855

    PubMed  PubMed Central  Google Scholar 

  57. White MG, Bogdan R, Fisher PM, Muñoz KE, Williamson DE, Hariri AR (2012) FKBP5 and emotional neglect interact to predict individual differences in amygdala reactivity. Genes Brain Behav 11(7):869–878, http://doi.org/10.1111/j.1601-183X.2012.00837.x

    CAS  PubMed  Google Scholar 

  58. Gianaros PJ, Horenstein JA, Hariri AR, Sheu LK, Manuck SB, Matthews KA, Cohen S (2008) Potential neural embedding of parental social standing. Soc Cogn Affect Neurosci 3(2):91–96, http://doi.org/10.1093/scan/nsn003

    PubMed  PubMed Central  Google Scholar 

  59. Evans GW, Swain JE, King AP, Wang X, Javanbakht A, Ho SS et al (2016) Childhood cumulative risk exposure and adult amygdala volume and function. J Neurosci Res 94(6):535–543, http://doi.org/10.1002/jnr.23681

    CAS  PubMed  Google Scholar 

  60. Javanbakht A, King AP, Evans GW, Swain JE, Angstadt M, Phan KL, Liberzon I (2015) Childhood poverty predicts adult amygdala and frontal activity and connectivity in response to emotional faces. Front Behav Neurosci 9(154), http://doi.org/10.3389/fnbeh.2015.00154

  61. Gee DG, Gabard-Durnam LJ, Flannery J, Goff B, Humphreys KL, Telzer EH et al (2013) Early developmental emergence of human amygdala-prefrontal connectivity after maternal deprivation. Proc Natl Acad Sci U S A 110(39):15638–15643, http://doi.org/10.1073/pnas.1307893110

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Maheu FS, Dozier M, Guyer AE, Mandell D, Peloso E, Poeth K, Jenness J (2010) Preliminary study of medial temporal lobe function in youths with a history of caregiver deprivation and emotional neglect. Cogn Affect Behav Neurosci 10(1):34–49, http://doi.org/10.3758/CABN.10.1.34.A

    PubMed  PubMed Central  Google Scholar 

  63. Tottenham N, Hare TA, Millner A, Gilhooly T, Zevin JD, Casey BJ (2011) Elevated amygdala response to faces following early deprivation. Dev Sci 14(2):190–204, http://doi.org/10.1111/j.1467-7687.2010.00971.x

    CAS  PubMed  PubMed Central  Google Scholar 

  64. McCrory EJ, De Brito SA, Kelly PA, Bird G, Sebastian CL, Mechelli A et al (2013) Amygdala activation in maltreated children during pre-attentive emotional processing. Br J Psychiatry 202(4):269–276, http://doi.org/10.1192/bjp.bp.112.116624

    PubMed  Google Scholar 

  65. McLaughlin KA, Peverill M, Gold AL, Alves S, Sheridan MA (2015) Child maltreatment and neural systems underlying emotion regulation. J Am Acad Child Adolesc Psychiatry 54(9):753–762, http://doi.org/10.1016/j.jaac.2015.06.010

    PubMed  PubMed Central  Google Scholar 

  66. Marusak HA, Martin KR, Etkin A, Thomason ME (2014) Childhood trauma exposure disrupts the automatic regulation of emotional processing. Neuropsychopharmacology 40(5):1250–1258, http://doi.org/10.1038/npp.2014.311

    Google Scholar 

  67. McCrory EJ, De Brito SA, Sebastian CL, Mechelli A, Bird G, Kelly PA, Viding E (2011) Heightened neural reactivity to threat in child victims of family violence. Curr Biol 21(23):R947–R948, http://doi.org/10.1016/j.cub.2011.10.015

    CAS  PubMed  Google Scholar 

  68. Swartz JR, Williamson DE, Hariri AR (2015) Developmental change in amygdala reactivity during adolescence: effects of family history for depression and stressful life events. Am J Psychiatry 172(3):276–283, http://doi.org/10.1176/appi.ajp.2014.14020195

    PubMed  Google Scholar 

  69. Jedd K, Hunt RH, Cicchetti D, Hunt E, Cowell RA, Rogosch FA et al (2015) Long-term consequences of childhood maltreatment: altered amygdala functional connectivity. Dev Psychopathol 27:1577–1589, http://doi.org/10.1017/S0954579415000954

    PubMed  PubMed Central  Google Scholar 

  70. Kim P, Evans GW, Angstadt M, Ho SS, Sripada CS, Swain JE (2013) Effects of childhood poverty and chronic stress on emotion regulatory brain function in adulthood. Proc Natl Acad Sci U S A 110(46):18442–18447, http://doi.org/10.1073/pnas.1308240110/-/DCSupplemental.www.pnas.org/cgi/doi/10.1073/pnas.1308240110

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Cicchetti D, Rogosch FA (1996) Equifinality and multifinality in developmental psychopathology. Dev Psychopathol 8:597–600. Retrieved from file://localhost/Users/lornaquandt/Documents/Papers/2007/Unknown/2007-3.pdf\npapers://4f210845-804c-495f-b761-84503ca2694d/Paper/p757

    Google Scholar 

  72. Fan Y, Herrera-Melendez AL, Pestke K, Feeser M, Aust S, Otte C et al (2014) Early life stress modulates amygdala-prefrontal functional connectivity: implications for oxytocin effects. Hum Brain Mapp 35(10):5328–5339, http://doi.org/10.1002/hbm.22553

    PubMed  PubMed Central  Google Scholar 

  73. Herringa RJ, Birn RM, Ruttle PL, Burghy CA, Stodola DE, Davidson RJ, Essex MJ (2013) Childhood maltreatment is associated with altered fear circuitry and increased internalizing symptoms by late adolescence. Proc Natl Acad Sci U S A 110(47):19119–19124, http://doi.org/10.1073/pnas.1310766110

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Thomason ME, Marusak HA, Tocco MA, Vila AM, McGarragle O, Rosenberg DR (2015) Altered amygdala connectivity in urban youth exposed to trauma. Soc Cogn Affect Neurosci 10(11):1460–1468, http://doi.org/10.1093/scan/nsv030

    PubMed  PubMed Central  Google Scholar 

  75. Pagliaccio D, Luby JL, Bogdan R, Agrawal A, Gaffrey MS, Belden AC et al (2015) Amygdala functional connectivity, HPA axis genetic variation, and life stress in children and relations to anxiety and emotion regulation. J Abnorm Psychol 124(4):817–833

    PubMed  PubMed Central  Google Scholar 

  76. Graham AM, Pfeifer JH, Fisher PA, Carpenter S, Fair DA (2015) Early life stress is associated with default system integrity and emotionality during infancy. J Child Psychol Psychiatry 56(11):1212–1222, http://doi.org/10.1111/jcpp.12409

    PubMed  PubMed Central  Google Scholar 

  77. Graham AM, Pfeifer JH, Fisher PA, Lin W, Gao W, Fair DA (2014) The potential of infant fMRI research and the study of early life stress as a promising exemplar. Dev Cogn Neurosci 12:12–39, http://doi.org/10.1016/j.dcn.2014.09.005

    PubMed  PubMed Central  Google Scholar 

  78. Pagliaccio D, Luby JL, Luking KR, Belden AC, Barch DM (2014) Brain–behavior relationships in the experience and regulation of negative emotion in healthy children: Implications for risk for childhood depression. Dev Psychopathol 26:1289–1303

    PubMed  PubMed Central  Google Scholar 

  79. Crozier JC, Wang L, Huettel SA, De Bellis MD (2014) Neural correlates of cognitive and affective processing in maltreated youth with posttraumatic stress symptoms: does gender matter? Dev Psychopathol 26(2):491–513, http://doi.org/10.1017/S095457941400008X

    PubMed  PubMed Central  Google Scholar 

  80. Suzuki H, Luby JL, Botteron KN, Dietrich R, McAvoy MP, Barch DM (2014) Early life stress and trauma and enhanced limbic activation to emotionally valenced faces in depressed and healthy children. J Am Acad Child Adolesc Psychiatry 53(7):800–813.e10. http://doi.org/10.1016/j.jaac.2014.04.013

  81. Gaffrey MS, Barch DM, Luby JL (2016) Amygdala reactivity to sad faces in preschool children: an early neural marker of persistent negative affect. Dev Cogn Neurosci 17:94–100, http://doi.org/10.1016/j.dcn.2015.12.015

    PubMed  PubMed Central  Google Scholar 

  82. Moriceau S, Sullivan RM (2006) Maternal presence serves as a switch between learning fear and attraction in infancy. Nat Neurosci 9(8):1004–1006, http://doi.org/10.1038/nn1733

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Burghy CA, Stodola DE, Ruttle PL, Molloy EK, Armstrong JM, Oler JA et al (2012) Developmental pathways to amygdala-prefrontal function and internalizing symptoms in adolescence. Nat Neurosci 15(12):1736–1741, http://doi.org/10.1038/nn.3257

    CAS  PubMed  PubMed Central  Google Scholar 

  84. McGloin JM, Widom CS (2001) Resilience among abused and neglected children grown up. Dev Psychopathol 13(4):1021–1038, http://doi.org/10.1017/S095457940100414X

    CAS  PubMed  Google Scholar 

  85. Masten AS (2004) Regulatory processes, risk, and resilience in adolescent development. Ann N Y Acad Sci 1021:310–319, http://doi.org/10.1196/annals.1308.036

    PubMed  Google Scholar 

  86. Jaffee SR, Caspi A, Moffitt TE, Polo-Tomás M, Taylor A (2007) Individual, family, and neighborhood factors distinguish resilient from non-resilient maltreated children: a cumulative stressors model. Child Abuse Negl 31(3):231–253, http://doi.org/10.1016/j.chiabu.2006.03.011

    PubMed  PubMed Central  Google Scholar 

  87. Cicchetti D, Blender JA (2006) A multiple-levels-of-analysis perspective on resilience: implications for the developing brain, neural plasticity, and preventive interventions. Ann N Y Acad Sci 1094:248–258, http://doi.org/10.1196/annals.1376.029

    PubMed  Google Scholar 

  88. McLaughlin KA (2016) Future directions in childhood adversity and youth psychopathology. J Clin Child Adolesc Psychol 45(3):361–382, http://doi.org/10.1080/15374416.2015.1110823

    PubMed  PubMed Central  Google Scholar 

  89. Afifi TO, MacMillan HL (2011) Resilience following child maltreatment: a review of protective factors. Can J Psychiatry 56(5):266–272

    PubMed  Google Scholar 

  90. DuMont KA, Widom CS, Czaja SJ (2007) Predictors of resilience in abused and neglected children grown-up: the role of individual and neighborhood characteristics. Child Abuse Negl 31(3):255–274, http://doi.org/10.1016/j.chiabu.2005.11.015

    PubMed  Google Scholar 

  91. Collishaw S, Pickles A, Messer J, Rutter M, Shearer C, Maughan B (2007) Resilience to adult psychopathology following childhood maltreatment: evidence from a community sample. Child Abuse Negl 31(3):211–229, http://doi.org/10.1016/j.chiabu.2007.02.004

    PubMed  Google Scholar 

  92. Miller-Graff LE, Cater ÅK, Howell KH, Graham-Bermann SA (2016) Parent-child warmth as a potential mediator of childhood exposure to intimate partner violence and positive adulthood functioning. Anxiety Stress Coping 29(3):259–273, http://doi.org/10.1080/10615806.2015.1028030

    PubMed  Google Scholar 

  93. Hennessy MB, Kaiser S, Sachser N (2009) Social buffering of the stress response: diversity, mechanisms, and functions. Front Neuroendocrinol 30(4):470–482, http://doi.org/10.1016/j.yfrne.2009.06.001

    CAS  PubMed  Google Scholar 

  94. Kikusui T, Winslow JT, Mori Y (2006) Social buffering: relief from stress and anxiety. Philos Trans R Soc B Biol Sci 361(1476):2215–2228, http://doi.org/10.1098/rstb.2006.1941

    CAS  Google Scholar 

  95. Hostinar CE, Johnson AE, Gunnar MR (2014) Parent support is less effective in buffering cortisol stress reactivity for adolescents compared to children. Dev Sci 2:281–297, http://doi.org/10.1111/desc.12195

    Google Scholar 

  96. Gee DG, Gabard-Durnam L, Telzer EH, Humphreys KL, Goff B, Shapiro M et al (2014) Maternal buffering of human amygdala-prefrontal circuitry during childhood but not during adolescence. Psychol Sci 25(11):2067–2078, http://doi.org/10.1177/0956797614550878

    PubMed  Google Scholar 

  97. Troller-Renfree S, Mcdermott JM, Nelson CA, Zeanah CH, Fox NA (2015) The effects of early foster care intervention on attention biases in previously institutionalized children in Romania. Dev Sci 18(5):713–722, http://doi.org/10.1111/desc.12261

    PubMed  Google Scholar 

  98. Troller-renfree S, Mclaughlin KA, Sheridan MA, Nelson CA, Zeanah CH, Fox NA (2016) The benefits of a positive attention bias amongst children with a history of psychosocial deprivation. Biol Psychol. http://doi.org/10.1016/j.biopsycho.2016.04.008

  99. Hostinar CE, Johnson AE, Gunnar MR (2015) Early social deprivation and the social buffering of cortisol stress responses in late childhood: an experimental study. Dev Psychol 51(11):1597–1608

    PubMed  PubMed Central  Google Scholar 

  100. Pechtel P, Lyons-Ruth K, Anderson CM, Teicher MH (2014) Sensitive periods of amygdala development: the role of maltreatment in preadolescence. Neuroimage 97:236–244, http://doi.org/10.1016/j.neuroimage.2014.04.025

    PubMed  Google Scholar 

  101. Goff B, Tottenham N (2015) Early-life adversity and adolescent depression: mechanisms involving the ventral striatum. CNS Spectr 20(4):337–345, http://doi.org/10.1017/S1092852914000674

    PubMed  Google Scholar 

  102. Heim C, Binder EB (2012) Current research trends in early life stress and depression: review of human studies on sensitive periods, gene-environment interactions, and epigenetics. Exp Neurol 233(1):102–111, http://doi.org/10.1016/j.expneurol.2011.10.032

    PubMed  Google Scholar 

  103. Uher R, McGuffin P (2008) The moderation by the serotonin transporter gene of environmental adversity in the aetiology of mental illness: review and methodological analysis. Mol Psychiatry 13(2):131–146, http://doi.org/10.1038/sj.mp.4002067

    CAS  PubMed  Google Scholar 

  104. Casey BJ, Glatt CE, Tottenham N, Soliman F, Bath K, Amso D et al (2009) Brain-derived neurotrophic factor as a model system for examining gene by environment interactions across development. Neuroscience 164(1):108–120, http://doi.org/10.1016/j.neuroscience.2009.03.081

    CAS  PubMed  Google Scholar 

  105. Scarr S, Mccartney K (1983) How people make their own environments: a theory of genotype → environment effects author (s): Sandra Scarr and Kathleen McCartney Published by: Wiley on behalf of the Society for Research in Child Development Stable URL: http://www.jstor.org/stable/. Child Dev 54(2):424–435

    CAS  PubMed  Google Scholar 

  106. Swartz JR, Hariri AR, Williamson DE (2016) An epigenetic mechanism links socioeconomic status to changes in depression-related brain function in high-risk adolescents. Mol Psychiatry. http://doi.org/10.1038/mp.2016.82

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Acknowledgements

This work was supported by the NIMH under grant R01MH091864 (N. Tottenham, PI), an NSF Conference Grant conference grant BCS-1439258 (N. Tottenham, co-I), and the Dana Foundation (N. Tottenham, PI), and the NSF Graduate Research Fellowship Program under Grant No. DGE-16-44869 (M. R. VanTieghem). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institute of Mental Health, the National Institutes of Health, the National Science Foundation, or the Dana Foundation.

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VanTieghem, M.R., Tottenham, N. (2017). Neurobiological Programming of Early Life Stress: Functional Development of Amygdala-Prefrontal Circuitry and Vulnerability for Stress-Related Psychopathology. In: Vermetten, E., Baker, D.G., Risbrough, V.B. (eds) Behavioral Neurobiology of PTSD. Current Topics in Behavioral Neurosciences, vol 38. Springer, Cham. https://doi.org/10.1007/7854_2016_42

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