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Developmental Contributors to Trauma Response: The Importance of Sensitive Periods, Early Environment, and Sex Differences

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Behavioral Neurobiology of PTSD

Abstract

This review considers early factors that interact with development to contribute to later trauma responses, including developmental sensitive periods, the effects of early environment, and the emergence of sex differences. We also describe development of neural substrates that have been associated with posttraumatic stress disorder and specifically focus on fear behavior and circuitry. Emerging evidence suggests that there may be developmental shifts around age 10 in these underlying circuits that may contribute to vulnerability. We also discuss age-related changes in the importance of caregiver availability as positive buffering factors. Hormonal changes later in development with onset during puberty appear to further shape development trajectories toward risk or resilience. We highlight these recent findings as well as the great need for further longitudinal research from middle childhood through early adulthood.

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References

  • Administration on Children, Youth and Families, US Department of Health and Human Services (2012) Child maltreatment

    Google Scholar 

  • Admon R, Lubin G, Stern O, Rosenberg K, Sela L, Ben-Ami H, Hendler T (2009) Human vulnerability to stress depends on amygdala’s predisposition and hippocampal plasticity. Proc Natl Acad Sci 106(33):14120–14125. doi:10.1073/pnas.0903183106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Admon R, Lubin G, Rosenblatt JD, Stern O, Kahn I, Assaf M, Hendler T (2013) Imbalanced neural responsivity to risk and reward indicates stress vulnerability in humans. Cereb Cortex 23(1):28–35. doi:10.1093/cercor/bhr369

    Article  PubMed  Google Scholar 

  • Barr GA, Moriceau S, Shionoya K, Muzny K, Gao P, Wang S, Sullivan RM (2009) Transitions in infant learning are modulated by dopamine in the amygdala. Nat Neurosci 12(11):1367–1369 http://www.nature.com/neuro/journal/v12/n11/suppinfo/nn.2403_S1.html

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bayart F, Hayashi KT, Faull KF, Barchas JD, Levine S (1990) Influence of maternal proximity on behavioral and physiological responses to separation in infant rhesus monkeys (Macaca mulatta). Behav Neurosci 104(1):98–107

    CAS  PubMed  Google Scholar 

  • Beesdo K, Knappe S, Pine DS (2009) Anxiety and anxiety disorders in children and adolescents: developmental issues and implications for DSM-V. Psychiatr Clin North Am 32(3):483–524 http://dx.doi.org/10.1016/j.psc.2009.06.002

    PubMed  PubMed Central  Google Scholar 

  • Bevans K, Cerbone AB, Overstreet S (2009) The interactive effects of elevated mid-afternoon cortisol and trauma history on PTSD symptoms in children: a preliminary study. Psychoneuroendocrinology 34(10):1582–1585. doi:10.1016/j.psyneuen.2009.04.010

    Article  CAS  PubMed  Google Scholar 

  • Bick J, Nelson CA (2016) Early adverse experiences and the developing brain. Neuropsychopharmacology 41(1):177–196

    CAS  PubMed  Google Scholar 

  • Björkenstam E, Burström B, Brännström L, Vinnerljung B, Björkenstam C, Pebley AR (2015) Cumulative exposure to childhood stressors and subsequent psychological distress. An analysis of US panel data. Soc Sci Med 142:109–117 http://dx.doi.org/10.1016/j.socscimed.2015.08.006

    PubMed  Google Scholar 

  • Bos K, Zeanah CH, Fox NA, Drury SS, McLaughlin KA, Nelson CA (2011) Psychiatric outcomes in young children with a history of institutionalization. Harv Rev Psychiatry 19(1):15–24. doi:10.3109/10673229.2011.549773

    Article  PubMed  PubMed Central  Google Scholar 

  • Burghy CA, Stodola DE, Ruttle PL, Molloy EK, Armstrong JM, Oler JA, Fox ME, Hayes AS, Kalin NH, Essex MJ (2012) Developmental pathways to amygdala-prefrontal function and internalizing symptoms in adolescence. Nat Neurosci 15(12):1736–1741

    CAS  PubMed  PubMed Central  Google Scholar 

  • Callaghan BL, Tottenham N (2016) The neuro-environmental loop of plasticity: a cross-species analysis of parental effects on emotion circuitry development following typical and adverse caregiving. Neuropsychopharmacology 41(1):163–176

    PubMed  Google Scholar 

  • Chen LS, Tzeng WY, Chuang JY, Cherng CG, Gean PW, Yu L (2014) Roles of testosterone and amygdaloid LTP induction in determining sex differences in fear memory magnitude. Horm Behav 66(3):498–508. doi:10.1016/j.yhbeh.2014.07.008

    Article  CAS  PubMed  Google Scholar 

  • Clark AS, Maclusky NJ, Goldman-Rakic PS (1988) Androgen binding and metabolism in the cerebral cortex of the developing rhesus monkey. Endocrinology 123(2):932–940. doi:10.1210/endo-123-2-932

    Article  CAS  PubMed  Google Scholar 

  • Clarke AS, Snipes M (1998) Early behavioral development and temperamental traits in mother- vs peer-reared rhesus monkeys. Primates 39(4):433–448

    Google Scholar 

  • Coe CL, Mendoza SP, Smotherman WP, Levine S (1978) Mother-infant attachment in the squirrel monkey: adrenal response to separation. Behav Biol 22(2):256–263. doi:10.1016/S0091-6773(78)92305-2

    Article  CAS  PubMed  Google Scholar 

  • Cohen JA, Scheeringa MS (2009) Post-traumatic stress disorder diagnosis in children: challenges and promises. Dialogues Clin Neurosci 11(1):91–99

    PubMed  PubMed Central  Google Scholar 

  • Cohen P, Cohen J, Kasen S, Velez CN, Hartmark C, Johnson J, Rojas M, Brook J, Streuning EL (1993) An epidemiological study of disorders in late childhood and adolescence--I. Age- and gender-specific prevalence. J Child Psychol Psychiatry 34(6):851–867

    CAS  PubMed  Google Scholar 

  • Cui M, Yang Y, Yang J, Zhang J, Han H, Ma W, Li H, Mao R, Xu L, Hao W, Cao J (2006) Enriched environment experience overcomes the memory deficits and depressive-like behavior induced by early life stress. Neurosci Lett 404(1–2):208–212. doi:10.1016/j.neulet.2006.05.048

    Article  CAS  PubMed  Google Scholar 

  • DaSilva JK, Husain E, Lei Y, Mann GL, Tejani-Butt S, Morrison AR (2011) Social partnering significantly reduced rapid eye movement sleep fragmentation in fear-conditioned, stress-sensitive Wistar-Kyoto rats. Neuroscience 199:193–204

    CAS  PubMed  Google Scholar 

  • Davis M, Falls WA, Campeau S, Kim M (1993) Fear-potentiated startle: a neural and pharmacological analysis. Behav Brain Res 58:175–198

    CAS  PubMed  Google Scholar 

  • De Bellis MD, Keshavan M, Shifflett H, Iyengar S, Beers SR, Hall J, et al (2002) Brain structures in pediatric maltreatment-related PTSD: a sociodemographically matched study. Biol Psychiatry 52:1066–1078

    Google Scholar 

  • Dell'Osso L, Carmassi C, Massimetti G, Stratta P, Riccardi I, Capanna C, Akiskal KK, Akiskal HS, Rossi A (2013) Age, gender and epicenter proximity effects on post-traumatic stress symptoms in L’Aquila 2009 earthquake survivors. J Affect Disord 146(2):174–180

    CAS  PubMed  Google Scholar 

  • Dinenberg RE, McCaslin SE, Bates MN, Cohen BE (2014) Social support may protect against development of posttraumatic stress disorder: findings from the heart and soul study. Am J Health Promot 28(5):294–297. doi:10.4278/ajhp.121023-QUAN-511

    Article  PubMed  Google Scholar 

  • Engman J, Linnman C, Van Dijk KR, Milad MR (2016) Amygdala subnuclei resting-state functional connectivity sex and estrogen differences. Psychoneuroendocrinology 63:34–42. doi:10.1016/j.psyneuen.2015.09.012

    Article  CAS  PubMed  Google Scholar 

  • Fanselow MS (1994) Neural organization of the defensive behavior system responsible for fear. Psychon Bull Rev 1:429–438

    CAS  PubMed  Google Scholar 

  • Fonzo GA, Simmons AN, Thorp SR, Norman SB, Paulus MP, Stein MB (2010) Exaggerated and disconnected insular-amygdalar blood oxygenation level-dependent response to threat-related emotional faces in women with intimate-partner violence posttraumatic stress disorder. Biol Psychiatry 68(5):433–441. doi:10.1016/J.Biopsych.2010.04.028

    Article  PubMed  PubMed Central  Google Scholar 

  • Francis DD, Diorio J, Plotsky PM, Meaney MJ (2002) Environmental enrichment reverses the effects of maternal separation on stress reactivity. J Neurosci 22(18):7840–7843

    CAS  PubMed  PubMed Central  Google Scholar 

  • Funayama ES, Grillon C, Davis M, Phelps EA (2001) A double dissociation in the affective modulation of startle in humans: effects of unilateral temporal lobectomy. J Cogn Neurosci 13(6):721–729

    CAS  PubMed  Google Scholar 

  • Gamwell K, Nylocks M, Cross D, Bradley B, Norrholm SD, Jovanovic T (2015) Fear conditioned responses and PTSD symptoms in children: sex differences in fear-related symptoms. Dev Psychobiol 57(7):799–808. doi:10.1002/dev.21313

    Article  PubMed  PubMed Central  Google Scholar 

  • Gee DG, Humphreys KL, Flannery J, Goff B, Telzer EH, Shapiro M, Hare TA, Bookheimer SY, Tottenham N (2013a) A developmental shift from positive to negative connectivity in human amygdala–Prefrontal circuitry. J Neurosci 33(10):4584–4593. doi:10.1523/jneurosci.3446-12.2013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gee DG, Gabard-Durnam LJ, Flannery J, Goff B, Humphreys KL, Telzer EH, Hare TA, Bookheimer SY, Tottenham N (2013b) Early developmental emergence of human amygdala-prefrontal connectivity after maternal deprivation. Proc Natl Acad Sci U S A 110(39):15638–15643. doi:10.1073/pnas.1307893110

    Article  PubMed  PubMed Central  Google Scholar 

  • Gee DG, Gabard-Durnam L, Telzer EH, Humphreys KL, Goff B, Shapiro M, Flannery J, Lumian DS, Fareri DS, Caldera C, Tottenham N (2014) Maternal buffering of human amygdala-prefrontal circuitry during childhood but not during adolescence. Psychol Sci 25(11):2067–2078. doi:10.1177/0956797614550878

    Article  PubMed  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

    CAS  PubMed  Google Scholar 

  • Giedd JN, Blumenthal J, Jeffries NO, Castellanos FX, Liu H, Zijdenbos A, Paus T, Evans AC, Rapoport JL (1999) Brain development during childhood and adolescence: a longitudinal MRI study. Nat Neurosci 2(10):861–863

    CAS  PubMed  Google Scholar 

  • Giedd JN, Raznahan A, Alexander-Bloch A, Schmitt E, Gogtay N, Rapoport JL (2015) Child psychiatry branch of the National Institute of Mental Health longitudinal structural magnetic resonance imaging study of human brain development. Neuropsychopharmacology 40(1):43–49. doi:10.1038/npp.2014.236

    Article  PubMed  Google Scholar 

  • Glenn CR, Klein DN, Lissek S, Britton JC, Pine DS, Hajcak G (2011) The development of fear learning and generalization in 8–13 year-olds. Dev Psychobiol 54(7):675–684. doi:10.1002/dev.20616

    Article  PubMed  PubMed Central  Google Scholar 

  • Glover EM, Jovanovic T, Mercer KB, Kerley K, Bradley B, Ressler KJ, Norrholm SD (2012) Estrogen levels are associated with extinction deficits in women with posttraumatic stress disorder. Biol Psychiatry 72(1):19–24. doi:10.1016/j.biopsych.2012.02.031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Glover EM, Mercer KB, Norrholm SD, Davis M, Duncan E, Bradley B, Ressler KJ, Jovanovic T (2013) Inhibition of fear is differentially associated with cycling estrogen levels in women. J Psychiatry Neurosci 38(3):120129

    Google Scholar 

  • Gogtay N, Giedd JN, Lusk L, Hayashi KM, Greenstein D, Vaituzis AC, Nugent TF, Herman DH, Clasen LS, Toga AW, Rapoport JL, Thompson PM (2004) Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci U S A 101(21):8174–8179. doi:10.1073/pnas.0402680101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guyer AE, Monk CS, McClure-Tone EB, Nelson EE, Roberson-Nay R, Adler AD, Fromm SJ, Leibenluft E, Pine DS, Ernst M (2008) A developmental examination of amygdala response to facial expressions. J Cogn Neurosci 20(9):1565–1582. doi:10.1162/jocn.2008.20114

    Article  PubMed  PubMed Central  Google Scholar 

  • Hendriksen H, Prins J, Olivier B, Oosting RS (2010) Environmental enrichment induces behavioral recovery and enhanced hippocampal cell proliferation in an antidepressant-resistant animal model for PTSD. PLoS One 5(8):e11943. doi:10.1371/journal.pone.0011943

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. doi:10.1073/pnas.1310766110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hill HM, Levermore M, Twaite J, Jones LP (1996) Exposure to community violence and social support as predictors of anxiety and social and emotional behavior among African American children. J Child Fam Stud 5(4):399–399

    Google Scholar 

  • Hostinar CE, Johnson AE, Gunnar MR (2015) Parent support is less effective in buffering cortisol stress reactivity for adolescents compared to children. Dev Sci 18(2):281–297. doi:10.1111/desc.12195

    Article  PubMed  Google Scholar 

  • Hu S, Pruessner JC, Coupe P, Collins DL (2013) Volumetric analysis of medial temporal lobe structures in brain development from childhood to adolescence. Neuroimage 74:276–287. doi:10.1016/j.neuroimage.2013.02.032

    Article  PubMed  Google Scholar 

  • Humphreys KL, Gleason MM, Drury SS, Miron D, Nelson 3rd 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. doi:10.1016/S2215-0366(15)00095-4

    Article  PubMed  PubMed Central  Google Scholar 

  • Hwang MJ, Zsido RG, Song H, Pace-Schott EF, Miller KK, Lebron-Milad K, Marin M-F, Milad MR (2015) Contribution of estradiol levels and hormonal contraceptives to sex differences within the fear network during fear conditioning and extinction. BMC Psychiatry 15(1):295

    PubMed  PubMed Central  Google Scholar 

  • Jovanovic T, Norrholm SD (2011) Neural mechanisms of impaired fear inhibition in posttraumatic stress disorder. Front Behav Neurosci:5. doi:10.3389/fnbeh.2011.00044

  • Jovanovic T, Ressler KJ (2010) How the neurocircuitry and genetics of fear inhibition may inform our understanding of PTSD. Am J Psychiatry 167(6):648–662. doi:10.1176/appi.ajp.2009.09071074

    Article  PubMed  PubMed Central  Google Scholar 

  • Jovanovic T, Norrholm SD, Blanding NQ, Davis M, Duncan E, Bradley B, Ressler KJ (2010) Impaired fear inhibition is a biomarker of PTSD but not depression. Depress Anxiety 27(3):244–251. doi:10.1002/da.20663

    Article  PubMed  PubMed Central  Google Scholar 

  • Jovanovic T, Norrholm SD, Davis J, Mercer KB, Almli L, Nelson A, Cross D, Smith A, Ressler KJ, Bradley B (2013) PAC1 receptor (ADCYAP1R1) genotype is associated with dark-enhanced startle in children. Mol Psychiatry 18(7):742–743. doi:10.1038/mp.2012.98

    Article  CAS  PubMed  Google Scholar 

  • Jovanovic T, Nylocks KM, Gamwell KL, Smith A, Davis TA, Norrholm SD, Bradley B (2014) Development of fear acquisition and extinction in children: effects of age and anxiety. Neurobiol Learn Mem 113:135–142. doi:10.1016/j.nlm.2013.10.016

    Article  PubMed  Google Scholar 

  • Kaufman J, Yang B-Z, Douglas-Palumberi H, Grasso D, Lipschitz D, Houshyar S, Krystal JH, Gelernter J (2006) Brain-derived neurotrophic factor–5-HTTLPR Gene interactions and environmental modifiers of depression in children. Biol Psychiatry 59(8):673–680 http://dx.doi.org/10.1016/j.biopsych.2005.10.026

    CAS  PubMed  Google Scholar 

  • Keding TJ, Herringa RJ (2015) Abnormal structure of fear circuitry in pediatric post-traumatic stress disorder. Neuropsychopharmacology 40(3):537–545. doi:10.1038/npp.2014.239

    Article  PubMed  Google Scholar 

  • Kessler RC, Sonnega A, Bromet E, Hughes M, Nelson CB (1995) Posttraumatic stress disorder in the National Comorbidity Survey. Arch Gen Psychiatry 52(12):1048–1060. doi:10.1001/archpsyc.1995.03950240066012

    Article  CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kline A, Ciccone DS, Weiner M, Interian A, St. Hill L, Falca-Dodson M, Black CM, Losonczy M (2013) Gender differences in the risk and protective factors associated with PTSD: a prospective study of National Guard troops deployed to Iraq. Psychiatry 76(3):256–272

    PubMed  Google Scholar 

  • Koch SB, van Zuiden M, Nawijn L, Frijling JL, Veltman DJ, Olff M (2016) Intranasal oxytocin normalizes amygdala functional connectivity in post-traumatic stress disorder. Neuropsychopharmacology. doi:10.1038/npp.2016.1

    Article  PubMed  PubMed Central  Google Scholar 

  • Kolb B, Mychasiuk R, Muhammad A, Li Y, Frost DO, Gibb R (2012) Experience and the developing prefrontal cortex. Proc Natl Acad Sci 109(Supplement 2):17186–17193. doi:10.1073/pnas.1121251109

    Article  PubMed  PubMed Central  Google Scholar 

  • Lebel C, Gee M, Camicioli R, Wieler M, Martin W, Beaulieu C (2012) Diffusion tensor imaging of white matter tract evolution over the lifespan. Neuroimage 60(1):340–352

    CAS  PubMed  Google Scholar 

  • LeDoux J (1992) Brain mechanisms of emotion and emotional learning. Curr Opin Neurobiol 2:191–197

    CAS  PubMed  Google Scholar 

  • Levine S, Johnson DF, Gonzalez CA (1985) Behavioral and hormonal responses to separation in infant rhesus monkeys and mothers. Behav Neurosci 99(3):399–410

    CAS  PubMed  Google Scholar 

  • Li S, Kim JH, Richardson R (2012) Differential involvement of the medial prefrontal cortex in the expression of learned fear across development. Behav Neurosci 126:217–225

    PubMed  Google Scholar 

  • Lissek S, Bradford DE, Alvarez RP, Burton P, Espensen-Sturges T, Reynolds RC, Grillon C (2014) Neural substrates of classically conditioned fear-generalization in humans: a parametric fMRI study. Soc Cogn Affect Neurosci 9(8):1134–1142. doi:10.1093/scan/nst096

    Article  PubMed  Google Scholar 

  • MacLusky NJ, Naftolin F, Goldman-Rakic PS (1986) Estrogen formation and binding in the cerebral cortex of the developing rhesus monkey. Proc Natl Acad Sci U S A 83(2):513–516

    CAS  PubMed  PubMed Central  Google Scholar 

  • Makley AT, Falcone Jr RA (2010) Posttraumatic stress disorder in the pediatric trauma patient. Semin Pediatr Surg 19(4):292–299. doi:10.1053/j.sempedsurg.2010.06.006

    Article  PubMed  Google Scholar 

  • McClure EB, Monk CS, Nelson EE, Zarahn E, Leibenluft E, Bilder RM, Charney DS, Ernst M, Pine DS (2004) A developmental examination of gender differences in brain engagement during evaluation of threat. Biol Psychiatry 55(11):1047–1055. doi:10.1016/j.biopsych.2004.02.013

    Article  PubMed  Google Scholar 

  • McLaughlin KA, Fox NA, Zeanah CH, Nelson CA (2011) Adverse rearing environments and neural development in children: the development of frontal electroencephalogram asymmetry. Biol Psychiatry 70(11):1008–1015. doi:10.1016/j.biopsych.2011.08.006

    Article  PubMed  PubMed Central  Google Scholar 

  • McManis MH, Bradley MM, Berg WK, Cuthbert BN, Lang PJ (2001) Emotional reactions in children: verbal, physiological, and behavioral responses to affective pictures. Psychophysiology 38(2):222–231

    CAS  PubMed  Google Scholar 

  • Michalska KJ, Shechner T, Hong M, Britton JC, Leibenluft E, Pine DS, Fox NA (2016) A developmental analysis of threat/safety learning and extinction recall during middle childhood. J Exp Child Psychol 146:95–105. doi:10.1016/j.jecp.2016.01.008

    Article  PubMed  PubMed Central  Google Scholar 

  • Michopoulos V, Rothbaum AO, Corwin E, Bradley B, Ressler KJ, Jovanovic T (2014) Psychophysiology and posttraumatic stress disorder symptom profile in pregnant African-American women with trauma exposure. Arch Womens Ment Health 18(4):639–648

    PubMed  PubMed Central  Google Scholar 

  • Mithoefer MC, Grob CS, Brewerton TD (2016) Novel psychopharmacological therapies for psychiatric disorders: psilocybin and MDMA. Lancet Psychiatry 3(5):481–488. doi:10.1016/S2215-0366(15)00576-3

    Article  PubMed  Google Scholar 

  • 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://www.nature.com/neuro/journal/v9/n8/suppinfo/nn1733_S1.html

    CAS  PubMed  PubMed Central  Google Scholar 

  • Moulson MC, Westerlund A, Fox NA, Zeanah CH, Nelson CA (2009) The effects of early experience on face recognition: an event-related potential study of institutionalized children in Romania. Child Dev 80(4):1039–1056. doi:10.1111/j.1467-8624.2009.01315.x

    Article  PubMed  Google Scholar 

  • Nelson CA, Zeanah CH, Fox NA, Marshall PJ, Smyke AT, Guthrie D (2007) Cognitive recovery in socially deprived young children: the Bucharest early intervention project. Science 318(5858):1937–1940. doi:10.1126/science.1143921

    Article  CAS  PubMed  Google Scholar 

  • Nemeroff CB, Bremner JD, Foa EB, Mayberg HS, North CS, Stein MB (2006) Posttraumatic stress disorder: a state-of-the-science review. J Psychiatr Res 40(1):1–21

    PubMed  Google Scholar 

  • Nithianantharajah J, Hannan AJ (2006) Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat Rev Neurosci 7(9):697–709

    CAS  PubMed  Google Scholar 

  • Nowakowska E, Kus K, Ratajczak P, Cichocki M, Woźniak A (2014) The influence of aripiprazole, olanzapine and enriched environment on depressant-like behavior, spatial memory dysfunction and hippocampal level of BDNF in prenatally stressed rats. Pharmacol Rep 66(3):404–411. doi:10.1016/j.pharep.2013.12.008

    Article  CAS  PubMed  Google Scholar 

  • Pagliaccio D, Luby JL, Gaffrey MS, Belden AC, Botteron KN, Harms MP, Barch DM (2013) Functional brain activation to emotional and nonemotional faces in healthy children: evidence for developmentally undifferentiated amygdala function during the school-age period. Cogn Affect Behav Neurosci 13(4):771–789. doi:10.3758/s13415-013-0167-5

    Article  PubMed  Google Scholar 

  • Pagliaccio D, Luby JL, Bogdan R, Agrawal A, Gaffrey MS, Belden AC, Botteron KN, Harms MP, Barch DM (2015) HPA axis genetic variation, pubertal status, and sex interact to predict amygdala and hippocampus responses to negative emotional faces in school-age children. Neuroimage 109:1–11. doi:10.1016/j.neuroimage.2015.01.017

    Article  PubMed  Google Scholar 

  • 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. doi:10.1016/j.neuroimage.2014.04.025

    Article  PubMed  Google Scholar 

  • Pietrzak RH, Johnson DC, Goldstein MB, Malley JC, Southwick SM (2009) Psychological resilience and postdeployment social support protect against traumatic stress and depressive symptoms in soldiers returning from Operations Enduring Freedom and Iraqi Freedom. Depress Anxiety 26(8):745–751. doi:10.1002/da.20558

    Article  PubMed  Google Scholar 

  • Pietrzak RH, Johnson DC, Goldstein MB, Malley JC, Rivers AJ, Morgan CA, Southwick SM (2010) Psychosocial buffers of traumatic stress, depressive symptoms, and psychosocial difficulties in veterans of Operations Enduring Freedom and Iraqi Freedom: the role of resilience, unit support, and postdeployment social support. J Affect Disord 120(1–3):188–192

    PubMed  Google Scholar 

  • Pohlack ST, Nees F, Ruttorf M, Cacciaglia R, Winkelmann T, Schad LR, Witt SH, Rietschel M, Flor H (2015) Neural mechanism of a sex-specific risk variant for posttraumatic stress disorder in the Type I receptor of the pituitary adenylate cyclase activating polypeptide. Biol Psychiatry 78(12):840–847

    CAS  PubMed  Google Scholar 

  • Rauch SL, Whalen PJ, Shin LM, McInerney SC, Macklin ML, Lasko NB, Orr SP, Pitman RK (2000) Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder: a functional MRI study. Biol Psychiatry 47(9):769–776

    CAS  PubMed  Google Scholar 

  • Ressler KJ, Mercer KB, Bradley B, Jovanovic T, Mahan A, Kerley K, Norrholm SD, Kilaru V, Smith AK, Myers AJ, Ramirez M, Engel A, Hammack SE, Toufexis D, Braas KM, Binder EB, May V (2011) Post-traumatic stress disorder is associated with PACAP and the PAC1 receptor. Nature 470(7335):492–497. doi:10.1038/nature09856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roselli CE, Klosterman S, Resko JA (2001) Anatomic relationships between aromatase and androgen receptor mRNA expression in the hypothalamus and amygdala of adult male cynomolgus monkeys. J Comp Neurol 439(2):208–223

    CAS  PubMed  Google Scholar 

  • Ros-Simó C, Valverde O (2012) Early-life social experiences in mice affect emotional behaviour and hypothalamic-pituitary-adrenal axis function. Pharmacol Biochem Behav 102(3):434–441

    PubMed  Google Scholar 

  • Sanchez M, Ladd C, Plotsky P (2001) Early adverse experience as a developmental risk factor for later psychopathology: evidence from rodent and primate models. Dev Psychopathol 13(3):419

    CAS  PubMed  Google Scholar 

  • Sarro EC, Wilson DA, Sullivan RM (2014) Maternal regulation of infant brain state. Curr Biol 24(14):1664–1669. doi:10.1016/j.cub.2014.06.017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schüssler-Fiorenza Rose SM, Xie D, Stineman M (2014) Adverse childhood experiences and disability in U.S. adults. PM R 6(8):670–680. doi:10.1016/j.pmrj.2014.01.013

    Article  PubMed  Google Scholar 

  • Schwartz CE, Kunwar PS, Greve DN, Kagan J, Snidman NC, Bloch RB (2012) A phenotype of early infancy predicts reactivity of the amygdala in male adults. Mol Psychiatry 17(10):1042–1050. doi:10.1038/mp.2011.96

    Article  CAS  PubMed  Google Scholar 

  • Shannon C, Champoux M, Suomi SJ (1998) Rearing condition and plasma cortisol in rhesus monkey infants. Am J Primatol 46(4):311–321. doi:10.1002/(SICI)1098-2345(1998)46:4<311::AID-AJP3>3.0.CO;2-L

    Article  CAS  PubMed  Google Scholar 

  • Shansky RM, Hamo C, Hof PR, McEwen BS, Morrison JH (2009) Stress-induced dendritic remodeling in the prefrontal cortex is circuit specific. Cereb Cortex 19(10):2479–2484

    PubMed  PubMed Central  Google Scholar 

  • Shansky RM, Hamo C, Hof PR, Lou W, McEwen BS, Morrison JH (2010) Estrogen promotes stress sensitivity in a prefrontal cortex-amygdala pathway. Cereb Cortex 20(11):2560–2567. doi:10.1093/cercor/bhq003

    Article  PubMed  PubMed Central  Google Scholar 

  • Shaw P, Greenstein D, Lerch J, Clasen L, Lenroot R, Gogtay N, Evans A, Rapoport J, Giedd J (2006) Intellectual ability and cortical development in children and adolescents. Nature 440(7084):676

    CAS  PubMed  Google Scholar 

  • Shechner T, Britton JC, Ronkin EG, Jarcho JM, Mash JA, Michalska KJ, Leibenluft E, Pine DS (2015) Fear conditioning and extinction in anxious and nonanxious youth and adults: examining a novel developmentally appropriate fear-conditioning task. Depress Anxiety 32(4):277–288. doi:10.1002/da.22318

    Article  PubMed  Google Scholar 

  • Shin LM, Wright CI, Cannistraro PA, Wedig MM, McMullin K, Martis B, Macklin ML, Lasko NB, Cavanagh SR, Krangel TS, Orr SP, Pitman RK, Whalen PJ, Rauch SL (2005) A functional magnetic resonance imaging study of amygdala and medial prefrontal cortex responses to overtly presented fearful faces in posttraumatic stress disorder. Arch Gen Psychiatry 62(3):273–281. doi:10.1001/archpsyc.62.3.273

    Article  PubMed  Google Scholar 

  • Shin LM, Liberzon I (2010) The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology 35(1):169–191

    PubMed  Google Scholar 

  • Spinelli S, Chefer S, Suomi SJ, Higley JD, Barr CS, Stein E (2009) Early-life stress induces long-term morphologic changes in primate brain. Arch Gen Psychiatry 66(6):658–665. doi:10.1001/archgenpsychiatry.2009.52

    Article  PubMed  Google Scholar 

  • Sripada RK, King AP, Garfinkel SN, Wang X, Sripada CS, Welsh RC, Liberzon I (2012) Altered resting-state amygdala functional connectivity in men with posttraumatic stress disorder. J Psychiatry Neurosci 37(4):241–249. doi:10.1503/jpn.110069

    Article  PubMed  PubMed Central  Google Scholar 

  • Steven BK, Williams G, Najman J, Alati R (2013) Exploring the female specific risk to partial and full PTSD following physical assault. J Trauma Stress 26(1):86

    Google Scholar 

  • Stevens JS, Hamann S (2012) Sex differences in brain activation to emotional stimuli: a meta-analysis of neuroimaging studies. Neuropsychologia 50(7):1578–1593. doi:10.1016/j.neuropsychologia.2012.03.011

    Article  PubMed  Google Scholar 

  • Stevens JS, Jovanovic T, Fani N, Ely TD, Glover EM, Bradley B, Ressler KJ (2013) Disrupted amygdala-prefrontal functional connectivity in civilian women with posttraumatic stress disorder. J Psychiatr Res 47(10):1469–1478. doi:10.1016/j.jpsychires.2013.05.031

    Article  PubMed  PubMed Central  Google Scholar 

  • Stevens JS, Almli LM, Fani N, Gutman DA, Bradley B, Norrholm SD, Reiser E, Ely TD, Dhanani R, Glover EM, Jovanovic T, Ressler KJ (2014) PACAP receptor gene polymorphism impacts fear responses in the amygdala and hippocampus. Proc Natl Acad Sci U S A 111(8):3158–3163. doi:10.1073/pnas.1318954111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suitts S (2015) A new majority: low income students now a majority in the Nation’s Public Schools. Southern Education Foundation Report

    Google Scholar 

  • Sullivan RM, Landers M, Yeaman B, Wilson DA (2000) Neurophysiology: good memories of bad events in infancy. Nature 407(6800):38–39

    CAS  PubMed  PubMed Central  Google Scholar 

  • Takuma K, Ago Y, Matsuda T (2011) Preventive effects of an enriched environment on rodent psychiatric disorder models. J Pharmacol Sci 117(2):71–76. doi:10.1254/jphs.11R07CP

    Article  CAS  PubMed  Google Scholar 

  • Tolin DF, Foa EB (2006) Sex differences in trauma and posttraumatic stress disorder: a quantitative review of 25 years of research. Psychol Bull 132(6):959

    PubMed  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. doi:10.3389/neuro.09.068.2009

    Article  PubMed  Google Scholar 

  • Tottenham N, Hare TA, Quinn BT, McCarry TW, Nurse M, Gilhooly T, Millner A, Galvan A, Davidson MC, Eigsti I-M, Thomas KM, Freed PJ, Booma ES, Gunnar MR, Altemus M, Aronson J, Casey BJ (2010) Prolonged institutional rearing is associated with atypically large amygdala volume and difficulties in emotion regulation. Dev Sci 13(1):46–61

    PubMed  PubMed Central  Google Scholar 

  • 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. doi:10.1111/j.1467-7687.2010.00971.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Rooij SJH, Cross D, Stevens JS, Vance LA, Kim YJ, Bradley B, Tottenham N, Jovanovic T (2016) Maternal buffering of fear-potentiated startle in children and adolescents with trauma exposure. Soc Neurosci. doi:10.1080/17470919.2016.1164244

    Article  PubMed  PubMed Central  Google Scholar 

  • Velez CN, Johnson JIM, Cohen P (1989) A longitudinal analysis of selected risk factors for childhood psychopathology. J Am Acad Child Adolesc Psychiatry 28(6):861–864. doi:10.1097/00004583-198911000-00009

    Article  CAS  PubMed  Google Scholar 

  • Waters AM, Craske MG, Bergman RL, Naliboff BD, Negoro H, Ornitz EM (2008) Developmental changes in startle reactivity in school-age children at risk for and with actual anxiety disorder. Int J Psychophysiol 70(3):158–164

    PubMed  Google Scholar 

  • Winslow JT, Noble PL, Lyons CK, Sterk SM, Insel TR (2003) Rearing effects on cerebrospinal fluid oxytocin concentration and social buffering in rhesus monkeys. Neuropsychopharmacology 28(5):910–918

    CAS  PubMed  Google Scholar 

  • Wolf RC, Herringa RJ (2016) Prefrontal-amygdala dysregulation to threat in pediatric posttraumatic stress disorder. Neuropsychopharmacology 41(3):822–831

    PubMed  Google Scholar 

  • Yang J, Li W, Liu X, Li Z, Li H, Yang G, Xu L, Li L (2006) Enriched environment treatment counteracts enhanced addictive and depressive-like behavior induced by prenatal chronic stress. Brain Res 1125(1):132–137. doi:10.1016/j.brainres.2006.10.028

    Article  CAS  PubMed  Google Scholar 

  • Yang J, Hou C, Ma N, Liu J, Zhang Y, Zhou J, Xu L, Li L (2007) Enriched environment treatment restores impaired hippocampal synaptic plasticity and cognitive deficits induced by prenatal chronic stress. Neurobiol Learn Mem 87(2):257–263. doi:10.1016/j.nlm.2006.09.001

    Article  PubMed  Google Scholar 

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Stevens, J.S., van Rooij, S.J.H., Jovanovic, T. (2016). Developmental Contributors to Trauma Response: The Importance of Sensitive Periods, Early Environment, and Sex Differences. 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_38

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