Advertisement

Behavioral Problems After Early Life Stress: Contributions of the Hippocampus and Amygdala

      Abstract

      Background

      Early life stress (ELS) can compromise development, with higher amounts of adversity linked to behavioral problems. To understand this linkage, a growing body of research has examined two brain regions involved with socioemotional functioning—amygdala and hippocampus. Yet empirical studies have reported increases, decreases, and no differences within human and nonhuman animal samples exposed to different forms of ELS. This divergence in findings may stem from methodological factors, nonlinear effects of ELS, or both.

      Methods

      We completed rigorous hand-tracing of the amygdala and hippocampus in three samples of children who experienced different forms of ELS (i.e., physical abuse, early neglect, or low socioeconomic status). Interviews were also conducted with children and their parents or guardians to collect data about cumulative life stress. The same data were also collected in a fourth sample of comparison children who had not experienced any of these forms of ELS.

      Results

      Smaller amygdala volumes were found for children exposed to these different forms of ELS. Smaller hippocampal volumes were also noted for children who were physically abused or from low socioeconomic status households. Smaller amygdala and hippocampal volumes were also associated with greater cumulative stress exposure and behavioral problems. Hippocampal volumes partially mediated the relationship between ELS and greater behavioral problems.

      Conclusions

      This study suggests ELS may shape the development of brain areas involved with emotion processing and regulation in similar ways. Differences in the amygdala and hippocampus may be a shared diathesis for later negative outcomes related to ELS.

      Keywords

      To read this article in full you will need to make a payment

      Subscribe:

      Subscribe to Biological Psychiatry
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

      1. Shonkoff J.P. Phillips D.A. From Neurons to Neighborhoods. The Science of Early Childhood Development. National Academies Press, Washington, DC2000
        • Belfer M.L.
        Child and adolescent mental disorders: The magnitude of the problem across the globe.
        J Child Psychol Psychiatry. 2008; 49: 226-236
        • Reef J.
        • Diamantopoulou S.
        • van Meurs I.
        • Verhulst F.C.
        • van der Ende J.
        Developmental trajectories of child to adolescent externalizing behavior and adult DSM-IV disorder: Results of a 24-year longitudinal study.
        Soc Psychiatry Psychiatr Epidemiol. 2011; 46: 1233-1241
        • Scott S.
        • Knapp M.
        • Henderson J.
        • Maughan B.
        Financial cost of social exclusion: Follow up study of antisocial children into adulthood.
        BMJ. 2001; 323: 191
        • Ameis S.H.
        • Ducharme S.
        • Albaugh M.D.
        • Hudziak J.J.
        • Botteron K.N.
        • Lepage C.
        • et al.
        Cortical thickness, cortico-amygdalar networks, and externalizing behaviors in healthy children.
        Biol Psychiatry. 2014; 75: 65-72
        • Beauchaine T.P.
        • Gatzke-Kopp L.M.
        Instantiating the multiple levels of analysis perspective in a program of study on externalizing behavior.
        Dev Psychopathol. 2012; 24: 1003-1018
        • Levy F.
        Internalizing versus externalizing comorbidity: Neural circuit hypothesis.
        Aust N Z J Psychiatry. 2010; 44: 399-409
        • Patrick C.J.
        • Durbin C.E.
        • Moser J.S.
        Reconceptualizing antisocial deviance in neurobehavioral terms.
        Dev Psychopathol. 2012; 24: 1047-1071
        • Fergusson D.M.
        • Horwood L.J.
        Resilience to childhood adversity. Results of a 21-year study.
        in: Luthar Luthar Resilience and Vulnerability: Adaptation in the Context of Childhood Adversities. Cambridge University Press, New York2003: 130-155
        • Hicks B.M.
        • South S.C.
        • DiRago A.C.
        • Iacono W.G.
        • McGue M.
        Environmental adversity and increasing genetic risk for externalizing disorders.
        Arch Gen Psychiatry. 2009; 66: 640-648
        • Jaffee S.R.
        • Caspi A.
        • Moffitt T.E.
        • Taylor A.
        Physical maltreatment victim to antisocial child: Evidence of an environmentally mediated process.
        J Abnorm Psychol. 2004; 113: 44-55
        • Jaffee S.R.
        • Caspi A.
        • Moffitt T.E.
        • Polo-Tomás M.
        • Taylor A.
        Individual, family, and neighborhood factors distinguish resilient from non-resilient maltreated children: A cumulative stressors model.
        Child Abuse Neglect. 2007; 31: 231-253
        • Lansford J.E.
        • Dodge K.A.
        • Pettit G.S.
        • Bates J.E.
        • Crozier J.
        • Kaplow J.
        A 12-year prospective study of the long-term effects of early child physical maltreatment on psychological, behavioral, and academic problems in adolescence.
        Arch Pediatr Adolesc Med. 2002; 156: 824-830
        • Lansford J.E.
        • Miller-Johnson S.
        • Berlin L.J.
        • Dodge K.A.
        • Bates J.E.
        • Pettit G.S.
        Early physical abuse and later violent delinquency. A prospective longitudinal study.
        Child Maltreatment. 2007; 12: 233-245
        • Hawk B.
        • McCall R.B.
        CBCL behavior problems of post-institutionalized international adoptees.
        Clin Child Fam Psychol Rev. 2010; 13: 199-211
        • Merz E.C.
        • McCall R.B.
        Behavior problems in children adopted from psychosocially depriving institutions.
        J Abnorm Child Psychol. 2010; 38: 459-470
        • Wiik K.L.
        • Loman M.M.
        • Van Ryzin M.J.
        • Armstrong J.M.
        • Essex M.J.
        • Pollak S.D.
        • Gunnar M.R.
        Behavioral and emotional symptoms of post-institutionalized children in middle childhood.
        J Child Psychol Psychiatry. 2010; 52: 56-63
        • Bradley R.H.
        • Corwyn R.F.
        Socioeconomic status and child development.
        Annu Rev Psychol. 2002; 53: 371-399
        • Brooks-Gunn J.
        • Duncan G.J.
        The effects of poverty on children.
        The Future of Children. 1997; 7: 55-71
        • McLoyd V.C.
        Socioeconomic disadvantage and child development.
        Am Psychol. 1998; 53: 185-204
        • Barnow S.
        • Schuckit M.A.
        • Lucht M.
        • John U.
        • Freyberger H.J.
        The importance of a positive family history of alcoholism, parental rejection and emotional warmth, behavioral problems and peer substance use for alcohol problems in teenagers: A path analysis.
        J Stud Alcohol Drugs. 2002; 63: 305-315
        • Briggs-Gowan M.J.
        • Carter A.S.
        • Clark R.
        • Augustyn M.
        • McCarthy K.J.
        • Ford J.D.
        Exposure to potentially traumatic events in early childhood: Differential links to emergent psychopathology.
        J Child Psychol Psychiatry. 2010; 51: 1132-1140
        • Essex M.J.
        • Shirtcliff E.A.
        • Burk L.R.
        • Ruttle P.L.
        • Klein M.H.
        • Slattery M.J.
        • et al.
        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. 2011; 23: 1039-1058
        • Lovallo W.R.
        • Farag N.H.
        • Sorocco K.H.
        • Cohoon A.J.
        • Vincent A.S.
        Lifetime adversity leads to blunted stress axis reactivity: Studies from the Oklahoma Family Health Patterns Project.
        Biol Psychiatry. 2012; 71: 344-349
        • Maughan B.
        • McCarthy G.
        Childhood adversities and psychosocial disorders.
        Br Med Bull. 1997; 53: 156-169
        • Pechtel P.
        • Pizzagalli D.A.
        Effects of early life stress on cognitive and affective function: An integrated review of human literature.
        Psychopharmacology. 2011; 214: 55-70
        • Arnsten A.F.
        Stress signalling pathways that impair prefrontal cortex structure and function.
        Nat Rev Neurosci. 2009; 10: 410-422
        • Lupien S.J.
        • McEwen B.S.
        • Gunnar M.R.
        • Heim C.
        Effects of stress throughout the lifespan on the brain, behaviour and cognition.
        Nat Rev Neurosci. 2009; 10: 434-445
        • Karl A.
        • Schaefer M.
        • Malta L.S.
        • Dörfel D.
        • Rohleder N.
        • Werner A.
        A meta-analysis of structural brain abnormalities in PTSD.
        Neurosci Biobehav Rev. 2006; 30: 1004-1031
        • Woon F.L.
        • Hedges D.W.
        Hippocampal and amygdala volumes in children and adults with childhood maltreatment-related posttraumatic stress disorder. A meta-analysis.
        Hippocampus. 2008; 18: 729-736
        • Drake B.
        • Pandey S.
        Understanding the relationship between neighborhood poverty and specific types of child maltreatment.
        Child Abuse Neglect. 1996; 20: 1003-1018
        • Hellerstedt W.L.
        • Madsen N.J.
        • Gunnar M.R.
        • Grotevant H.D.
        • Lee R.M.
        • Johnson D.E.
        The international adoption project: Population-based surveillance of Minnesota parents who adopted children internationally.
        Matern Child Health J. 2008; 12: 162-171
        • Rutter M.
        Developmental catch-up, and deficit, following adoption after severe global early privation.
        J Child Psychol Psychiatry. 1998; 39: 465-476
        • Bousha D.M.
        • Twentyman C.T.
        Mother-child interactional style in abuse, neglect, and control groups. Naturalistic observations in the home.
        J Abnorm Psychol. 1984; 93: 106-114
        • Jacobson L.
        • Sapolsky R.
        The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis.
        Endocr Rev. 1991; 12: 118-134
        • Jarrard L.E.
        On the role of the hippocampus in learning and memory in the rat.
        Behav Neural Biol. 1993; 60: 9-26
        • Adolphs R.
        • Tranel D.
        • Damasio H.
        • Damasio A.R.
        Fear and the human amygdala.
        J Neurosci. 1995; 15: 5879-5891
        • Aggleton J.P.
        • Young A.W.
        The enigma of the amygdala. On its contribution to human emotion.
        in: Lane R.D. Nadel L. Series in Affective Science. Oxford University Press, New York2000: 106-128
        • Tottenham N.
        • Sheridan M.A.
        A review of adversity, the amygdala and the hippocampus: A consideration of developmental timing.
        Front Hum Neurosci. 2009; 3: 68
        • Conrad C.D.
        • Magariños A.M.
        • LeDoux J.E.
        • McEwen B.S.
        Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy.
        Behav Neurosci. 1999; 113: 902-913
        • Lambert K.G.
        • Buckelew S.K.
        • Staffiso-Sandoz G.
        • Gaffga S.
        • Carpenter W.
        • Fisher J.
        • Kinsley C.H.
        Activity-stress induces atrophy of apical dendrites of hippocampal pyramidal neurons in male rats.
        Physiol Behav. 1998; 65: 43-49
        • Magarinos A.M.
        • McEwen B.S.
        Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: Involvement of glucocorticoid secretion and excitatory amino acid receptors.
        Neuroscience. 1995; 69: 89-98
        • Andersen S.L.
        • Tomada A.
        • Vincow E.S.
        • Valente E.
        • Polcari A.
        • Teicher M.H.
        Preliminary evidence for sensitive periods in the effect of childhood sexual abuse on regional brain development.
        J Neuropsychiatry Clin Neurosci. 2008; 20: 292-301
        • Teicher M.H.
        • Anderson C.M.
        • Polcari A.
        Childhood maltreatment is associated with reduced volume in the hippocampal subfields CA3, dentate gyrus, and subiculum.
        Proc Natl Acad Sci U S A. 2012; 109: E563-E572
        • Hanson J.L.
        • Chandra A.
        • Wolfe B.L.
        • Pollak S.D.
        Association between income and the hippocampus.
        PLoS One. 2011; 6: e18712
        • Noble K.G.
        • Houston S.M.
        • Kan E.
        • Sowell E.R.
        Neural correlates of socioeconomic status in the developing human brain.
        Dev Sci. 2012; 15: 516-527
        • Luby J.
        • Belden A.
        • Botteron K.
        • Marrus N.
        • Harms M.P.
        • Babb C.
        • et al.
        The effects of poverty on childhood brain development. The mediating effect of caregiving and stressful life events.
        JAMA Pediatr. 2013; 167: 1135-1142
        • Rao U.
        • Chen L.-A.
        • Bidesi A.S.
        • Shad M.U.
        • Thomas M.A.
        • Hammen C.L.
        Hippocampal changes associated with early-life adversity and vulnerability to depression.
        Biol Psychiatry. 2010; 67: 357-364
        • Spinelli S.
        • Chefer S.
        • Suomi S.J.
        • Higley J.D.
        • Barr C.S.
        • Stein E.
        Early-life stress induces long-term morphologic changes in primate brain.
        Arch Gen Psychiatry. 2009; 66: 658-665
        • Mehta M.A.
        • Golembo N.I.
        • Nosarti C.
        • Colvert E.
        • Mota A.
        • Williams S.C.R.
        • et al.
        Amygdala, hippocampal and corpus callosum size following severe early institutional deprivation. The English and Romanian Adoptees Study Pilot.
        J Child Psychol Psychiatry. 2009; 50: 943-951
        • Tottenham N.
        • Hare T.A.
        • Quinn B.T.
        • McCarry T.W.
        • Nurse M.
        • Gilhooly T.
        • et al.
        Prolonged institutional rearing is associated with atypically large amygdala volume and difficulties in emotion regulation.
        Dev Sci. 2010; 13: 46-61
        • Sheridan M.A.
        • Fox N.A.
        • Zeanah C.H.
        • McLaughlin K.A.
        • Nelson C.A.
        Variation in neural development as a result of exposure to institutionalization early in childhood.
        Proc Natl Acad Sci U S A. 2012; 109: 12927-12932
        • McLaughlin K.A.
        • Sheridan M.A.
        • Winter W.
        • Fox N.A.
        • Zeanah C.H.
        • Nelson C.A.
        Widespread reductions in cortical thickness following severe early-life deprivation. A neurodevelopmental pathway to attention-deficit/hyperactivity disorder [published online ahead of print Oct 3].
        Biol Psychiatry. 2013; (doi:10.1016/j.biopsych.2013.08.016)
        • Carrion V.G.
        • Weems C.F.
        • Eliez S.
        • Patwardhan A.
        • Brown W.
        • Ray R.D.
        • Reiss A.L.
        Attenuation of frontal asymmetry in pediatric posttraumatic stress disorder.
        Biol Psychiatry. 2001; 50: 943-951
        • De Bellis M.D.
        • Keshavan M.S.
        • Clark D.B.
        • Casey B.J.
        • Giedd J.N.
        • Boring A.M.
        • et al.
        A.E. Bennett Research Award. Developmental traumatology. Part II. Brain development.
        Biol Psychiatry. 1999; 45: 1271-1284
        • De Bellis M.D.
        • Keshavan M.S.
        • Shifflett H.
        • Iyengar S.
        • Beers S.R.
        • Hall J.
        • Moritz G.
        Brain structures in pediatric maltreatment-related posttraumatic stress disorder: A sociodemographically matched study.
        Biol Psychiatry. 2002; 52: 1066-1078
        • De Bellis M.D.
        • Hall J.
        • Boring A.M.
        • Frustaci K.
        • Moritz G.
        A pilot longitudinal study of hippocampal volumes in pediatric maltreatment-related posttraumatic stress disorder.
        Biol Psychiatry. 2001; 50: 305-309
        • Mitra R.
        • Jadhav S.
        • McEwen B.S.
        • Vyas A.
        • Chattarji S.
        Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala.
        Proc Natl Acad Sci U S A. 2005; 102: 9371-9376
        • Padival M.A.
        • Blume S.R.
        • Rosenkranz J.A.
        Repeated restraint stress exerts different impact on structure of neurons in the lateral and basal nuclei of the amygdala.
        Neuroscience. 2013; 246: 230-242
        • Vyas A.
        • Mitra R.
        • Shankaranarayana Rao B.S.
        • Chattarji S.
        Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons.
        J Neurosci. 2002; 22: 6810-6818
        • Vyas A.
        • Jadhav S.
        • Chattarji S.
        Prolonged behavioral stress enhances synaptic connectivity in the basolateral amygdala.
        Neuroscience. 2006; 143: 387-393
        • Edmiston E.E.
        • Wang F.
        • Mazure C.M.
        • Guiney J.
        • Sinha R.
        • Mayes L.C.
        • Blumberg H.P.
        Corticostriatal-limbic gray matter morphology in adolescents with self-reported exposure to childhood maltreatment.
        Arch Pediatr Adolesc Med. 2011; 165: 1069-1077
        • Østby Y.
        • Tamnes C.K.
        • Fjell A.M.
        • Westlye L.T.
        • Due-Tønnessen P.
        • Walhovd K.B.
        Heterogeneity in subcortical brain development: A structural magnetic resonance imaging study of brain maturation from 8 to 30 years.
        J Neurosci. 2009; 29: 11772-11782
        • Goddings A.L.
        • Mills K.L.
        • Clasen L.S.
        • Giedd J.N.
        • Viner R.M.
        • Blakemore S.J.
        The influence of puberty on subcortical brain development.
        Neuroimage. 2014; 88: 242-251
        • Brierley B.
        • Shaw P.
        • David A.S.
        The human amygdala: A systematic review and meta-analysis of volumetric magnetic resonance imaging.
        Brain Res Brain Res Rev. 2002; 39: 84-105
        • Teipel S.J.
        • Ewers M.
        • Wolf S.
        • Jessen F.
        • Kölsch H.
        • Arlt S.
        • et al.
        Multicentre variability of MRI-based medial temporal lobe volumetry in Alzheimer’s disease.
        Psychiatry Res Neuroimaging. 2010; 182: 244-250
        • Hanson J.L.
        • Suh J.W.
        • Nacewicz B.M.
        • Sutterer M.J.
        • Cayo A.A.
        • Stodola D.E.
        • et al.
        Robust automated amygdala segmentation via multi-atlas diffeomorphic registration.
        Front Neurosci. 2012; 6: 166
        • Morey R.A.
        • Petty C.M.
        • Xu Y.
        • Hayes J.P.
        • Ii H.R.W.
        • Lewis D.V.
        • et al.
        A comparison of automated segmentation and manual tracing for quantifying hippocampal and amygdala volumes.
        Neuroimage. 2009; 45: 855-866
        • Dewey J.
        • Hana G.
        • Russell T.
        • Price J.
        • McCaffrey D.
        • Harezlak J.
        • et al.
        Reliability and validity of MRI-based automated volumetry software relative to auto-assisted manual measurement of subcortical structures in HIV-infected patients from a multisite study.
        Neuroimage. 2010; 51: 1334-1344
        • McEwen B.S.
        Glucocorticoids, depression, and mood disorders: Structural remodeling in the brain.
        Metabolism. 2005; 54: 20-23
        • Nacewicz B.M.
        • Dalton K.M.
        • Johnstone T.
        • Long M.T.
        • McAuliff E.M.
        • Oakes T.R.
        • et al.
        Amygdala volume and nonverbal social impairment in adolescent and adult males with autism.
        Arch Gen Psychiatry. 2006; 63: 1417-1428
        • Schumann C.M.
        • Amaral D.G.
        Stereological estimation of the number of neurons in the human amygdaloid complex.
        J Comp Neurol. 2005; 491: 320-329
        • Schmidt M.V.
        • Wang X.D.
        • Meijer O.C.
        Early life stress paradigms in rodents: Potential animal models of depression?.
        Psychopharmacology. 2011; 214: 131-140
        • Rosenkranz J.A.
        • Venheim E.R.
        • Padival M.
        Chronic stress causes amygdala hyperexcitability in rodents.
        Biol Psychiatry. 2010; 67: 1128-1136
        • Padival M.
        • Quinette D.
        • Rosenkranz J.A.
        Effects of repeated stress on excitatory drive of basal amygdala neurons in vivo.
        Neuropsychopharmacology. 2013; 38: 1748-1762
        • McEwen B.S.
        Mood disorders and allostatic load.
        Biol Psychiatry. 2003; 54: 200-207
        • Frodl T.
        • Meisenzahl E.M.
        • Zetzsche T.
        • Born C.
        • Jäger M.
        • Groll C.
        • et al.
        Larger amygdala volumes in first depressive episode as compared to recurrent major depression and healthy control subjects.
        Biol Psychiatry. 2003; 53: 338-344
        • Siegle G.J.
        • Konecky R.O.
        • Thase M.E.
        • Carter C.S.
        Relationships between amygdala volume and activity during emotional information processing tasks in depressed and never-depressed individuals.
        Ann N Y Acad Sci. 2003; 985: 481-484
        • Sheline Y.I.
        • Gado M.H.
        • Price J.L.
        Amygdala core nuclei volumes are decreased in recurrent major depression.
        Neuroreport. 1998; 9: 2023-2028
        • Mosconi M.W.
        • Cody-Hazlett H.
        • Poe M.D.
        • Gerig G.
        • Gimpel-Smith R.
        • Piven J.
        Longitudinal study of amygdala volume and joint attention in 2- to 4-year-old children with autism.
        Arch Gen Psychiatry. 2009; 66: 509-516
        • Kim J.E.
        • Lyoo I.K.
        • Estes A.M.
        • Renshaw P.F.
        • Shaw D.W.
        • Friedman S.D.
        • et al.
        Laterobasal amygdalar enlargement in 6- to 7-year-old children with autism spectrum disorder.
        Arch Gen Psychiatry. 2010; 67: 1187-1197
        • Ding J.
        • Han F.
        • Shi Y.
        Single-prolonged stress induces apoptosis in the amygdala in a rat model of post-traumatic stress disorder.
        J Psychiatr Res. 2010; 44: 48-55
        • Maheu F.S.
        • Dozier M.
        • Guyer A.E.
        • Mandell D.
        • Peloso E.
        • Poeth K.
        • et al.
        A preliminary study of medial temporal lobe function in youths with a history of caregiver deprivation and emotional neglect.
        Cogn Affect Behav Neurosci. 2010; 10: 34-49
        • McCrory E.J.
        • De Brito S.A.
        • Sebastian C.L.
        • Mechelli A.
        • Bird G.
        • Kelly P.A.
        • Viding E.
        Heightened neural reactivity to threat in child victims of family violence.
        Curr Biol. 2011; 21: R947-R948
        • Tottenham N.
        • Hare T.A.
        • Millner A.
        • Gilhooly T.
        • Zevin J.D.
        • Casey B.J.
        Elevated amygdala response to faces following early deprivation.
        Dev Sci. 2011; 14: 190-204
        • Vyas A.
        • Pillai A.G.
        • Chattarji S.
        Recovery after chronic stress fails to reverse amygdaloid neuronal hypertrophy and enhanced anxiety-like behavior.
        Neuroscience. 2004; 128: 667-673
        • Kuo J.R.
        • Kaloupek D.G.
        • Woodward S.H.
        Amygdala volume in combat-exposed veterans with and without posttraumatic stress disorder. A cross-sectional study.
        Arch Gen Psychiatry. 2012; 69: 1080-1086
        • Straus M.A.
        • Hamby S.L.
        • Finkelhor D.
        • Moore D.W.
        • Runyan D.
        Identification of child maltreatment with the Parent-Child Conflict Tactics Scales: Development and psychometric data for a national sample of American parents.
        Child Abuse Neglect. 1998; 22: 249-270
        • Hollingshead A.B.
        Two Factor Index of Social Position.
        Yale University, New Haven, CT1957
        • Marshall W.A.
        • Tanner J.M.
        Variations in pattern of pubertal changes in girls.
        Arch Dis Child. 1969; 44: 291-303
        • Marshall W.A.
        • Tanner J.M.
        Variations in the pattern of pubertal changes in boys.
        Arch Dis Child. 1970; 45: 13-23
        • Rusch B.D.
        • Abercrombie H.C.
        • Oakes T.R.
        • Schaefer S.M.
        • Davidson R.J.
        Hippocampal morphometry in depressed patients and control subjects: Relations to anxiety symptoms.
        Biol Psychiatry. 2001; 50: 960-964
        • Duvernoy H.M.
        The human brain stem and cerebellum. surface, structure, vascularization, and three-dimensional sectional anatomy with MRI.
        Springer-Verlag. 1995;
        • Mai J.K.
        • Assheuer J.
        • Paxinos G.
        Atlas of the Human Brain.
        Academic Press, San Diego1997
        • Rudolph K.D.
        • Flynn M.
        Childhood adversity and youth depression. Influence of gender and pubertal status.
        Dev Psychopathol. 2007; 19: 1-34
        • Rudolph K.D.
        • Hammen C.
        Age and gender as determinants of stress exposure, generation, and reactions in youngsters. a transactional perspective.
        Child Dev. 1999; 70: 660-677
        • Rudolph K.D.
        • Hammen C.
        • Burge D.
        • Lindberg N.
        • Herzberg D.
        • Daley S.E.
        Toward an interpersonal life-stress model of depression: The developmental context of stress generation.
        Dev Psychopathol. 2000; 12: 215-234
        • Wethington E.
        • Brown G.
        • Kessler R.
        Interview measurement of stressful life events.
        in: Cohen S. Underwood G. Kessler R. Measuring Stress. Oxford University Press, New York1995
        • Roberts J.A.
        • Scott K.A.
        Interpreting assessment data of internationally adopted children.
        Top Lang Disord. 2009; 29: 82-99
        • Rutter M.M.
        • Dunn J.J.
        • Plomin R.R.
        • Simonoff E.E.
        • Pickles A.A.
        • Maughan B.B.
        • et al.
        Integrating nature and nurture: Implications of person-environment correlations and interactions for developmental psychopathology.
        Dev Psychopathol. 1997; 9: 335-364
        • Sobel M.E.
        Some new results on indirect effects and their standard errors in covariance structure models.
        in: Tuma N. Sociological Methodology. American Sociological Association, Washington, DC1986: 159-186
        • Nacewicz B.M.
        • Angelos L.
        • Dalton K.M.
        • Fischer R.
        • Anderle M.J.
        • Alexander A.L.
        • Davidson R.J.
        Reliable non-invasive measurement of human neurochemistry using proton spectroscopy with an anatomically defined amygdala-specific voxel.
        Neuroimage. 2012; 59: 2548-2559
        • Drevets W.C.
        Functional neuroimaging studies of depression: The anatomy of melancholia.
        Annu Rev Med. 1998; 49: 341-361
        • MacMillan H.L.
        • Fleming J.E.
        • Streiner D.L.
        • Lin E.
        • Boyle M.H.
        • Jamieson E.
        • et al.
        Childhood abuse and lifetime psychopathology in a community sample.
        Am J Psychiatry. 2001; 158: 1878-1883