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Neurobiological Markers of Resilience to Depression Following Childhood Maltreatment: The Role of Neural Circuits Supporting the Cognitive Control of Emotion

      Abstract

      Background

      Childhood adversity is strongly linked to negative mental health outcomes, including depression and anxiety. Leveraging cognitive neuroscience to identify mechanisms that contribute to resilience in children with a history of maltreatment may provide viable intervention targets for the treatment or prevention of psychopathology. We present a conceptual model of a potential neurobiological mechanism of resilience to depression and anxiety following childhood adversity. Specifically, we argue that neural circuits underlying the cognitive control of emotion may promote resilience, wherein a child’s ability to recruit the frontoparietal control network to modulate amygdala reactivity to negative emotional cues—such as during cognitive reappraisal—buffers risk for internalizing symptoms following exposure to adversity.

      Methods

      We provide preliminary support for this model of resilience in a longitudinal sample of 151 participants 8 to 17 years of age with (n = 79) and without (n = 72) a history of childhood maltreatment who completed a cognitive reappraisal task while undergoing functional magnetic resonance imaging.

      Results

      Among maltreated youths, those who were better able to recruit prefrontal control regions and modulate amygdala reactivity during reappraisal exhibited lower risk for depression over time. By contrast, no association was observed between neural functioning during reappraisal and depression among youths without a history of maltreatment.

      Conclusions

      These preliminary findings support the hypothesis that children who are better able to regulate emotion through recruitment of the frontoparietal network exhibit greater resilience to depression following childhood maltreatment. Interventions targeting cognitive reappraisal and other cognitive emotion regulation strategies may have potential for reducing vulnerability to depression among children exposed to adversity.

      Keywords

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      References

        • Green J.G.
        • McLaughlin K.A.
        • Berglund P.A.
        • Gruber M.J.
        • Sampson N.A.
        • Zaslavsky A.M.
        • Kessler R.C.
        Childhood adversities and adult psychiatric disorders in the National Comorbidity Survey Replication I: Associations with first onset of DSM-IV disorders.
        Arch Gen Psychiatry. 2010; 67: 113-123
        • Kessler R.C.
        • McLaughlin K.A.
        • Green J.G.
        • Gruber M.J.
        • Sampson N.A.
        • Zaslavsky A.M.
        • et al.
        Childhood adversities and adult psychopathology in the WHO World Mental Health Surveys.
        Br J Psychiatry. 2010; 197: 378-385
        • McLaughlin K.A.
        • Green J.G.
        • Gruber M.J.
        • Sampson N.A.
        • Zaslavsky A.M.
        • Kessler R.C.
        Childhood adversities and first onset of psychiatric disorders in a national sample of US adolescents.
        Arch Gen Psychiatry. 2012; 69: 1151-1160
        • McLaughlin K.A.
        Future directions in childhood adversity and youth psychopathology.
        J Clin Child Adolesc Psychol. 2016; 45: 361-382
        • Sheridan M.A.
        • McLaughlin K.A.
        Dimensions of early experience and neural development: deprivation and threat.
        Trends Cogn Sci. 2014; 18: 580-585
        • McLaughlin K.A.
        • Sheridan M.A.
        Beyond cumulative risk: A dimensional approach to childhood adversity.
        Curr Dir Psychol Sci. 2016; 25: 239-245
        • McLaughlin K.A.
        • Sheridan M.A.
        • Lambert H.K.
        Childhood adversity and neural development: Deprivation and threat as distinct dimensions of early experience.
        Neurosci Biobehav Rev. 2014; 47: 578-591
        • Cicchetti D.
        • Toth S.L.
        A developmental psychopathology perspective on child abuse and neglect.
        J Am Acad Child Adolesc Psychiatry. 1995; 34: 541-565
        • Cohen P.
        • Brown J.
        • Smailes E.
        Child abuse and neglect and the development of mental disorders in the general population.
        Dev Psychopathol. 2001; 13: 981-999
        • 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
        • Barnes A.J.
        • Lafavor T.L.
        • Cutuli J.J.
        • Zhang L.
        • Oberg C.N.
        • Masten A.S.
        Health and self-regulation among school-age children experiencing family homelessness.
        Children. 2017; 4: 70
        • Beardslee W.R.
        • Podorefsky D.
        Resilient adolescents whose parents have serious affective and other psychiatric disorders: Importance of self-understanding and relationships.
        Am J Psychiatry. 1988; 145: 63-69
        • Cicchetti D.
        • Rogosch F.A.
        • Lynch M.
        • Holt K.D.
        Resilience in maltreated children: Processes leading to adaptive outcome.
        Dev Psychopathol. 1993; 5: 629-647
        • Garmezy N.
        Children in poverty: Resilience despite risk.
        Psychiatry. 1993; 56: 127-136
        • Masten A.S.
        • Best K.M.
        • Garmezy N.
        Resilience and development: Contributions from the study of children who overcome adversity.
        Dev Psychopathol. 1990; 2: 425-444
        • Luthar S.S.
        • Cicchetti D.
        • Becker B.
        The construct of resilience: A critical evaluation and guidelines for future work.
        Child Dev. 2000; 71: 543-562
        • Connor K.M.
        • Davidson J.R.T.
        Development of a new resilience scale: The Connor-Davidson Resilience Scale (CD-RISC).
        Depress Anxiety. 2003; 18: 76-82
        • Wagnild G.
        A review of the resilience scale.
        J Nurs Meas. 2009; 17: 105-113
        • Wagnild G.
        • Young H.M.
        Resilience among older women.
        Image J Nurs Sch. 1990; 22: 252-255
        • Southwick S.M.
        • Charney D.S.
        The science of resilience: Implications for the prevention and treatment of depression.
        Science. 2012; 338: 79-82
        • Rutter M.
        Resilience in the face of adversity: Protective factors and resistance to psychiatric disorder.
        Br J Psychiatry. 1985; 147: 598-611
        • Bronfenbrenner U.
        • Ceci S.J.
        Nature-nuture reconceptualized in developmental perspective: A bioecological model.
        Psychol Rev. 1994; 101: 568-586
        • Ungar M.
        The social ecology of resilience: Addressing contextual and cultural ambiguity of a nascent construct.
        Am J Orthopsychiatry. 2011; 81: 1-17
        • Ungar M.
        • Ghazinour M.
        • Richter J.
        Annual research review: What is resilience within the social ecology of human development?.
        J Child Psychol Psychiatry. 2013; 54: 348-366
        • Ungar M.
        Resilience across cultures.
        Br J Soc Work. 2008; 38: 218-235
        • Odgers C.L.
        • Moffitt T.E.
        • Tach L.M.
        • Sampson R.J.
        • Taylor A.
        • Matthews C.L.
        • Caspi A.
        The protective effects of neighborhood collective efficacy on British children growing up in deprivation: A developmental analysis.
        Dev Psychol. 2009; 45: 942-957
        • Benzies K.
        • Mychasiuk R.
        Fostering family resiliency: A review of the key protective factors.
        Child Fam Soc Work. 2009; 14: 103-114
        • Wachs T.D.
        Contributions of temperament to buffering and sensitization processes in children’s development.
        Ann N Y Acad Sci. 2006; 1094: 28-39
        • Kim-Cohen J.
        • Gold A.L.
        Measured gene–environment interactions and mechanisms promoting resilient development.
        Curr Dir Psychol Sci. 2009; 18: 138-142
        • Shechner T.
        • Britton J.C.
        • Pérez-Edgar K.
        • Bar-Haim Y.
        • Ernst M.
        • Fox N.A.
        • et al.
        Attention biases, anxiety, and development: toward or away from threats or rewards?.
        Depress Anxiety. 2012; 29: 282-294
        • Goldin P.R.
        • McRae K.
        • Ramel W.
        • Gross J.J.
        The neural bases of emotion regulation: Reappraisal and suppression of negative emotion.
        Biol Psychiatry. 2008; 63: 577-586
        • Gross J.J.
        The emerging field of emotion regulation: An integrative review.
        Rev Gen Psychol. 1998; 2: 271-299
        • Heller A.S.
        • Johnstone T.
        • Shackman A.J.
        • Light S.N.
        • Peterson M.J.
        • Kolden G.G.
        • et al.
        Reduced capacity to sustain positive emotion in major depression reflects diminished maintenance of fronto-striatal brain activation.
        Proc Natl Acad Sci U S A. 2009; 106: 22445-22450
        • Ochsner K.N.
        • Bunge S.A.
        • Gross J.J.
        • Gabrieli J.D.E.
        Rethinking feelings: An fMRI study of the cognitive regulation of emotion.
        J Cogn Neurosci. 2002; 14: 1215-1229
        • Ochsner K.N.
        • Ray R.D.
        • Cooper J.C.
        • Robertson E.R.
        • Chopra S.
        • Gabrieli J.D.E.
        • Gross J.J.
        For better or for worse: Neural systems supporting the cognitive down- and up-regulation of negative emotion.
        Neuroimage. 2004; 23: 483-499
        • Silvers J.A.
        • Shu J.
        • Hubbard A.D.
        • Weber J.
        • Ochsner K.N.
        Concurrent and lasting effects of emotion regulation on amygdala response in adolescence and young adulthood.
        Dev Sci. 2015; 18: 771-784
        • Gross J.J.
        Antecedent- and response-focused emotion regulation: Divergent consequences for experience, expression, and physiology.
        J Pers Soc Psychol. 1998; 74: 224-237
        • Gross J.J.
        • John O.P.
        Individual differences in two emotion regulation processes: Implications for affect, relationships, and well-being.
        J Pers Soc Psychol. 2003; 85: 348-362
        • McRae K.
        • Hughes B.
        • Chopra S.
        • Gabrieli J.D.E.
        • Gross J.J.
        • Ochsner K.N.
        The neural bases of distraction and reappraisal.
        J Cogn Neurosci. 2009; 22: 248-262
        • Webb T.L.
        • Miles E.
        • Sheeran P.
        Dealing with feeling: A meta-analysis of the effectiveness of strategies derived from the process model of emotion regulation.
        Psychol Bull. 2012; 138: 775-808
        • John O.P.
        • Gross J.J.
        Healthy and unhealthy emotion regulation: Personality Processes, individual differences, and life span development.
        J Pers. 2004; 72: 1301-1334
        • Beck A.T.
        Cognitive Therapy of Depression.
        Guilford Press, New York1979
        • Chorpita B.F.
        • Daleiden E.L.
        Mapping evidence-based treatments for children and adolescents: Application of the distillation and matching model to 615 treatments from 322 randomized trials.
        J Consult Clin Psychol. 2009; 77: 566-579
        • Compton S.N.
        • March J.S.
        • Brent D.
        • Albano A.M.
        • Weersing V.R.
        • Curry J.
        Cognitive-behavioral psychotherapy for anxiety and depressive disorders in children and adolescents: An evidence-based medicine review.
        J Am Acad Child Adolesc Psychiatry. 2004; 43: 930-959
        • Ochsner K.N.
        • Gross J.J.
        The cognitive control of emotion.
        Trends Cogn Sci. 2005; 9: 242-249
        • Davis J.I.
        • Gross J.J.
        • Ochsner K.N.
        Psychological distance and emotional experience: What you see is what you get.
        Emotion. 2011; 11: 438-444
        • Denny B.T.
        • Ochsner K.N.
        Behavioral effects of longitudinal training in cognitive reappraisal.
        Emotion. 2014; 14: 425-433
        • Erk S.
        • Mikschl A.
        • Stier S.
        • Ciaramidaro A.
        • Gapp V.
        • Weber B.
        • Walter H.
        Acute and sustained effects of cognitive emotion regulation in major depression.
        J Neurosci. 2010; 30: 15726-15734
        • McLaughlin K.A.
        • Peverill M.
        • Gold A.L.
        • Alves S.
        • Sheridan M.A.
        Child maltreatment and neural systems underlying emotion regulation.
        J Am Acad Child Adolesc Psychiatry. 2015; 54: 753-762
        • Buhle J.T.
        • Silvers J.A.
        • Wager T.D.
        • Lopez R.
        • Onyemekwu C.
        • Kober H.
        • et al.
        Cognitive reappraisal of emotion: A meta-analysis of human neuroimaging studies.
        Cereb Cortex. 2014; 24: 2981-2990
        • Miller E.K.
        • Cohen J.D.
        An integrative theory of prefrontal cortex function.
        Annu Rev Neurosci. 2001; 24: 167-202
        • Niendam T.A.
        • Laird A.R.
        • Ray K.L.
        • Dean Y.M.
        • Glahn D.C.
        • Carter C.S.
        Meta-analytic evidence for a superordinate cognitive control network subserving diverse executive functions.
        Cogn Affect Behav Neurosci. 2012; 12: 241-268
        • Banks S.J.
        • Eddy K.T.
        • Angstadt M.
        • Nathan P.J.
        • Phan K.L.
        Amygdala–frontal connectivity during emotion regulation.
        Soc Cogn Affect Neurosci. 2007; 2: 303-312
        • Eippert F.
        • Veit R.
        • Weiskopf N.
        • Erb M.
        • Birbaumer N.
        • Anders S.
        Regulation of emotional responses elicited by threat-related stimuli.
        Hum Brain Mapp. 2007; 28: 409-423
        • Lee H.
        • Heller A.S.
        • van Reekum C.M.
        • Nelson B.
        • Davidson R.J.
        Amygdala–prefrontal coupling underlies individual differences in emotion regulation.
        Neuroimage. 2012; 62: 1575-1581
        • Ochsner K.N.
        • Silvers J.A.
        • Buhle J.T.
        Functional imaging studies of emotion regulation: A synthetic review and evolving model of the cognitive control of emotion.
        Ann N Y Acad Sci. 2012; 1251: E1-E24
        • Silvers J.A.
        • Insel C.
        • Powers A.
        • Franz P.
        • Helion C.
        • Martin R.E.
        • et al.
        vlPFC–vmPFC–amygdala interactions underlie age-related differences in cognitive regulation of emotion.
        Cereb Cortex. 2017; 27: 3502-3514
        • McRae K.
        • Gross J.J.
        • Weber J.
        • Robertson E.R.
        • Sokol-Hessner P.
        • Ray R.D.
        • et al.
        The development of emotion regulation: An fMRI study of cognitive reappraisal in children, adolescents and young adults.
        Soc Cogn Affect Neurosci. 2012; 7: 11-22
        • Silvers J.A.
        • McRae K.
        • Gabrieli J.D.E.
        • Gross J.J.
        • Remy K.A.
        • Ochsner K.N.
        Age-related differences in emotional reactivity, regulation, and rejection sensitivity in adolescence.
        Emotion. 2012; 12: 1235-1247
        • Ahmed S.P.
        • Somerville L.H.
        • Sebastian C.L.
        Using temporal distancing to regulate emotion in adolescence: Modulation by reactive aggression.
        Cogn Emot. 2018; 32: 812-826
        • Van Cauwenberge V.
        • Van Leeuwen K.
        • Hoppenbrouwers K.
        • Wiersema J.R.
        Developmental changes in neural correlates of cognitive reappraisal: An ERP study using the late positive potential.
        Neuropsychologia. 2017; 95: 94-100
        • Levesque J.
        • Joanette Y.
        • Mensour B.
        • Beaudoin G.
        • Leroux J.-M.
        • Bourgouin P.
        • Beauregard M.
        Neural basis of emotional self-regulation in childhood.
        Neurosci. 2004; 129: 361-369
        • McRae K.
        • Misra S.
        • Prasad A.K.
        • Pereira S.C.
        • Gross J.J.
        Bottom-up and top-down emotion generation: Implications for emotion regulation.
        Soc Cogn Affect Neurosci. 2012; 7: 253-262
        • Pitskel N.B.
        • Bolling D.Z.
        • Kaiser M.D.
        • Crowley M.J.
        • Pelphrey K.A.
        How grossed out are you? The neural bases of emotion regulation from childhood to adolescence.
        Dev Cogn Neurosci. 2011; 1: 324-337
        • Anderson A.K.
        • Phelps E.A.
        Lesions of the human amygdala impair enhanced perception of emotionally salient events.
        Nature. 2001; 411: 305-309
        • Cunningham W.A.
        • Brosch T.
        Motivational salience: Amygdala tuning from traits, needs, values, and goals.
        Curr Dir Psychol Sci. 2012; 21: 54-59
        • Vuilleumier P.
        • Pourtois G.
        Distributed and interactive brain mechanisms during emotion face perception: Evidence from functional neuroimaging.
        Neuropsychologia. 2007; 45: 174-194
        • Hartley C.A.
        • Phelps E.A.
        Changing fear: The neurocircuitry of emotion regulation.
        Neuropsychopharmacology. 2010; 35: 136-146
        • Johnstone T.
        • Reekum CM van
        • Urry H.L.
        • Kalin N.H.
        • Davidson R.J.
        Failure to regulate: Counterproductive recruitment of top-down prefrontal-subcortical circuitry in major depression.
        J Neurosci. 2007; 27: 8877-8884
        • Phelps E.A.
        • Delgado M.R.
        • Nearing K.I.
        • LeDoux J.E.
        Extinction learning in humans: Role of the amygdala and vmPFC.
        Neuron. 2004; 43: 897-905
        • Quirk G.J.
        • Likhtik E.
        • Pelletier J.G.
        • Paré D.
        Stimulation of medial prefrontal cortex decreases the responsiveness of central amygdala output neurons.
        J Neurosci. 2003; 23: 8800-8807
        • Urry H.L.
        • van Reekum C.M.
        • Johnstone T.
        • Kalin N.H.
        • Thurow M.E.
        • Schaefer H.S.
        • et al.
        Amygdala and ventromedial prefrontal cortex are inversely coupled during regulation of negative affect and predict the diurnal pattern of cortisol secretion among older adults.
        J Neurosci. 2006; 26: 4415-4425
        • Beauregard M.
        • Paquette V.
        • Levesque J.
        Dysfunction in the neural circuitry of emotional self-regulation in major depressive disorder.
        Neuroreport. 2006; 17: 843
        • Carthy T.
        • Horesh N.
        • Apter A.
        • Edge M.D.
        • Gross J.J.
        Emotional reactivity and cognitive regulation in anxious children.
        Behav Res Ther. 2010; 48: 384-393
        • Goldin P.R.
        • Manber T.
        • Hakimi S.
        • Canli T.
        • Gross J.J.
        Neural bases of social anxiety disorder: emotional reactivity and cognitive regulation during social and physical threat.
        Arch Gen Psychiatry. 2009; 66: 170-180
        • Miller A.B.
        • McLaughlin K.A.
        • Busso D.S.
        • Brueck S.
        • Peverill M.
        • Sheridan M.A.
        Neural correlates of emotion regulation and adolescent suicidal ideation.
        Biol Psychiatry Cogn Neurosci Neuroimaging. 2018; 3: 125-132
        • Perlman G.
        • Simmons A.N.
        • Wu J.
        • Hahn K.S.
        • Tapert S.F.
        • Max J.E.
        • et al.
        Amygdala response and functional connectivity during emotion regulation: A study of 14 depressed adolescents.
        J Affect Disord. 2012; 139: 75-84
        • Pico-Perez M.
        • Radua J.
        • Steward T.
        • Menchón J.M.
        • Soriano-Mas C.
        Emotion regulation in mood and anxiety disorders: A meta-analysis of fMRI cognitive reappraisal studies.
        Prog Neuropsychopharmacol Biol Psychiatry. 2017; 79: 96-104
        • Glaser J.P.
        • van Os J.
        • Portegijs P.J.M.
        • Myin-Germeys I.
        Childhood trauma and emotional reactivity to daily life stress in adult frequent attenders of general practitioners.
        J Psychosom Res. 2006; 61: 229-236
        • Heleniak C.
        • Jenness J.L.
        • Vander Stoep A.
        • McCauley E.
        • McLaughlin K.A.
        Childhood maltreatment exposure and disruptions in emotion regulation: A transdiagnostic pathway to adolescent internalizing and externalizing psychopathology.
        Cogn Ther Res. 2016; 40: 394-415
        • Weissman D.G.
        • Bitran D.
        • Miller A.B.
        • Schaefer J.D.
        • Sheridan M.A.
        • McLaughlin K.A.
        Difficulties with emotion regulation as a transdiagnostic mechanism linking child maltreatment with the emergence of psychopathology.
        Dev Psychopathol. 2019; 31: 899-915
        • Wichers M.
        • Schrijvers D.
        • Geschwind N.
        • Jacobs N.
        • Myin-Germeys I.
        • Thiery E.
        • et al.
        Mechanisms of gene–environment interactions in depression: Evidence that genes potentiate multiple sources of adversity.
        Psychol Med. 2009; 39: 1077-1086
        • Heleniak C.
        • McLaughlin K.A.
        • Ormel J.
        • Riese H.
        Cardiovascular reactivity as a mechanism linking child trauma to adolescent psychopathology.
        Biol Psychol. 2016; 120: 108-119
        • McLaughlin K.A.
        • Sheridan M.A.
        • Alves S.
        • Mendes W.B.
        Child maltreatment and autonomic nervous system reactivity: Identifying dysregulated stress reactivity patterns by using the biopsychosocial model of challenge and threat.
        Psychosom Med. 2014; 76: 538-546
        • Herringa R.J.
        • Birn R.M.
        • Ruttle P.L.
        • Burghy C.A.
        • Stodola D.E.
        • Davidson R.J.
        • Essex M.J.
        Childhood maltreatment is associated with altered fear circuitry and increased internalizing symptoms by late adolescence.
        Proc Natl Acad Sci U S A. 2013; 110: 19119-19124
        • Marusak H.A.
        • Martin K.R.
        • Etkin A.
        • Thomason M.E.
        Childhood trauma exposure disrupts the automatic regulation of emotional processing.
        Neuropsychopharmacology. 2015; 40: 1250-1258
        • McCrory E.J.
        • Brito S.A.D.
        • Kelly P.A.
        • Bird G.
        • Sebastian C.L.
        • Mechelli A.
        • et al.
        Amygdala activation in maltreated children during pre-attentive emotional processing.
        Br J Psychiatry. 2013; 202: 269-276
        • McCrory E.J.
        • De Brito S.A.
        • Viding E.
        The impact of childhood maltreatment: A review of neurobiological and genetic factors.
        Front Psychiatry. 2011; 2: 48
        • Tottenham N.
        • Hare T.A.
        • Millner A.
        • Gilhooly T.
        • Zevin J.
        • Casey B.J.
        Elevated amygdala response to faces following early deprivation.
        Dev Sci. 2011; 14: 190-204
        • Hein T.C.
        • Monk C.S.
        Research review: Neural response to threat in children, adolescents, and adults after child maltreatment—a quantitative meta-analysis.
        J Child Psychol Psychiatry. 2017; 58: 222-230
        • McLaughlin K.A.
        • Lambert H.K.
        Child trauma exposure and psychopathology: Mechanisms of risk and resilience.
        Curr Opin Psychol. 2017; 14: 29-34
        • Anthony J.L.
        • Lonigan C.J.
        • Hooe E.S.
        • Phillips B.M.
        An affect-based, hierarchical model of temperament and its relations with internalizing symptomatology.
        J Clin Child Adolesc Psychol. 2002; 31: 480-490
        • Heleniak C.
        • King K.M.
        • Monahan K.C.
        • McLaughlin K.A.
        Disruptions in emotion regulation as a mechanism linking community violence exposure to adolescent internalizing problems.
        J Res Adolesc. 2018; 28: 229-244
        • McLaughlin K.A.
        • Hatzenbuehler M.L.
        • Hilt L.M.
        Emotion dysregulation as a mechanism linking peer victimization to internalizing symptoms in adolescents.
        J Consult Clin Psychol. 2009; 77: 894-904
        • Silk J.S.
        • Steinberg L.
        • Morris A.S.
        Adolescents’ emotion regulation in daily life: Links to depressive symptoms and problem behavior.
        Child Dev. 2003; 74: 1869-1880
        • Kim J.
        • Cicchetti D.
        Longitudinal pathways linking child maltreatment, emotion regulation, peer relations, and psychopathology.
        J Child Psychol Psychiatry. 2010; 51: 706-716
        • Gee D.G.
        • Gabard-Durnam L.J.
        • Flannery J.
        • Goff B.
        • Humphreys K.L.
        • Telzer E.H.
        • et al.
        Early developmental emergence of human amygdala–prefrontal connectivity after maternal deprivation.
        Proc Natl Acad Sci U S A. 2013; 110: 15638-15643
        • Hanson J.L.
        • Chung M.K.
        • Avants B.B.
        • Shirtcliff E.A.
        • Gee J.C.
        • Davidson R.J.
        • Pollak S.D.
        Early stress is associated with alterations in the orbitofrontal cortex: A tensor-based morphometry investigation of brain structure and behavioral risk.
        J Neurosci. 2010; 30: 7466-7472
        • Herringa R.J.
        • Burghy C.A.
        • Stodola D.E.
        • Fox M.E.
        • Davidson R.J.
        • Essex M.J.
        Enhanced prefrontal-amygdala connectivity following childhood adversity as a protective mechanism against internalizing in adolescence.
        Biol Psychiatry Cogn Neurosci Neuroimaging. 2016; 1: 326-334
        • Miller G.E.
        • Chen E.
        • Armstrong C.C.
        • Carroll A.L.
        • Ozturk S.
        • Rydland K.J.
        • et al.
        Functional connectivity in central executive network protects youth against cardiometabolic risks linked with neighborhood violence.
        Proc Natl Acad Sci U S A. 2018; 115: 12063-12068
        • McLaughlin K.A.
        • Conron K.J.
        • Koenen K.C.
        • Gilman S.E.
        Childhood adversity, adult stressful life events, and risk of past-year psychiatric disorder: A test of the stress sensitization hypothesis in a population-based sample of adults.
        Psychol Med. 2010; 40: 1647-1658
        • Hammen C.
        Generation of stress in the course of unipolar depression.
        J Abnorm Psychol. 1991; 100: 555-561
        • Hammen C.
        Stress generation in depression: Reflections on origins, research, and future directions.
        J Clin Psychol. 2006; 62: 1065-1082
        • Kendler K.S.
        • Karkowski L.M.
        • Prescott C.A.
        Causal relationship between stressful life events and the onset of major depression.
        Am J Psychiatry. 1999; 156: 837-841
        • Mazure C.M.
        Life stressors as risk factors in depression.
        Clin Psychol Sci Pract. 1998; 5: 291-313
        • Bandoli G.
        • Campbell-Sills L.
        • Kessler R.C.
        • Heeringa S.G.
        • Nock M.K.
        • Rosellini A.J.
        • et al.
        Childhood adversity, adult stress, and the risk of major depression or generalized anxiety disorder in US soldiers: A test of the stress sensitization hypothesis.
        Psychol Med. 2017; 47: 2379-2392
        • Espejo E.P.
        • Hammen C.L.
        • Connolly N.P.
        • Brennan P.A.
        • Najman J.M.
        • Bor W.
        Stress sensitization and adolescent depressive severity as a function of childhood adversity: A link to anxiety disorders.
        J Abnorm Child Psychol. 2007; 35: 287-299
        • Hammen C.
        • Henry R.
        • Daley S.E.
        Depression and sensitization to stressors among young women as a function of childhood adversity.
        J Consult Clin Psychol. 2000; 68: 782-787
        • Kendler K.S.
        • Kuhn J.W.
        • Prescott C.A.
        Childhood sexual abuse, stressful life events and risk for major depression in women.
        Psychol Med. 2004; 34: 1475-1482
        • Troy A.S.
        • Wilhelm F.H.
        • Shallcross A.J.
        • Mauss I.B.
        Seeing the silver lining: Cognitive reappraisal ability moderates the relationship between stress and depressive symptoms.
        Emotion. 2010; 10: 783-795
        • Lyons D.M.
        • Parker K.J.
        • Schatzberg A.F.
        Animal models of early life stress: Implications for understanding resilience.
        Dev Psychobiol. 2010; 52: 616-624
        • Badura-Brack A.S.
        • Naim R.
        • Ryan T.J.
        • Levy O.
        • Abend R.
        • Khanna M.M.
        • et al.
        Effect of attention training on attention bias variability and PTSD symptoms: Randomized controlled trials in Israeli and U.S. combat veterans.
        Am J Psychiatry. 2015; 172: 1233-1241
        • Lazarov A.
        • Marom S.
        • Yahalom N.
        • Pine D.S.
        • Hermesh H.
        • Bar-Haim Y.
        Attention bias modification augments cognitive–behavioral group therapy for social anxiety disorder: A randomized controlled trial.
        Psychol Med. 2018; 48: 2177-2185
        • Wald I.
        • Fruchter E.
        • Ginat K.
        • Stolin E.
        • Dagan D.
        • Bliese P.D.
        • et al.
        Selective prevention of combat-related post-traumatic stress disorder using attention bias modification training: A randomized controlled trial.
        Psychol Med. 2016; 46: 2627-2636
        • White L.K.
        • Sequeira S.
        • Britton J.C.
        • Brotman M.A.
        • Gold A.L.
        • Berman E.
        • et al.
        Complementary features of attention bias modification therapy and cognitive-behavioral therapy in pediatric anxiety disorders.
        Am J Psychiatry. 2017; 174: 775-784
        • MacLeod C.
        • Rutherford E.
        • Campbell L.
        • Ebsworthy G.
        • Holker L.
        Selective attention and emotional vulnerability: Assessing the causal basis of their association through the experimental manipulation of attentional bias.
        J Abnorm Psychol. 2002; 111: 107-123
        • Bar-Haim Y.
        Research review: Attention bias modification (ABM): A novel treatment for anxiety disorders.
        J Child Psychol Psychiatry. 2010; 51: 859-870
        • Briggs-Gowan M.J.
        • Grasso D.
        • Bar-Haim Y.
        • Voss J.
        • McCarthy K.J.
        • Pine D.S.
        • Wakschlag L.S.
        Attention bias in the developmental unfolding of post-traumatic stress symptoms in young children at risk.
        J Child Psychol Psychiatry. 2016; 57: 1083-1091
        • Clark D.A.
        • Beck A.T.
        Cognitive theory and therapy of anxiety and depression: Convergence with neurobiological findings.
        Trends Cogn Sci. 2010; 14: 418-424
        • Frewen P.A.
        • Dozois D.J.A.
        • Lanius R.A.
        Neuroimaging studies of psychological interventions for mood and anxiety disorders: Empirical and methodological review.
        Clin Psychol Rev. 2008; 28: 228-246
        • Teicher M.H.
        • Samson J.A.
        Childhood maltreatment and psychopathology: A case for ecophenotypic variants as clinically and neurobiologically distinct subtypes.
        Am J Psychiatry. 2013; 170: 1114-1133

      Linked Article

      • Erratum
        Biological PsychiatryVol. 87Issue 3
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          Erratum to: “Neurobiological Markers of Resilience to Depression Following Childhood Maltreatment: The Role of Neural Circuits Supporting the Cognitive Control of Emotion,” by Rodman et al. (Biol Psychiatry 2019; 86:464–473); https://doi.org/10.1016/j.biopsych.2019.04.033 .
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