Atypical Prefrontal–Amygdala Circuitry Following Childhood Exposure to Abuse: Links With Adolescent Psychopathology

Adverse childhood experiences have been associated with more negative coupling between the ventromedial prefrontal cortex (vmPFC) and amygdala, a brain network involved in emotion regulation in both children and adults. This pattern may be particularly likely to emerge in individuals exposed to threatening experiences during childhood (e.g., exposure to child abuse), although this has not been examined in prior research. We collected functional magnetic resonance imaging data on 57 adolescents during an emotion regulation task. Greater negative functional connectivity between vmPFC and amygdala occurred during viewing of negative compared to neutral images. This vmPFC-amygdala task-related functional connectivity was more negative in adolescents exposed to physical, sexual, or emotional abuse than those without a history of maltreatment and was associated with abuse severity. This pattern of more negative functional connectivity was associated with higher levels of externalizing psychopathology concurrently and 2 years later. Greater negative connectivity in the vmPFC-amygdala network during passive viewing of negative images may reflect disengagement of regulatory responses from vmPFC in situations eliciting strong amygdala reactivity, potentially due to stronger appraisals of threat in children exposed to early threatening environments. This pattern may be adaptive in the short term but place adolescents at higher risk of psychopathology later in life.

[1]  Martin H. Teicher,et al.  Childhood stress, grown-up brain networks: corticolimbic correlates of threat-related early life stress and adult stress response , 2017, Psychological Medicine.

[2]  Matthew L. Dixon,et al.  Emotion and the Prefrontal Cortex: An Integrative Review , 2017, Psychological bulletin.

[3]  K. McLaughlin,et al.  Child Trauma Exposure and Psychopathology: Mechanisms of Risk and Resilience. , 2017, Current opinion in psychology.

[4]  D. Pine,et al.  Childhood abuse and reduced cortical thickness in brain regions involved in emotional processing. , 2016, Journal of child psychology and psychiatry, and allied disciplines.

[5]  Katie A McLaughlin,et al.  Beyond Cumulative Risk , 2016, Current directions in psychological science.

[6]  Cory A. Burghy,et al.  Enhanced prefrontal-amygdala connectivity following childhood adversity as a protective mechanism against internalizing in adolescence. , 2016, Biological psychiatry. Cognitive neuroscience and neuroimaging.

[7]  Thomas J. Grabowski,et al.  Using Make for Reproducible and Parallel Neuroimaging Workflow and Quality-Assurance , 2016, Front. Neuroinform..

[8]  K. McLaughlin,et al.  Childhood Maltreatment Exposure and Disruptions in Emotion Regulation: A Transdiagnostic Pathway to Adolescent Internalizing and Externalizing Psychopathology , 2016, Cognitive Therapy and Research.

[9]  D. Rosenberg,et al.  Altered amygdala connectivity in urban youth exposed to trauma. , 2015, Social cognitive and affective neuroscience.

[10]  A. Gold,et al.  Child Maltreatment and Neural Systems Underlying Emotion Regulation. , 2015, Journal of the American Academy of Child and Adolescent Psychiatry.

[11]  Amit Etkin,et al.  Childhood Trauma Exposure Disrupts the Automatic Regulation of Emotional Processing , 2015, Neuropsychopharmacology.

[12]  Jennifer A. Silvers,et al.  Cognitive reappraisal of emotion: a meta-analysis of human neuroimaging studies. , 2014, Cerebral cortex.

[13]  Eva H. Telzer,et al.  Maternal Buffering of Human Amygdala-Prefrontal Circuitry During Childhood but Not During Adolescence , 2014, Psychological science.

[14]  M. Phillips,et al.  CHILDHOOD MALTREATMENT AND COMBAT POSTTRAUMATIC STRESS DIFFERENTIALLY PREDICT FEAR‐RELATED FRONTO‐SUBCORTICAL CONNECTIVITY , 2014, Depression and anxiety.

[15]  Kosuke Imai,et al.  mediation: R Package for Causal Mediation Analysis , 2014 .

[16]  S. Pollak,et al.  Impact of physical maltreatment on the regulation of negative affect and aggression , 2014, Development and Psychopathology.

[17]  Cory A. Burghy,et al.  Childhood maltreatment is associated with altered fear circuitry and increased internalizing symptoms by late adolescence , 2013, Proceedings of the National Academy of Sciences.

[18]  Todd A. Hare,et al.  Early developmental emergence of human amygdala–prefrontal connectivity after maternal deprivation , 2013, Proceedings of the National Academy of Sciences.

[19]  Todd A. Hare,et al.  A Developmental Shift from Positive to Negative Connectivity in Human Amygdala–Prefrontal Circuitry , 2013, The Journal of Neuroscience.

[20]  A. Mechelli,et al.  Amygdala activation in maltreated children during pre-attentive emotional processing , 2013, British Journal of Psychiatry.

[21]  S. Rombouts,et al.  Resting-state functional connectivity in adults with childhood emotional maltreatment , 2012, Psychological Medicine.

[22]  R. Kessler,et al.  Childhood adversities and first onset of psychiatric disorders in a national sample of US adolescents. , 2012, Archives of general psychiatry.

[23]  Richard J. Davidson,et al.  Developmental pathways to amygdala-prefrontal function and internalizing symptoms in adolescence , 2012, Nature Neuroscience.

[24]  Timothy E. J. Behrens,et al.  Tools of the trade: psychophysiological interactions and functional connectivity. , 2012, Social cognitive and affective neuroscience.

[25]  Jennifer A. Silvers,et al.  Functional imaging studies of emotion regulation: a synthetic review and evolving model of the cognitive control of emotion , 2012, Annals of the New York Academy of Sciences.

[26]  G. Quirk,et al.  Fear extinction as a model for translational neuroscience: ten years of progress. , 2012, Annual review of psychology.

[27]  D. Gee,et al.  Anxiety dissociates dorsal and ventral medial prefrontal cortex functional connectivity with the amygdala at rest. , 2011, Cerebral cortex.

[28]  T. Egner,et al.  Emotional processing in anterior cingulate and medial prefrontal cortex , 2011, Trends in Cognitive Sciences.

[29]  Susanne Schweizer,et al.  Emotion-regulation strategies across psychopathology: A meta-analytic review. , 2010, Clinical psychology review.

[30]  R. Kessler,et al.  Childhood adversities and adult psychiatric disorders in the national comorbidity survey replication I: associations with first onset of DSM-IV disorders. , 2010, Archives of general psychiatry.

[31]  D. Cicchetti,et al.  Longitudinal pathways linking child maltreatment, emotion regulation, peer relations, and psychopathology. , 2009, Journal of child psychology and psychiatry, and allied disciplines.

[32]  J. Green Childhood adversities and adult psychopathology in the National Comorbidity Survey Replication (NCS-R) I: Associations with first onset of DSM-IV disorders , 2010 .

[33]  J. Price,et al.  Neurocircuitry of Mood Disorders , 2010, Neuropsychopharmacology.

[34]  P. Whalen,et al.  The Structural Integrity of an Amygdala–Prefrontal Pathway Predicts Trait Anxiety , 2009, The Journal of Neuroscience.

[35]  Martin P Paulus,et al.  Anxiety vulnerability is associated with altered anterior cingulate response to an affective appraisal task , 2008, Neuroreport.

[36]  E. Kandel,et al.  Resolving Emotional Conflict: A Role for the Rostral Anterior Cingulate Cortex in Modulating Activity in the Amygdala , 2006, Neuron.

[37]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[38]  P. Lang International affective picture system (IAPS) : affective ratings of pictures and instruction manual , 2005 .

[39]  Joseph E LeDoux,et al.  Extinction Learning in Humans Role of the Amygdala and vmPFC , 2004, Neuron.

[40]  R. Vertes Differential projections of the infralimbic and prelimbic cortex in the rat , 2004, Synapse.

[41]  P. Sinha,et al.  Effects of early experience on children's recognition of facial displays of emotion. , 2002, Developmental psychology.

[42]  J. Brown,et al.  Child abuse and neglect and the development of mental disorders in the general population , 2001, Development and Psychopathology.

[43]  D. Shaffer,et al.  NIMH Diagnostic Interview Schedule for Children Version IV (NIMH DISC-IV): description, differences from previous versions, and reliability of some common diagnoses. , 2000, Journal of the American Academy of Child and Adolescent Psychiatry.

[44]  M. Kelley,et al.  Development and Validation of the Screen for Adolescent Violence Exposure (SAVE) , 1997, Journal of abnormal child psychology.

[45]  D. Bernstein,et al.  Validity of the Childhood Trauma Questionnaire in an adolescent psychiatric population. , 1997, Journal of the American Academy of Child and Adolescent Psychiatry.

[46]  A. Bifulco,et al.  Childhood Experience of Care and Abuse (CECA): a retrospective interview measure. , 1994, Journal of child psychology and psychiatry, and allied disciplines.

[47]  G. S. Pettit,et al.  Mechanisms in the cycle of violence. , 1990, Science.