Enhanced Prefrontal-Amygdala Connectivity Following Childhood Adversity as a Protective Mechanism Against Internalizing in Adolescence

Biological Psychiatry: Cognitive Neuroscience and Neuroimaging

Volumn 1, Issue 4, 2016, Pages 326-334

  Herringa, Ryan J ^a   Burghy, Cory A ^b   Stodola, Diane E ^b   Fox, Michelle E ^d   Davidson, Richard J ^a,b,c   Essex, Marilyn J ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

^d GEORGIA STATE UNIVERSITY   (United States)

Author keywords

Adolescence; Anxiety; Childhood adversity; Depression; Neuroimaging; Stress adaptation

Indexed keywords

ADOLESCENT DISEASE; ADULT; AMYGDALA; ARTICLE; BRAIN FUNCTION; CHILDHOOD DISEASE; EMOTION; FEMALE; HIPPOCAMPUS; HUMAN; LIFESPAN; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MALE; PREFRONTAL CORTEX; SEX DIFFERENCE; YOUNG ADULT;

EID: 84975460047     PISSN: 24519022     EISSN: 24519030     Source Type: Journal    
DOI: 10.1016/j.bpsc.2016.03.003     Document Type: Article

References (41)

1. R.F. Anda, V.J. Felitti, J.D. Bremner, J.D. Walker, C. Whitfield, B.D. Perry, and et al. The enduring effects of abuse and related adverse experiences in childhood. A convergence of evidence from neurobiology and epidemiology Eur Arch Psychiatry Clin Neurosci 256 2006 174 186
2. J.G. Green, K.A. McLaughlin, P.A. Berglund, M.J. Gruber, N.A. Sampson, A.M. Zaslavsky, and R.C. Kessler Childhood adversities and adult psychiatric disorders in the national comorbidity survey replication I: Associations with first onset of DSM-IV disorders Arch Gen Psychiatry 67 2010 113 123
3. N.P. Daskalakis, R.C. Bagot, K.J. Parker, C.H. Vinkers, and E.R. de Kloet The three-hit concept of vulnerability and resilience: Toward understanding adaptation to early-life adversity outcome Psychoneuroendocrinology 38 2013 1858 1873
4. K.A. DuMont, C.S. Widom, and S.J. Czaja Predictors of resilience in abused and neglected children grown-up: The role of individual and neighborhood characteristics Child Abuse Negl 31 2007 255 274
5. A.S. Garrett, V. Carrion, H. Kletter, A. Karchemskiy, C.F. Weems, and A. Reiss Brain activation to facial expressions in youth with PTSD symptoms Depress Anxiety 29 2012 449 459
6. D.G. Gee, L.J. Gabard-Durnam, J. Flannery, B. Goff, K.L. Humphreys, E.H. Telzer, and et al. Early developmental emergence of human amygdala-prefrontal connectivity after maternal deprivation Proc Natl Acad Sci U S A 110 2013 15638 15643
7. P. Kim, G.W. Evans, M. Angstadt, S.S. Ho, C.S. Sripada, J.E. Swain, and et al. Effects of childhood poverty and chronic stress on emotion regulatory brain function in adulthood Proc Natl Acad Sci U S A 110 2013 18442 18447
8. E.J. McCrory, S.A. De Brito, C.L. Sebastian, A. Mechelli, G. Bird, P.A. Kelly, and E. Viding Heightened neural reactivity to threat in child victims of family violence Curr Biol 21 2011 R947 948
9. K.A. McLaughlin, M. Peverill, A.L. Gold, S. Alves, and M.A. Sheridan Child maltreatment and neural systems underlying emotion regulation J Am Acad Child Adolesc Psychiatry. 54 2015 753 762
10. J.R. Swartz, D.E. Williamson, and A.R. Hariri Developmental change in amygdala reactivity during adolescence: effects of family history of depression and stressful life events Am J Psychiatry 172 2015 276 283
11. U. Dannlowski, A. Stuhrmann, V. Beutelmann, P. Zwanzger, T. Lenzen, D. Grotegerd, and et al. Limbic scars: Long-term consequences of childhood maltreatment revealed by functional and structural magnetic resonance imaging Biol Psychiatry 71 2012 286 293
12. U. Dannlowski, H. Kugel, F. Huber, A. Stuhrmann, R. Redlich, D. Grotegerd, and et al. Childhood maltreatment is associated with an automatic negative emotion processing bias in the amygdala Hum Brain Mapp 34 2013 2899 2909
13. H. Suzuki, J.L. Luby, K.N. Botteron, R. Dietrich, M.P. McAvoy, and D.M. Barch Early life stress and trauma and enhanced limbic activation to emotionally valenced faces in depressed and healthy children J Am Acad Child Adolesc Psychiatry 53 2014 800-813.e10
14. F.S. Maheu, M. Dozier, A.E. Guyer, D. Mandell, E. Peloso, K. Poeth, and 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 10 2010 34 49
15. M. Malter Cohen, D. Jing, R.R. Yang, N. Tottenham, F.S. Lee, and B.J. Casey Early-life stress has persistent effects on amygdala function and development in mice and humans Proc Natl Acad Sci U S A 110 2013 18274 18278
16. N. Tottenham, T.A. Hare, A. Millner, T. Gilhooly, J.D. Zevin, and B.J. Casey Elevated amygdala response to faces following early deprivation Dev Sci 14 2011 190 204
17. J.C. Crozier, L. Wang, S.A. Huettel, and M.D. De Bellis Neural correlates of cognitive and affective processing in maltreated youth with posttraumatic stress symptoms: does gender matter? Dev Psychopathol 26 2014 491 513
18. G.A. Fonzo, J. Huemer, and A. Etkin History of childhood maltreatment augments dorsolateral prefrontal processing of emotional valence in PTSD J Psychiatr Res 74 2016 45 54
19. R.C. Wolf, and R.J. Herringa Prefrontal-amygdala dysregulation to threat in pediatric posttraumatic stress disorder Neuropsychopharmacology 41 2016 822 831
20. M.J. Kim, D.G. Gee, R.A. Loucks, F.C. Davis, and P.J. Whalen Anxiety dissociates dorsal and ventral medial prefrontal cortex functional connectivity with the amygdala at rest Cereb Cortex 21 2011 1667 1673
21. H. Lee, A.S. Heller, C.M. van Reekum, B. Nelson, and R.J. Davidson Amygdala-prefrontal coupling underlies individual differences in emotion regulation Neuroimage 62 2012 1575 1581
22. C.A. Burghy, D.E. Stodola, P.L. Ruttle, E.K. Molloy, J.M. Armstrong, J.A. Oler, and et al. Developmental pathways to amygdala-prefrontal function and internalizing symptoms in adolescence Nat Neurosci 15 2012 1736 1741
23. R.J. Herringa, R.M. Birn, P.L. Ruttle, C.A. Burghy, D.E. Stodola, R.J. Davidson, and M.J. Essex Childhood maltreatment is associated with altered fear circuitry and increased internalizing symptoms by late adolescence Proc Natl Acad Sci U S A 110 2013 19119 19124
24. S. Maren, K.L. Phan, and I. Liberzon The contextual brain: Implications for fear conditioning, extinction and psychopathology Nat Rev Neurosci 14 2013 417 428
25. M.J. Essex, W.T. Boyce, L.H. Goldstein, J.M. Armstrong, H.C. Kraemer, and D.J. Kupfer The confluence of mental, physical, social, and academic difficulties in middle childhood. II: Developing the MacArthur Health and Behavior Questionnaire J Am Acad Child Adolesc Psychiatry 41 2002 588 603
26. B.S. Schuyler, T.R.A. Kral, J. Jacquart, C.A. Burghy, H.Y. Weng, D.M. Perlman, and et al. Temporal dynamics of emotional responding: Amygdala recovery predicts emotional traits Soc Cogn Affect Neurosci 9 2014 176 181
27. M.J. Essex, M.H. Klein, E. Cho, and N.H. Kalin Maternal stress beginning in infancy may sensitize children to later stress exposure: Effects on cortisol and behavior Biol Psychiatry 52 2002 776 784
28. P.J. Lang, M.M. Bradley, and B.N. Cuthbert International Affective Picture System (IAPS): Affective Ratings of Pictures and Instruction Manual. Technical Report A-8 2008 University of Florida Gainesville, FL
29. J. Ashburner A fast diffeomorphic image registration algorithm Neuroimage 38 2007 95 113
30. R.W. Cox AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages Comput Biomed Res 29 1996 162 173
31. J.C. Britton, C. Grillon, S. Lissek, M.A. Norcross, K.L. Szuhany, G. Chen, and et al. Response to learned threat: An FMRI study in adolescent and adult anxiety Am J Psychiatry 170 2013 1195 1204
32. J.L. Lancaster, M.G. Woldorff, L.M. Parsons, M. Liotti, C.S. Freitas, L. Rainey, and et al. Automated Talairach Atlas labels for functional brain mapping Hum Brain Mapp 10 2000 120 131
33. M.J. Essex, H.C. Kraemer, J.M. Armstrong, W.T. Boyce, H.H. Goldsmith, M.H. Klein, and et al. Exploring risk factors for the emergence of children's mental health problems Arch Gen Psychiatry 63 2006 1246 1256
34. M. Rutter Resilience as a dynamic concept Dev Psychopathol 24 2012 335 344
35. J.P. Hamilton, A. Etkin, D.J. Furman, M.G. Lemus, R.F. Johnson, and I.H. Gotlib Functional neuroimaging of major depressive disorder: A meta-analysis and new integration of base line activation and neural response data Am J Psychiatry 169 2012 693 703
36. A. Etkin, and T.D. Wager Functional neuroimaging of anxiety: A meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia Am J Psychiatry 164 2007 1476 1488
37. K.N. Ochsner, J.A. Silvers, and J.T. Buhle Functional imaging studies of emotion regulation: A synthetic review and evolving model of the cognitive control of emotion Ann N Y Acad Sci 1251 2012 E1 24
38. M.R. Milad, and G.J. Quirk Fear extinction as a model for translational neuroscience: Ten years of progress Annu Rev Psychol 63 2012 129 151
39. R. Admon, G. Lubin, O. Stern, K. Rosenberg, L. Sela, H. Ben-Ami, and T. Hendler Human vulnerability to stress depends on amygdala's predisposition and hippocampal plasticity Proc Natl Acad Sci U S A 106 2009 14120 14125
40. A.X. Gorka, J.L. Hanson, S.R. Radtke, and A.R. Hariri Reduced hippocampal and medial prefrontal gray matter mediate the association between reported childhood maltreatment and trait anxiety in adulthood and predict sensitivity to future life stress Biol Mood Anxiety Disord 4 2014 12
41. R.C. Kessler, P. Berglund, O. Demler, R. Jin, K.R. Merikangas, and E.E. Walters Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication Arch Gen Psychiatry 62 2005 593 602