Childhood emotional maltreatment severity is associated with dorsal medial prefrontal cortex responsivity to social exclusion in young adults

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Van Harmelen, Anne Laura ^a,b   Hauber, Kirsten ^c   Moor, Bregtje Gunther ^a   Spinhoven, Philip ^a,d   Boon, Albert E ^c,e,f   Crone, Eveline A ^a   Elzinga, Bernet M ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c De Jutters Centre of Youth Mental Healthcare Haaglanden   (Netherlands)

^d LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^e Centre of Orthopsychiatry and Forensic Youth Psychiatry   (Netherlands)

^f Acad Ctr Child and Adol Psychiat   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; BEHAVIOR DISORDER; BRAIN FUNCTION; CHILDHOOD DISEASE; CHILDHOOD EMOTIONAL MALTREATMENT; CLINICAL ARTICLE; COGNITION; DISEASE SEVERITY; DISTRESS SYNDROME; DORSAL MEDIAL PREFRONTAL CORTEX; EMOTIONAL DISORDER; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MALE; POSTERIOR CINGULATE; PREFRONTAL CORTEX; SELF REPORT; SOCIAL EXCLUSION; THINKING; VENTROMEDIAL PREFRONTAL CORTEX; YOUNG ADULT;

ADOLESCENT; BRAIN MAPPING; CHILD ABUSE; EMOTIONS; FEMALE; GYRUS CINGULI; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; PARENTS; PREFRONTAL CORTEX; SELF CONCEPT; SOCIAL DISTANCE; YOUNG ADULT;

EID: 84896918416     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0085107     Document Type: Article

References (69)

1. APSAC APS on the A of C (1995) Guidelines for psychosocial evaluation of suspected psychological maltreatment in children and adolescents.
2. Hart H, Rubia K (2012) Neuroimaging of child abuse: a critical review. Front Hum Neurosci 6: 52. Available: http://www.pubmedcentral.nih.gov/ articlerender.fcgi?artid=3307045&tool=pmcentrez&rendertype=abstract. Accessed 11 March 2013.
3. Iffland B, Sansen LM, Catani C, Neuner F (2012) Emotional but not physical maltreatment is independently related to psychopathology in subjects with various degrees of social anxiety: a web-based internet survey. BMC Psychiatry 12: 49. Available: http://www.pubmedcentral.nih.gov/articlerender. fcgi?artid=3528417&tool=pmcentrez&rendertype=abstract. Accessed 20 May 2013.
4. Spinhoven P, Elzinga BM, Hovens JGFM, Roelofs K, Zitman FG, et al. (2010) The specificity of childhood adversities and negative life events across the life span to anxiety and depressive disorders. J Affect Disord 126: 103-112. Available: http://www.ncbi.nlm.nih.gov/pubmed/20304501. Accessed 11 March 2013.
5. DeWall CN, Bushman BJ (2011) Social Acceptance and Rejection: The Sweet and the Bitter. Curr Dir Psychol Sci 20: 256-260. Available: http://cdp.sagepub.com/content/20/4/256.full. Accessed 5 March 2013.
6. Rosenbach C, Renneberg B (2011) Abgelehnt, ausgeschlossen, ignoriert: Die Wahrnehmung sozialer Zurückweisung und psychische Störungen - eine Übersicht. Verhaltenstherapie 21: 87-98. Available: http://www.karger.com/ doi/10.1159/000328839. Accessed 20 May 2013.
7. Masten CL, Eisenberger NI, Borofsky L a, McNealy K, Pfeifer JH, et al. (2011) Subgenual anterior cingulate responses to peer rejection: a marker of adolescents' risk for depression. Dev Psychopathol 23: 283-292. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3229829&tool= pmcentrez&ren dertype=abstract. Accessed 19 March 2013.
8. Williams KD, Cheung CK, Choi W (2000) Cyberostracism: effects of being ignored over the Internet. J Pers Soc Psychol 79: 748-762. Available: http://www.ncbi.nlm.nih.gov/pubmed/11079239.
9. Williams KD, Jarvis B (2006) Cyberball: a program for use in research on interpersonal ostracism and acceptance. Behav Res Methods 38: 174-180. Available: http://www.ncbi.nlm.nih.gov/pubmed/16817529.
10. Boyes ME, French DJ (2009) Having a Cyberball: Using a ball-throwing game as an experimental social stressor to examine the relationship between neuroticism and coping. Pers Individ Dif 47: 396-401. Available: http://linkinghub.elsevier.com/retrieve/pii/S0191886909001615. Accessed 27 March 2013.
11. Moor BG, Güroǧlu B, Op de Macks Z a, Rombouts S a RB, Van der Molen MW, et al. (2012) Social exclusion and punishment of excluders: neural correlates and developmental trajectories. Neuroimage 59: 708-717. Available: http://www.ncbi.nlm.nih.gov/pubmed/21791248. Accessed 28 February 2013.
12. Themanson JR, Khatcherian SM, Ball AB, Rosen PJ (2012) An event-related examination of neural activity during social interactions. Soc Cogn Affect Neurosci: 1-7. Available: http://www.ncbi.nlm.nih.gov/pubmed/22577169. Accessed 20 May 2013.
13. Zadro L, Williams KD, Richardson R (2004) How low can you go? Ostracism by a computer is sufficient to lower self-reported levels of belonging, control, self-esteem, and meaningful existence. J Exp Soc Psychol 40: 560-567. Available: http://linkinghub.elsevier.com/retrieve/pii/S0022103103001823. Accessed 6 March 2013.
14. Eisenberger NI (2012) The pain of social disconnection: examining the shared neural underpinnings of physical and social pain. Nat Rev Neurosci 13: 421-434. Available: http://www.ncbi.nlm.nih.gov/pubmed/22551663. Accessed 3 March 2013.
15. Cacioppo S, Frum C, Asp E, Weiss RM, Lewis JW, et al. (2013) A Quantitative Meta-Analysis of Rejection: 10-12. doi:10.1038/srep02027.
16. Etkin A, Egner T, Kalisch R (2011) Emotional processing in anterior cingulate and medial prefrontal cortex. Trends Cogn Sci 15: 85-93. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3035157&tool= pmcentrez& rendertype=abstract. Accessed 1 March 2013.
17. Ridderinkhof KR, Ullsperger M, Crone E a, Nieuwenhuis S (2004) The role of the medial frontal cortex in cognitive control. Science 306: 443-447. Available: http://www.ncbi.nlm.nih.gov/pubmed/15486290.
18. Somerville LH, Heatherton TF, Kelley WM (2006) Anterior cingulate cortex responds differentially to expectancy violation and social rejection. Nat Neurosci 9: 1007-1008. Available: http://www.ncbi.nlm.nih.gov/pubmed/16819523. Accessed 10 March 2013.
19. Masten CL, Eisenberger NI, Pfeifer JH, Dapretto M (2010) Witnessing peer rejection during early adolescence: neural correlates of empathy for experiences of social exclusion. Soc Neurosci 5: 496-507. Available: http://www. pubmedcentral.nih.gov/articlerender.fcgi?artid=2957502&tool= pmcentrez&rendertype= abstract. Accessed 28 February 2013.
20. Yoshimura S, Ueda K, Suzuki S, Onoda K, Okamoto Y, et al. (2009) Self-referential processing of negative stimuli within the ventral anterior cingulate gyrus and right amygdala. Brain Cogn 69: 218-225. Available: http://www.ncbi.nlm.nih.gov/pubmed/18723260. Accessed 21 May 2013.
21. Masten CL, Eisenberger NI, Borofsky L a, Pfeifer JH, McNealy K, et al. (2009) Neural correlates of social exclusion during adolescence: understanding the distress of peer rejection. Soc Cogn Affect Neurosci 4: 143-157. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2686232&tool= pmcentrez&rendertype=abstract. Accessed 28 February 2013.
22. Sebastian CL, Tan GCY, Roiser JP, Viding E, Dumontheil I, et al. (2011) Developmental influences on the neural bases of responses to social rejection: implications of social neuroscience for education. Neuroimage 57: 686-694. Available: http://www.ncbi.nlm.nih.gov/pubmed/20923708. Accessed 28 February 2013.
23. Bolling DZ, Pitskel NB, Deen B, Crowley MJ, McPartland JC, et al. (2011) Enhanced neural responses to rule violation in children with autism: a comparison to social exclusion. Dev Cogn Neurosci 1: 280-294. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3129780&tool= pmcentrez&rendertype=abstract. Accessed 22 May 2013.
24. Eisenberger NI, Way BM, Taylor SE, Welch WT, Lieberman MD (2007) Understanding genetic risk for aggression: clues from the brain's response to social exclusion. Biol Psychiatry 61: 1100-1108. Available: http://www.ncbi.nlm. nih.gov/pubmed/17137563. Accessed 22 May 2013.
25. Burklund LJ, Eisenberger NI, Lieberman MD (2007) The face of rejection: rejection sensitivity moderates dorsal anterior cingulate activity to disapproving facial expressions. Soc Neurosci 2: 238-253. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2373282&tool= pmcentrez&rendertype=abstract. Accessed 22 May 2013.
26. DeWall CN, Masten CL, Powell C, Combs D, Schurtz DR, et al. (2012) Do neural responses to rejection depend on attachment style? An fMRI study. Soc Cogn Affect Neurosci 7: 184-192. Available: http://scan.oxfordjournals.org/ content/7/2/184.short. Accessed 28 February 2013.
27. Onoda K, Okamoto Y, Nakashima K, Nittono H, Yoshimura S, et al. (2010) Does low self-esteem enhance social pain? The relationship between trait self-esteem and anterior cingulate cortex activation induced by ostracism. Soc Cogn Affect Neurosci 5: 385-391. Available: http://www.pubmedcentral.nih.gov/ articlerender.fcgi?artid=2999754&tool=pmcentrez&rendertype=abstract. Accessed 22 May 2013.
28. Somerville LH, Kelley WM, Heatherton TF (2010) Self-esteem modulates medial prefrontal cortical responses to evaluative social feedback. Cereb Cortex 20: 3005-3013. Available: http://cercor.oxfordjournals.org/content/20/12/3005. short. Accessed 20 March 2013.
29. Spitzer RL, Williams JBW, Gibbon M, First MB (1990) Structured Clinical Interview for DSM-III-R, Patient Edition/Non-patient Edition,(SCID-P/SCIDNP), Washington, D.C.: American Psychiatric Press, Inc.
30. Bernstein DP, Fink L (1998) Childhood Trauma Questionnaire, a retrospective self-report manual. San Antonio, TX: The Psychological Corporation.
31. Wechsler D (1991) WISC-III: Wechsler intelligence scale for children. Available: http://www.getcited.org/pub/103253171. Accessed 31 May 2013.
32. Wechsler D (1997) WAIS-III: Wechsler adult intelligence scale. San Antonio: Psychological Corporation.
33. First MB, Gibbon M (1997) User's guide for the structured clinical interview for DSM-IV axis I disorders: SCID-1 clinician version. American Psychiatric Publisher.
34. Achenbach TM (1991) Manual for the Child Behavior Checklist.
35. Duijsens IJ, Eurelings-Bontekoe EHM, Diekstra RFW (1996) The VKP, a self-report instrument for DSM-III-R and ICD-10 personality disorders: construction and psychometric properties. Pers Individ Dif 20: 171-182. (Pubitemid 126400678)
36. Arntz A, Wessel I (1996) Jeugd trauma vragenlijst [Dutch version of the childhood trauma questionnaire]. The Netherlands.
37. Thombs BD, Bernstein DP, Lobbestael J, Arntz A (2009) A validation study of the Dutch Childhood Trauma Questionnaire-Short Form: factor structure, reliability, and known-groups validity. Child Abuse Negl 33: 518-523. Available: http://www.ncbi.nlm.nih.gov/pubmed/19758699. Accessed 22 May 2013.
38. Van Harmelen A-L, De Jong PJ, Glashouwer KA, Spinhoven P, Penninx BWJH, et al. (2010) Child abuse and negative explicit and automatic self-associations: the cognitive scars of emotional maltreatment. Behav Res Ther 48: 486-494. Available: http://www.ncbi.nlm.nih.gov/pubmed/20303472.
39. Van Harmelen A-L, Elzinga BM, Kievit RA, Spinhoven P (2011) Intrusions of autobiographical memories in individuals reporting childhood emotional maltreatment. Eur J Psychotraumatol 2. Available: http://www.pubmedcentral.nih. gov/articlerender.fcgi?artid=3402144&tool=pmcentrez&renabstract. Accessed 22 May dertype=2013.
40. Trickett PK, Mennen FE, Kim K, Sang J (2009) Emotional abuse in a sample of multiply maltreated, urban young adolescents: issues of definition and identification. Child Abuse Negl 33: 27-35. Available: http://www.ncbi.nlm.nih. gov/pubmed/19178945. Accessed 20 May 2013.
41. Van Beest I, Williams KD (2006) When inclusion costs and ostracism pays, ostracism still hurts. J Pers Soc Psychol 91: 918-928. Available: http://www.ncbi.nlm.nih.gov/pubmed/17059310. Accessed 22 May 2013.
42. Sebastian C, Viding E, Williams KD, Blakemore S-J (2010) Social brain development and the affective consequences of ostracism in adolescence. Brain Cogn 72: 134-145. Available: http://www.ncbi.nlm.nih.gov/pubmed/19628323. Accessed 22 May 2013.
43. Lieberman MD, Cunningham W a (2009) Type I and Type II error concerns in fMRI research: re-balancing the scale. Soc Cogn Affect Neurosci 4: 423-428. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid= 2799956&tool=pmcentrez&rendertype=abstract. Accessed 27 February 2013.
44. Meyer ML, Masten CL, Ma Y, Wang C, Shi Z, et al. (2012) Empathy for the social suffering of friends and strangers recruits distinct patterns of brain activation. Soc Cogn Affect Neurosci. Available: http://www.ncbi.nlm.nih.gov/ pubmed/22355182. Accessed 3 March 2013.
45. Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19: 1233-1239. Available: http://www.ncbi.nlm.nih.gov/ pubmed/12880848. Accessed 22 May 2013.
46. Brett MA.-L, Valabregue R, Poline J-B (2002) Region of interest analysis using an SPM toolbox. 8th International Conferance on Functional Mapping of the Human Brain. Sendai, Japan. p. abstract 497.
47. Sebastian CL, Fontaine NMG, Bird G, Blakemore S-J, Brito S a De, et al. (2012) Neural processing associated with cognitive and affective Theory of Mind in adolescents and adults. Soc Cogn Affect Neurosci 7: 53-63. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3252629&tool= pmcentrez&rendertype=abstract. Accessed 28 February 2013.
48. Van der Meer L, Costafreda S, Aleman A, David AS (2010) Self-reflection and the brain: a theoretical review and meta-analysis of neuroimaging studies with implications for schizophrenia. Neurosci Biobehav Rev 34: 935-946. Available: http://www.ncbi.nlm.nih.gov/pubmed/20015455. Accessed 21 May 2013.
49. Moran JM, Macrae CN, Heatherton TF, Wyland CL, Kelley WM (2006) Neuroanatomical evidence for distinct cognitive and affective components of self. J Cogn Neurosci 18: 1586-1594. Available: http://www.ncbi.nlm.nih.gov/ pubmed/16989558. Accessed 21 May 2013.
50. Grimm S, Ernst J, Boesiger P, Schuepbach D, Hell D, et al. (2009) Increased self-focus in major depressive disorder is related to neural abnormalities in subcortical-cortical midline structures. Hum Brain Mapp 30: 2617-2627. Available: http://www.ncbi.nlm.nih.gov/pubmed/19117277. Accessed 21 May 2013.
51. Blair KS, Geraci M, Smith BW, Hollon N, DeVido J, et al. (2012) Reduced dorsal anterior cingulate cortical activity during emotional regulation and top-down attentional control in generalized social phobia, generalized anxiety disorder, and comorbid generalized social phobia/generalized anxiety disorder. Biol Psychiatry 72: 476-482. Available: http://www.ncbi.nlm.nih.gov/pubmed/ 22592057. Accessed 4 March 2013.
52. Lemogne C, le Bastard G, Mayberg H, Volle E, Bergouignan L, et al. (2009) In search of the depressive self: extended medial prefrontal network during self-referential processing in major depression. Soc Cogn Affect Neurosci 4: 305-312. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid= 2728628&tool=pmcentrez&rendertype=abstract. Accessed 21 May 2013.
53. Lindquist K a, Wager TD, Kober H, Bliss-Moreau E, Barrett LF (2012) The brain basis of emotion: a meta-analytic review. Behav Brain Sci 35: 121-143. Available: http://www.ncbi.nlm.nih.gov/pubmed/22617651. Accessed 2 March 2013.
54. Beck AT (2008) The evolution of the cognitive model of depression and its neurobiological correlates. Am J Psychiatry 165: 969-977. Available: http://www.ncbi.nlm.nih.gov/pubmed/18628348. Accessed 21 March 2013.
55. Czéh B, Müller-Keuker JIH, Rygula R, Abumaria N, Hiemke C, et al. (2007) Chronic social stress inhibits cell proliferation in the adult medial prefrontal cortex: hemispheric asymmetry and reversal by fluoxetine treatment. Neuropsychopharmacology 32: 1490-1503. Available: http://www.ncbi.nlm.nih.gov/pubmed/17164819. Accessed 7 March 2013.
56. Sánchez MM, Ladd CO, Plotsky PM (2001) Early adverse experience as a developmental risk factor for later psychopathology: evidence from rodent and primate models. Dev Psychopathol 13: 419-449. Available: http://www.ncbi.nlm. nih.gov/pubmed/11523842.
57. Sanchez MM, Alagbe O, Felger JC, Zhang J, Graff AE, et al. (2007) Activated p38 MAPK is associated with decreased CSF 5-HIAA and increased maternal rejection during infancy in rhesus monkeys. Mol Psychiatry 12: 895-897. Available: http://www.ncbi.nlm.nih.gov/pubmed/17895923. Accessed 14 May 2013.
58. Arnsten AFT (2009) Stress signalling pathways that impair prefrontal cortex structure and function. Nat Rev Neurosci 10: 410-422. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2907136&tool= pmcentrez&rendertype=abstract. Accessed 1 March 2013.
59. Lupien SJ, McEwen BS, Gunnar MR, Heim C (2009) Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 10: 434-445. Available: http://www.ncbi.nlm.nih.gov/pubmed/19401723. Accessed 28 February 2013.
60. McEwen BS, Eiland L, Hunter RG, Miller MM (2012) Stress and anxiety: structural plasticity and epigenetic regulation as a consequence of stress. Neuropharmacology 62: 3-12. Available: http://www.pubmedcentral.nih.gov/ articlerender.fcgi?artid=3196296&tool=pmcentrez&rendertype=abstract. Accessed 5 March 2013.
61. Van Harmelen A-L, Van Tol M-J, Van Der Wee NJA, Veltman DJ, Aleman A, et al. (2010) Reduced medial prefrontal cortex volume in adults reporting childhood emotional maltreatment. Biol Psychiatry 68: 832-838. Available: http://www.ncbi.nlm.nih.gov/pubmed/20692648.
62. Dannlowski U, Stuhrmann A, Beutelmann V, Zwanzger P, Lenzen T, et al. (2012) Limbic scars: long-term consequences of childhood maltreatment revealed by functional and structural magnetic resonance imaging. Biol Psychiatry 71: 286-293. Available: http://www.ncbi.nlm.nih.gov/pubmed/22112927. Accessed 4 March 2013.
63. Tomoda A, Sheu Y-S, Rabi K, Suzuki H, Navalta CP, et al. (2011) Exposure to parental verbal abuse is associated with increased gray matter volume in superior temporal gyrus. Neuroimage 54 Suppl 1: S280-6. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2950228&tool= pmcentrez&rendertype=abstract. Accessed 17 May 2013.
64. Egeland B (2009) Taking stock: childhood emotional maltreatment and developmental psychopathology. Child Abuse Negl 33: 22-26. Available: http://www.ncbi.nlm.nih.gov/pubmed/19167068. Accessed 25 March 2013.
65. Gilbert R, Widom CS, Browne K, Fergusson D, Webb E, et al. (2009) Burden and consequences of child maltreatment in high-income countries. Lancet 373: 68-81. Available: http://www.ncbi.nlm.nih.gov/pubmed/19056114. Accessed 28 February 2013.
66. Ellis BJ, Boyce WT, Belsky J, Bakermans-Kranenburg MJ, van Ijzendoorn MH (2011) Differential susceptibility to the environment: an evolutionary - neurodevelopmental theory. Dev Psychopathol 23: 7-28. Available: http://www.ncbi.nlm.nih.gov/pubmed/21262036. Accessed 21 May 2013.
67. Hardt J, Rutter M (2004) Validity of adult retrospective reports of adverse childhood experiences: review of the evidence. J Child Psychol Psychiatry 45: 260-273. Available: http://www.ncbi.nlm.nih.gov/pubmed/14982240.
68. Tonmyr L, Draca J, Crain J, Macmillan HL (2011) Measurement of emotional/psychological child maltreatment: a review. Child Abuse Negl 35: 767-782. Available: http://www.ncbi.nlm.nih.gov/pubmed/22018520. Accessed 20 May 2013.
69. Etkin A, Prater KE, Hoeft F, Menon V, Schatzberg AF (2010) Failure of anterior cingulate activation and connectivity with the amygdala during implicit regulation of emotional processing in generalized anxiety disorder. Am J Psychiatry 167: 545-554. Available: http://www.ncbi.nlm.nih.gov/pubmed/20123913. Accessed 18 March 2013.