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Childhood trauma is associated with increased brain responses to emotionally negative as compared with positive faces in patients with psychotic disorders

Published online by Cambridge University Press:  11 November 2016

M. Aas ,
K. Kauppi ,
C. L. Brandt ,
M. Tesli ,
T. Kaufmann ,
N. E. Steen ,
I. Agartz ,
L. T. Westlye ,
O. A. Andreassen  and
I. Melle
M. Aas*
Affiliation:
NORMENT, K.G. Jebsen Centre for Psychosis Research, Institute of Clinical Medicine, University of Oslo, Oslo, Norway Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway
K. Kauppi
Affiliation:
NORMENT, K.G. Jebsen Centre for Psychosis Research, Institute of Clinical Medicine, University of Oslo, Oslo, Norway Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway
C. L. Brandt
Affiliation:
NORMENT, K.G. Jebsen Centre for Psychosis Research, Institute of Clinical Medicine, University of Oslo, Oslo, Norway Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway
M. Tesli
Affiliation:
NORMENT, K.G. Jebsen Centre for Psychosis Research, Institute of Clinical Medicine, University of Oslo, Oslo, Norway Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway
T. Kaufmann
Affiliation:
NORMENT, K.G. Jebsen Centre for Psychosis Research, Institute of Clinical Medicine, University of Oslo, Oslo, Norway Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway
N. E. Steen
Affiliation:
NORMENT, K.G. Jebsen Centre for Psychosis Research, Institute of Clinical Medicine, University of Oslo, Oslo, Norway Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway Drammen Outpatient Clinic, Clinic of Mental Health and Addiction, Vestre Viken Hospital Trust, Drammen, Norway
I. Agartz
Affiliation:
NORMENT, K.G. Jebsen Centre for Psychosis Research, Institute of Clinical Medicine, University of Oslo, Oslo, Norway Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway Department of Psychiatric Research, Diakonhjemmet Hospital, Oslo, Norway
L. T. Westlye
Affiliation:
NORMENT, K.G. Jebsen Centre for Psychosis Research, Institute of Clinical Medicine, University of Oslo, Oslo, Norway Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway Department of Psychology, University of Oslo, Oslo, Norway
O. A. Andreassen
Affiliation:
NORMENT, K.G. Jebsen Centre for Psychosis Research, Institute of Clinical Medicine, University of Oslo, Oslo, Norway Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway
I. Melle
Affiliation:
NORMENT, K.G. Jebsen Centre for Psychosis Research, Institute of Clinical Medicine, University of Oslo, Oslo, Norway Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway
*
*Address for correspondence: M. Aas, Ph.D., Division of Mental Health and Addiction, NORMENT, K.G. Jebsen Psychosis Research Centre, Institute of Clinical Medicine, Bygg 49, Oslo University Hospital, PO Box 4956 Nydalen, 0424 Oslo, Norway. (Email: monica.aas@medisin.uio.no)
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Abstract

Background

Childhood trauma increases risk of a range of mental disorders including psychosis. Whereas the mechanisms are unclear, previous evidence has implicated atypical processing of emotions among the core cognitive models, in particular suggesting altered attentional allocation towards negative stimuli and increased negativity bias. Here, we tested the association between childhood trauma and brain activation during emotional face processing in patients diagnosed with psychosis continuum disorders. In particular, we tested if childhood trauma was associated with the differentiation in brain responses between negative and positive face stimuli. We also tested if trauma was associated with emotional ratings of negative and positive faces.

Method

We included 101 patients with a Diagnostic and Statistical Manual of Mental Disorders (DSM) schizophrenia spectrum or bipolar spectrum diagnosis. History of childhood trauma was obtained using the Childhood Trauma Questionnaire. Brain activation was measured with functional magnetic resonance imaging during presentation of faces with negative or positive emotional expressions. After the scanner session, patients performed emotional ratings of the same faces.

Results

Higher levels of total childhood trauma were associated with stronger differentiation in brain responses to negative compared with positive faces in clusters comprising the right angular gyrus, supramarginal gyrus, middle temporal gyrus and the lateral occipital cortex (Cohen's d = 0.72–0.77). In patients with schizophrenia, childhood trauma was associated with reporting negative faces as more negative, and positive faces as less positive (Cohen's d > 0.8).

Conclusions

Along with the observed negativity bias in the assessment of emotional valence of faces, our data suggest stronger differentiation in brain responses between negative and positive faces with higher levels of trauma.

Keywords

Childhood maltreatmentface processingsevere mental illness
Type
Original Articles
Information
Psychological Medicine , Volume 47 , Issue 4 , March 2017 , pp. 669 - 679
Copyright
Copyright © Cambridge University Press 2016 

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References

Aas, M, Aminoff, SR, Vik, LT, Etain, B, Agartz, I, Andreassen, OA, Melle, I (2014 a). Affective lability in patients with bipolar disorders is associated with high levels of childhood trauma. Psychiatry Research 15, 252–255.Google Scholar
Aas, M, Dazzan, P, Mondelli, V, Melle, I, Murray, RM, Pariante, CM (2014 b). A systematic review of cognitive function in first-episode psychosis, including a discussion on childhood trauma, stress, and inflammation. Frontiers in Psychiatry 4, 182.CrossRefGoogle Scholar
Aas, M, Steen, NE, Agartz, I, Aminoff, SR, Lorentzen, S, Sundet, K, Andreassen, OA, Melle, I (2012 c). Is cognitive impairment following early life stress in severe mental disorders based on specific or general cognitive functioning? Psychiatry Research 198, 495–500.Google Scholar
Aminoff, SR, Jensen, J, Lagerberg, TV, Andreassen, OA, Melle, I (2011). Decreased self-reported arousal in schizophrenia during aversive picture viewing compared to bipolar disorder and healthy controls. Psychiatry Research 185, 309–314.CrossRefGoogle ScholarPubMed
Berg, AO, Aas, M, Larsson, S, Nerhus, M, Hauff, E, Andreassen, OA, Melle, I (2014). Childhood trauma mediates the association between ethnic minority status and more severe hallucinations in psychotic disorder. Psychological Medicine 45, 133–142.CrossRefGoogle ScholarPubMed
Bernstein, DP, Stein, JA, Newcomb, MD, Walker, E, Pogge, D, Ahluvalia, T, Stokes, J, Handelsman, L, Medrano, M, Desmond, D, Zule, W (2003). Development and validation of a brief screening version of the Childhood Trauma Questionnaire. Child Abuse and Neglect 27, 169–190.CrossRefGoogle ScholarPubMed
Brown, GW, Birley, JL (1968). Crises and life changes and the onset of schizophrenia. Journal of Health and Social Behavior 9, 203–214.CrossRefGoogle ScholarPubMed
Cohen, J (1977). Statistical Power Analysis for the Behavioral Sciences. Academic Press: New York.Google Scholar
Corbalan, F, Beaulieu, S, Armony, JL (2015). Emotion regulation in bipolar disorder type I: an fMRI study. Psycholological Medicine 45, 2521–2531.Google Scholar
Craddock, N, Owen, MJ (2005). The beginning of the end for the Kraepelinian dichotomy. British Journal of Psychiatry 186, 364–366.CrossRefGoogle ScholarPubMed
Etain, B, Aas, M, Andreassen, OA, Lorentzen, S, Dieset, I, Gard, S, Kahn, JP, Bellivier, F, Leboyer, M, Melle, I, Henry, C (2013). Childhood trauma is associated with severe clinical characteristics of bipolar disorders. Journal of Clinical Psychiatry 74, 991–998.Google Scholar
Etain, B, Henry, C, Bellivier, F, Mathieu, F, Leboyer, M (2008). Beyond genetics: childhood affective trauma in bipolar disorder. Bipolar Disorder 10, 867–876.Google Scholar
Etain, B, Lajnef, M, Henrion, A, Dargel, AA, Stertz, L, Kapczinski, F, Mathieu, F, Henry, C, Gard, S, Kahn, JP, Leboyer, M, Jamain, S, Bellivier, F (2015). Interaction between SLC6A4 promoter variants and childhood trauma on the age at onset of bipolar disorders. Scientific Reports 5, 16301.Google Scholar
Fischl, B, Salat, DH, Busa, E, Albert, M, Dieterich, M, Haselgrove, C, van der Kouwe, A, Killiany, R, Kennedy, D, Klaveness, S, Montillo, A, Makris, N, Rosen, B, Dale, AM (2002). Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33, 341–355.Google Scholar
Fisher, HL, Craig, TK, Fearon, P, Morgan, K, Dazzan, P, Lappin, J, Hutchinson, G, Doody, GA, Jones, PB, McGuffin, P, Murray, RM, Leff, J, Morgan, C (2011). Reliability and comparability of psychosis patients’ retrospective reports of childhood abuse. Schizophrenia Bulletin 37, 546–553.Google Scholar
Glaser, JP, van, OJ, Portegijs, PJ, Myin-Germeys, I (2006). Childhood trauma and emotional reactivity to daily life stress in adult frequent attenders of general practitioners. Journal of Psychosomatic Research 61, 229–236.CrossRefGoogle ScholarPubMed
Hariri, AR, Mattay, VS, Tessitore, A, Kolachana, B, Fera, F, Goldman, D, Egan, MF, Weinberger, DR (2002 a). Serotonin transporter genetic variation and the response of the human amygdala. Science 297, 400–403.CrossRefGoogle ScholarPubMed
Hariri, AR, Tessitore, A, Mattay, VS, Fera, F, Weinberger, DR (2002 b). The amygdala response to emotional stimuli: a comparison of faces and scenes. NeuroImage 17, 317–323.Google Scholar
Hart, H, Rubia, K (2012). Neuroimaging of child abuse: a critical review. Frontiers in Human Neuroscience 6, 52.Google Scholar
Heim, CM, Mayberg, HS, Mletzko, T, Nemeroff, CB, Pruessner, JC (2013). Decreased cortical representation of genital somatosensory field after childhood sexual abuse. Americal Journal of Psychiatry 170, 616–623.Google Scholar
Jenkinson, M, Bannister, P, Brady, M, Smith, S (2002). Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage 17, 825–841.Google Scholar
Jenkinson, M, Beckmann, CF, Behrens, TE, Woolrich, MW, Smith, SM (2012). FSL. NeuroImage 62, 782–790.Google Scholar
Kay, SR, Fiszbein, A, Opler, LA (1987). The Positive and Negative Syndrome Scale (PANSS) for schizophrenia. Schizophrenia Bulletin 13, 261–276.CrossRefGoogle ScholarPubMed
Larsson, S, Andreassen, OA, Aas, M, Rossberg, JI, Mork, E, Steen, NE, Barrett, EA, Lagerberg, TV, Peleikis, D, Agartz, I, Melle, I, Lorentzen, S (2013). High prevalence of childhood trauma in patients with schizophrenia spectrum and affective disorder. Comprehensive Psychiatry 54, 123–127.Google Scholar
Linszen, DH, Dingemans, PM, Nugter, MA, van der Does, AJ, Scholte, WF, Lenior, MA (1997). Patient attributes and expressed emotion as risk factors for psychotic relapse. Schizophrenia Bulletin 23, 119–130.CrossRefGoogle ScholarPubMed
Livingstone, K, Harper, S, Gillanders, D (2009). An exploration of emotion regulation in psychosis. Clinical Psychology and Psychotherapy 16, 418–430.Google Scholar
Melle, I, Friis, S, Hauff, E, Island, TK, Lorentzen, S, Vaglum, P (1996). The importance of ward atmosphere in inpatient treatment of schizophrenia on short-term units. Psychiatric Services 47, 721–726.Google Scholar
Myin-Germeys, I, Delespaul, P, van, OJ (2005). Behavioural sensitization to daily life stress in psychosis. Psychological Medicine 35, 733–741.CrossRefGoogle ScholarPubMed
Myin-Germeys, I, van, OJ, Schwartz, JE, Stone, AA, Delespaul, PA (2001). Emotional reactivity to daily life stress in psychosis. Archives of General Psychiatry 58, 1137–1144.Google Scholar
Ousdal, OT, Anand, BA, Jensen, J, Nakstad, PH, Melle, I, Agartz, I, Djurovic, S, Bogdan, R, Hariri, AR, Andreassen, OA (2012). Associations between variants near a monoaminergic pathways gene (PHOX2B) and amygdala reactivity: a genome-wide functional imaging study. Twin Research and Human Genetics 15, 273–285.Google Scholar
Pedersen, G, Hagtvet, KA, Karterud, S (2007). Generalizability studies of the Global Assessment of Functioning-split version. Comprehensive Psychiatry 48, 88–94.CrossRefGoogle ScholarPubMed
Pollak, SD, Sinha, P (2002). Effects of early experience on children's recognition of facial displays of emotion. Developmental Psychology 38, 784–791.CrossRefGoogle ScholarPubMed
Ringen, PA, Lagerberg, TV, Birkenaes, AB, Engn, J, Faerden, A, Jonsdottir, H, Nesvag, R, Friis, S, Opjordsmoen, S, Larsen, F, Melle, I, Andreassen, OA (2008). Differences in prevalence and patterns of substance use in schizophrenia and bipolar disorder. Psychological Medicine 38, 1241–1249.CrossRefGoogle ScholarPubMed
Ringen, PA, Melle, I, Berg, AO, Agartz, I, Spigset, O, Simonsen, C, Sundet, K, Andreassen, OA (2013). Cannabis use and premorbid functioning as predictors of poorer neurocognition in schizophrenia spectrum disorder. Schizophrenia Research 143, 84–89.Google Scholar
Roy, A, Hu, XZ, Janal, MN, Goldman, D (2007). Interaction between childhood trauma and serotonin transporter gene variation in suicide. Neuropsychopharmacology 32, 2046–2052.Google Scholar
Smith, SM (2002). Fast robust automated brain extraction. Human Brain Mapping 17, 143–155.Google Scholar
Smith, SM, Brady, M (1997). SUSAN – a new approach to low level image processing. International Journal of Computer Vision 23, 45–78.CrossRefGoogle Scholar
Smith, SM, Nichols, TE (2009). Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. NeuroImage 44, 83–98.CrossRefGoogle ScholarPubMed
Taylor, SF, Kang, J, Brege, IS, Tso, IF, Hosanagar, A, Johnson, TD (2012). Meta-analysis of functional neuroimaging studies of emotion perception and experience in schizophrenia. Biological Psychiatry 71, 136–145.Google Scholar
Teicher, MH, Anderson, CM, Polcari, A (2012). Childhood maltreatment is associated with reduced volume in the hippocampal subfields CA3, dentate gyrus, and subiculum. Proceedings of the National Academy of Sciences U S A 109, E563–E572.Google Scholar
Teicher, MH, Andersen, SL, Polcari, A, Anderson, CM, Navalta, CP, Kim, DM (2003). The neurobiological consequences of early stress and childhood maltreatment. Neuroscience and Biobehavioral Reviews 27, 33–44.Google Scholar
Teicher, MH, Samson, JA, Polcari, A, McGreenery, CE (2006). Sticks, stones, and hurtful words: relative effects of various forms of childhood maltreatment. American Journal of Psychiatry 163, 993–1000.Google Scholar
Tesli, M, Kauppi, K, Bettella, F, Brandt, CL, Kaufmann, T, Espeseth, T, Mattingsdal, M, Agartz, I, Melle, I, Djurovic, S, Westlye, LT, Andreassen, OA (2015). Altered brain activation during emotional face processing in relation to both diagnosis and polygenic risk of bipolar disorder. PLOS ONE 10, e0134202.CrossRefGoogle ScholarPubMed
Tottenham, N, Tanaka, JW, Leon, AC, McCarry, T, Nurse, M, Hare, TA, Marcus, DJ, Westerlund, A, Casey, BJ, Nelson, C (2009). The NimStim set of facial expressions: judgments from untrained research participants. Psychiatry Research 168, 242–249.Google Scholar
van Harmelen, AL, van Tol, MJ, Demenescu, LR, van der Wee, NJ, Veltman, DJ, Aleman, A, van Buchem, MA, Spinhoven, P, Penninx, BW, Elzinga, BM (2013). Enhanced amygdala reactivity to emotional faces in adults reporting childhood emotional maltreatment. Social Cognitive and Affective Neuroscience 8, 362–369.Google Scholar
Varese, F, Smeets, F, Drukker, M, Lieverse, R, Lataster, T, Viechtbauer, W, Read, J, van, Os J, Bentall, RP (2012). Childhood adversities increase the risk of psychosis: a meta-analysis of patient–control, prospective- and cross-sectional cohort studies. Schizophrenia Bulletin 38, 661–671.CrossRefGoogle ScholarPubMed
Winkler, AM, Ridgway, GR, Webster, MA, Smith, SM, Nichols, TE (2014). Permutation inference for the general linear model. NeuroImage 92, 381–397.Google Scholar
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