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Investigating patterns of neural response associated with childhood abuse v. childhood neglect

Published online by Cambridge University Press:  13 June 2019

Vanessa Bianca Puetz Open the ORCID record for Vanessa Bianca Puetz [Opens in a new window] ,
Essi Viding ,
Mattia Indi Gerin ,
Jean-Baptiste Pingault ,
Arjun Sethi ,
Annchen R. Knodt ,
Spenser R. Radtke ,
Bart D. Brigidi ,
Ahmad R. Hariri  and
Eamon McCrory
Vanessa Bianca Puetz*
Affiliation:
Division of Psychology and Language Sciences, University College London, 26 Bedford Way, WC1H 0AP, London, UK Anna Freud National Centre for Children and Families, Kantor Centre of Excellence, 4-8 Rodney Street, LondonN1 9JH, UK
Essi Viding
Affiliation:
Division of Psychology and Language Sciences, University College London, 26 Bedford Way, WC1H 0AP, London, UK
Mattia Indi Gerin
Affiliation:
Division of Psychology and Language Sciences, University College London, 26 Bedford Way, WC1H 0AP, London, UK
Jean-Baptiste Pingault
Affiliation:
Division of Psychology and Language Sciences, University College London, 26 Bedford Way, WC1H 0AP, London, UK
Arjun Sethi
Affiliation:
Division of Psychology and Language Sciences, University College London, 26 Bedford Way, WC1H 0AP, London, UK
Annchen R. Knodt
Affiliation:
Department of Psychology and Neuroscience, Laboratory of NeuroGenetics, Duke University, Durham, NC27708, USA
Spenser R. Radtke
Affiliation:
Department of Psychology and Neuroscience, Laboratory of NeuroGenetics, Duke University, Durham, NC27708, USA
Bart D. Brigidi
Affiliation:
Department of Psychology and Neuroscience, Laboratory of NeuroGenetics, Duke University, Durham, NC27708, USA
Ahmad R. Hariri
Affiliation:
Department of Psychology and Neuroscience, Laboratory of NeuroGenetics, Duke University, Durham, NC27708, USA
Eamon McCrory
Affiliation:
Division of Psychology and Language Sciences, University College London, 26 Bedford Way, WC1H 0AP, London, UK Anna Freud National Centre for Children and Families, Kantor Centre of Excellence, 4-8 Rodney Street, LondonN1 9JH, UK
*
Author for correspondence: Vanessa Bianca Puetz, E-mail: [email protected]
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Abstract

Background

Childhood maltreatment is robustly associated with increased risk of poor mental health outcome and changes in brain function. The authors investigated whether childhood experience of abuse (e.g. physical, emotional and sexual abuse) and neglect (physical and emotional deprivation) was differentially associated with neural reactivity to threat.

Methods

Participants were drawn from an existing study and allocated to one of four groups based on self-report of childhood maltreatment experience: individuals with childhood abuse experiences (n = 70); individuals with childhood neglect experiences (n = 87); individuals with combined experience of childhood abuse and neglect (n = 50); and non-maltreated individuals (n = 207) propensity score matched (PSM) on gender, age, IQ, psychopathology and SES. Neural reactivity to facial cues signalling threat was compared across groups, allowing the differential effects associated with particular forms of maltreatment experience to be isolated.

Results

Brain imaging analyses indicated that while childhood abuse was associated with heightened localised threat reactivity in ventral amygdala, experiences of neglect were associated with heightened reactivity in a distributed cortical fronto-parietal network supporting complex social and cognitive processing as well as in the dorsal amygdala. Unexpectedly, combined experiences of abuse and neglect were associated with hypo-activation in several higher-order cortical regions as well as the amygdala.

Conclusions

Different forms of childhood maltreatment exert differential effects in neural threat reactivity: while the effects of abuse are more focal, the effects of neglect and combined experiences of abuse are more distributed. These findings are relevant for understanding the range of psychiatric outcomes following childhood maltreatment and have implications for intervention.

Keywords

Abuseamygdalaface processingfMRImaltreatmentneglect
Type
Original Articles
Information
Psychological Medicine , Volume 50 , Issue 8 , June 2020 , pp. 1398 - 1407
Copyright
Copyright © Cambridge University Press 2019

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References

Bernstein, DP and Fink, L (1998) CTQ Childhood Trauma Questionnaire: A Retrospective Self-Report. Manual. San Antonio, TX: The Psychological Corporation.Google Scholar
Bos, KJ, Fox, N, Zeanah, CH and Nelson, CA (2009) Effects of early psychosocial deprivation on the development of memory and executive function. Frontiers in Behavioral Neuroscience 3, 1–7.CrossRefGoogle ScholarPubMed
Buhle, JT, Silvers, JA, Wager, TD, Lopez, R, Onyemekwu, C, Kober, H, Weber, J and Ochsner, KN (2014) Cognitive reappraisal of emotion: a meta-analysis of human neuroimaging studies. Cerebral Cortex 24, 2981–2990.CrossRefGoogle ScholarPubMed
Carré, JM, Fisher, PM, Manuck, SB and Hariri, AR (2012) Interaction between trait anxiety and trait anger predict amygdala reactivity to angry facial expressions in men but not women. Social Cognitive and Affective Neuroscience 7, 213–221.CrossRefGoogle Scholar
Carré, JM, Hyde, LW, Neumann, CS, Viding, E and Hariri, AR (2013) The neural signatures of distinct psychopathic traits. Social Neuroscience 8, 122–135.10.1080/17470919.2012.703623CrossRefGoogle ScholarPubMed
Chechko, N, Augustin, M, Zvyagintsev, M, Schneider, F, Habel, U and Kellermann, T (2013) Brain circuitries involved in emotional interference task in major depression disorder. Journal of Affective Disorders 149, 136–145.CrossRefGoogle ScholarPubMed
Cicchetti, D and Rogosch, FA (2001) The impact of child maltreatment and psychopathology on neuroendocrine functioning. Development and Psychopathology 13, 783–804.CrossRefGoogle ScholarPubMed
Corbetta, M, Kincade, JM, Ollinger, JM, McAvoy, MP and Shulman, GL (2000) Voluntary orienting is dissociated from target detection in human posteriorparietal cortex. Nature Neuroscience 3, 292–297.CrossRefGoogle ScholarPubMed
Dannlowski, U, Stuhrmann, A, Beutelmann, V, Zwanzger, P, Lenzen, T, Grotegerd, D, Domschke, K, Hohoff, C, Ohrmann, P, Bauer, J, Lindner, C, Postert, C, Konrad, C, Arolt, V, Heindel, W, Suslow, T and Kugel, H (2012) Limbic scars: long-term consequences of childhood maltreatment revealed by functional and structural magnetic resonance imaging. Biological Psychiatry 71, 286–293.10.1016/j.biopsych.2011.10.021CrossRefGoogle ScholarPubMed
Davis, M and Whalen, PJ (2001) The amygdala: vigilance and emotion. Molecular Psychiatry 6, 13–34.10.1038/sj.mp.4000812CrossRefGoogle ScholarPubMed
Ekman, P and Friesen, WV (1976) Measuring facial movement. Environmental Psychology and Nonverbal Behavior 1, 56–75.CrossRefGoogle Scholar
Etkin, A, Klemenhagen, KC, Dudman, JT, Rogan, MT, Hen, R, Kandel, ER and Hirsch, J (2004) Individual differences in trait anxiety predict the response of the basolateral amygdala to unconsciously processed fearful faces. Neuron 44, 1043–1055.CrossRefGoogle ScholarPubMed
Gunnar, MR and Donzella, B (2001) Social regulation of the cortisol levels in early human development. Development and Psychopathology 13, 611–628.CrossRefGoogle Scholar
Hariri, AR, Mattay, VS, Tessitore, A, Kolachana, B, Fera, F, Goldman, D, Egan, MF and Weinberger, DR (2002) Serotonin transporter genetic variation and the response of the human amygdala. Science (New York, N.Y.) 297, 400–403.CrossRefGoogle ScholarPubMed
Hariri, AR, Drabant, EM, Munoz, KE, Kolachana, BS, Mattay, VS, Egan, MF and Weinberger, DR (2005) A susceptibility gene for affective disorders and the response of the human amygdala. Archives of General Psychiatry 62, 146.CrossRefGoogle ScholarPubMed
Hebb, DO (1949) The Organization of Behavior. New York: Wiley.Google Scholar
Ho, DE, Imai, K, King, G and Stuart, EA (2011) Matchit: nonparametric preprocessing for parametric causal inference. JSS Journal of Statistical Software 42.Google Scholar
Hyde, LW, Gorka, A, Manuck, SB and Hariri, AR (2011) Perceived social support moderates the link between threat-related amygdala reactivity and trait anxiety. Neuropsychologia 49, 651–656.CrossRefGoogle ScholarPubMed
Kanwisher, N, McDermott, J and Chun, MM (1997) The fusiform face area: a module in human extrastriate cortex specialized for face perception. Journal of Neuroscience 17, 4302–4311.CrossRefGoogle ScholarPubMed
Kolb, B, Mychasiuk, R, Muhammad, A, Li, Y, Frost, DO and Gibb, R (2012) Experience and the developing prefrontal cortex. Proceedings of the National Academy of Sciences of the United States of America 109(suppl), 17186–17193.CrossRefGoogle ScholarPubMed
Lanius, RA, Bluhm, R, Lanius, U and Pain, C (2006) A review of neuroimaging studies in PTSD: heterogeneity of response to symptom provocation. Journal of Psychiatric Research 40, 709–729.CrossRefGoogle ScholarPubMed
Manuck, SB, Marsland, AL, Flory, JD, Gorka, A, Ferrell, RE and Hariri, AR (2010) Salivary testosterone and a trinucleotide (CAG) length polymorphism in the androgen receptor gene predict amygdala reactivity in men. Psychoneuroendocrinology 35, 92–104.CrossRefGoogle Scholar
McCrory, EJ and Viding, E (2015) The theory of latent vulnerability: reconceptualizing the link between childhood maltreatment and psychiatric disorder. Development and Psychopathology 27, 493–505.CrossRefGoogle ScholarPubMed
McCrory, EJ, De Brito, SA, Sebastian, CL, Mechelli, A, Bird, G, Kelly, PA and Viding, E (2011) Heightened neural reactivity to threat in child victims of family violence. Current Biology: CB 21, R947–R948.CrossRefGoogle ScholarPubMed
McCrory, EJ, De Brito, SA, Kelly, PA, Bird, G, Sebastian, CL, Mechelli, A, Samuel, S and Viding, E (2013) Amygdala activation in maltreated children during pre-attentive emotional processing. The British Journal of Psychiatry: the Journal of Mental Science 202, 269–276.CrossRefGoogle ScholarPubMed
McCrory, EJ, Gerin, MI and Viding, E (2017 a) Annual Research Review: childhood maltreatment, latent vulnerability and the shift to preventative psychiatry - the contribution of functional brain imaging. Journal of Child Psychology and Psychiatry 58, 338–357.CrossRefGoogle ScholarPubMed
McCrory, EJ, Puetz, VB, Maguire, EA, Mechelli, A, Palmer, A, Gerin, MI, Kelly, PA, Koutoufa, I and Viding, E (2017 b) Autobiographical memory: a candidate latent vulnerability mechanism for psychiatric disorder following childhood maltreatment. The British Journal of Psychiatry: the Journal of Mental Science 211, 216–222.CrossRefGoogle ScholarPubMed
McEwen, BS (1998) Stress, adaptation, and disease. Allostasis and allostatic load. Annals of the New York Academy of Sciences 840, 33–44.CrossRefGoogle ScholarPubMed
McEwen, BS (2013) Brain on stress: how the social environment gets under the skin. Proceedings of the National Academy of Sciences of the United States of America 110, 17180–17185.Google Scholar
McLaughlin, KA, Sheridan, MA and Lambert, HK (2014) Childhood adversity and neural development: deprivation and threat as distinct dimensions of early experience. Neuroscience and Biobehavioral Reviews 47, 578–591.CrossRefGoogle ScholarPubMed
McLaughlin, KA, Sheridan, MA, Tibu, F, Fox, NA, Zeanah, CH and Nelson, CA (2015) Causal effects of the early caregiving environment on development of stress response systems in children. Proceedings of the National Academy of Sciences of the United States of America 112, 5637–5642.CrossRefGoogle ScholarPubMed
McLaughlin, KA, Sheridan, MA and Nelson, CA (2016) Neglect as a violation of species-expectant experience: neurodevelopmental consequences. Biological Psychiatry 82, 462–471.CrossRefGoogle Scholar
Newbury, JB, Arseneault, L, Moffitt, TE, Caspi, A, Danese, A, Baldwin, JR, Fisher, HL and Fisher, HL (2018) Measuring childhood maltreatment to predict early-adult psychopathology: comparison of prospective informant-reports and retrospective self-reports. Journal of Psychiatric Research 96, 57–64.CrossRefGoogle ScholarPubMed
O'Kusky, JR (1985) Synapse elimination in the developing visual cortex: a morphometric analysis in normal and dark-reared cats. Developmental Brain Research 22, 81–91.CrossRefGoogle Scholar
Pollak, SD and Tolley-Schell, SA (2003) Selective attention to facial emotion in physically abused children. Journal of Abnormal Psychology 112, 323–338.CrossRefGoogle ScholarPubMed
Puetz, VB, Kohn, N, Dahmen, B, Zvyagintsev, M, Schüppen, A, Schultz, RT, Heim, CM, Fink, GR, Herpertz-Dahlmann, B and Konrad, K (2014) Neural response to social rejection in children with early separation experiences. Journal of the American Academy of Child & Adolescent Psychiatry 53, 1328–1337, e8.CrossRefGoogle ScholarPubMed
Puetz, VB, Viding, E, Palmer, A, Kelly, PA, Lickley, R, Koutoufa, I, Sebastian, CL and McCrory, EJ (2016a) Altered neural response to rejection-related words in children exposed to maltreatment. Journal of Child Psychology and Psychiatry 57, 1165–1173.10.1111/jcpp.12595CrossRefGoogle Scholar
Puetz, VB, Zweerings, J, Dahmen, B, Ruf, C, Scharke, W, Herpertz-Dahlmann, B and Konrad, K (2016b) Multidimensional assessment of neuroendocrine and psychopathological profiles in maltreated youth. Journal of Neural Transmission 123, 1095–1106.CrossRefGoogle Scholar
Puetz, VB, Parker, D, Kohn, N, Dahmen, B, Verma, R and Konrad, K (2017) Altered brain network integrity after childhood maltreatment: a structural connectomic DTI-study. Human Brain Mapping 38, 855–868.CrossRefGoogle ScholarPubMed
Sheridan, MA and McLaughlin, KA (2014) Dimensions of early experience and neural development: deprivation and threat. Trends in Cognitive Sciences 18, 1–6.CrossRefGoogle ScholarPubMed
Tottenham, N, Hare, TA, Millner, A, Gilhooly, T, Zevin, JD and Casey, BJ (2011) Elevated amygdala response to faces following early deprivation. Developmental Science 14, 190–204.CrossRefGoogle ScholarPubMed
van der Vegt, EJM, van der Ende, J, Kirschbaum, C, Verhulst, FC and Tiemeier, H (2009) Early neglect and abuse predict diurnal cortisol patterns in adults A study of international adoptees. Psychoneuroendocrinology 34, 660–669.10.1016/j.psyneuen.2008.11.004CrossRefGoogle ScholarPubMed
White, MG, Bogdan, R, Fisher, PM, Muñoz, KE, Williamson, DE and Hariri, AR (2012) FKBP5 and emotional neglect interact to predict individual differences in amygdala reactivity. Genes, Brain and Behavior 11, 869–878.CrossRefGoogle ScholarPubMed
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