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

  • Vanessa Bianca Puetz (a1) (a2), Essi Viding (a1), Mattia Indi Gerin (a1), Jean-Baptiste Pingault (a1), Arjun Sethi (a1), Annchen R. Knodt (a3), Spenser R. Radtke (a3), Bart D. Brigidi (a3), Ahmad R. Hariri (a3) and Eamon McCrory (a1) (a2)...
  • Please note a correction has been issued for this article.

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.

Copyright

Corresponding author

Author for correspondence: Vanessa Bianca Puetz, E-mail: v.puetz@ucl.ac.uk

References

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Bernstein, DP and Fink, L (1998) CTQ Childhood Trauma Questionnaire: A Retrospective Self-Report. Manual. San Antonio, TX: The Psychological Corporation.
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, 17.
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, 29812990.
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, 213221.
Carré, JM, Hyde, LW, Neumann, CS, Viding, E and Hariri, AR (2013) The neural signatures of distinct psychopathic traits. Social Neuroscience 8, 122135.
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, 136145.
Cicchetti, D and Rogosch, FA (2001) The impact of child maltreatment and psychopathology on neuroendocrine functioning. Development and Psychopathology 13, 783804.
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, 292297.
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, 286293.
Davis, M and Whalen, PJ (2001) The amygdala: vigilance and emotion. Molecular Psychiatry 6, 1334.
Ekman, P and Friesen, WV (1976) Measuring facial movement. Environmental Psychology and Nonverbal Behavior 1, 5675.
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, 10431055.
Gunnar, MR and Donzella, B (2001) Social regulation of the cortisol levels in early human development. Development and Psychopathology 13, 611628.
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, 400403.
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.
Hebb, DO (1949) The Organization of Behavior. New York: Wiley.
Ho, DE, Imai, K, King, G and Stuart, EA (2011) Matchit: nonparametric preprocessing for parametric causal inference. JSS Journal of Statistical Software 42.
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, 651656.
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, 43024311.
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), 1718617193.
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, 709729.
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, 92104.
McCrory, EJ and Viding, E (2015) The theory of latent vulnerability: reconceptualizing the link between childhood maltreatment and psychiatric disorder. Development and Psychopathology 27, 493505.
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, R947R948.
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, 269276.
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, 338357.
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, 216222.
McEwen, BS (1998) Stress, adaptation, and disease. Allostasis and allostatic load. Annals of the New York Academy of Sciences 840, 3344.
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, 1718017185.
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, 578591.
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, 56375642.
McLaughlin, KA, Sheridan, MA and Nelson, CA (2016) Neglect as a violation of species-expectant experience: neurodevelopmental consequences. Biological Psychiatry 82, 462471.
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, 5764.
O'Kusky, JR (1985) Synapse elimination in the developing visual cortex: a morphometric analysis in normal and dark-reared cats. Developmental Brain Research 22, 8191.
Pollak, SD and Tolley-Schell, SA (2003) Selective attention to facial emotion in physically abused children. Journal of Abnormal Psychology 112, 323338.
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, 13281337, e8.
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, 11651173.
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, 10951106.
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, 855868.
Sheridan, MA and McLaughlin, KA (2014) Dimensions of early experience and neural development: deprivation and threat. Trends in Cognitive Sciences 18, 16.
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, 190204.
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, 660669.
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, 869878.

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