Skip to main content Accessibility help
×
Home

Altered fear processing in adolescents with a history of severe childhood maltreatment: an fMRI study

  • H. Hart (a1), L. Lim (a1), M. A. Mehta (a2), A. Simmons (a3), K. A. H. Mirza (a4) and K. Rubia (a1)...

Abstract

Background

Children with a history of maltreatment suffer from altered emotion processing but the neural basis of this phenomenon is unknown. This pioneering functional magnetic resonance imaging (fMRI) study investigated the effects of severe childhood maltreatment on emotion processing while controlling for psychiatric conditions, medication and substance abuse.

Method

Twenty medication-naive, substance abuse-free adolescents with a history of childhood abuse, 20 psychiatric control adolescents matched on psychiatric diagnoses but with no maltreatment and 27 healthy controls underwent a fMRI emotion discrimination task comprising fearful, angry, sad happy and neutral dynamic facial expressions.

Results

Maltreated participants responded faster to fearful expressions and demonstrated hyper-activation compared to healthy controls of classical fear-processing regions of ventromedial prefrontal cortex (vmPFC) and anterior cingulate cortex, which survived at a more lenient threshold relative to psychiatric controls. Functional connectivity analysis, furthermore, demonstrated reduced connectivity between left vmPFC and insula for fear in maltreated participants compared to both healthy and psychiatric controls.

Conclusions

The findings show that people who have experienced childhood maltreatment have enhanced fear perception, both at the behavioural and neurofunctional levels, associated with enhanced fear-related ventromedial fronto-cingulate activation and altered functional connectivity with associated limbic regions. Furthermore, the connectivity adaptations were specific to the maltreatment rather than to the developing psychiatric conditions, whilst the functional changes were only evident at trend level when compared to psychiatric controls, suggesting a continuum. The neurofunctional hypersensitivity of fear-processing networks may be due to childhood over-exposure to fear in people who have been abused.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Altered fear processing in adolescents with a history of severe childhood maltreatment: an fMRI study
      Available formats
      ×

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Altered fear processing in adolescents with a history of severe childhood maltreatment: an fMRI study
      Available formats
      ×

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Altered fear processing in adolescents with a history of severe childhood maltreatment: an fMRI study
      Available formats
      ×

Copyright

This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.

Corresponding author

Author for correspondence: Dr H. Hart, E-mail: heledd.hart@kcl.ac.uk

Footnotes

Hide All
*

These authors contributed equally as joint first authors.

Footnotes

References

Hide All
Ackerman, PT, Newton, JE, McPherson, WB, Jones, JG and Dykman, RA (1998) Prevalence of post-traumatic stress disorder and other psychiatric diagnoses in three groups of abused children (sexual, physical, and both). Child Abuse & Neglect 22, 759774.
Amaral, DG, Price, JL, Pitkanen, A and Carmichael, ST (1992) Anatomical organization of the primate amygdaloid complex. The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction 166.
Bernstein, D and Fink, L (1998) Childhood Trauma Questionnaire: A Retrospective Self-Report. Manual. San Antonio, TX: The Psychological Cooperation.
Bifulco, A, Brown, GW and Harris, TO (1994) Childhood Experience of Care and Abuse (CECA): a retrospective interview measure. Journal of Child Psychology and Psychiatry 35, 14191435.
Brown, J, Cohen, P, Johnson, JG and Salzinger, S (1998) A longitudinal analysis of risk factors for child maltreatment: findings of a 17-year prospective study of officially recorded and self-reported child abuse and neglect. Child Abuse & Neglect 22, 10651078.
Bugental, DB, Blue, J and Lewis, J (1990) Caregiver beliefs and dysphoric affect directed to difficult children. Developmental Psychology 26, 631.
Carrey, NJ, Butter, HJ, Persinger, MA and Bialik, RJ (1995) Physiological and cognitive correlates of child abuse. Journal of the American Academy of Child & Adolescent Psychiatry 34, 10671075.
Choi, J, Jeong, B, Rohan, ML, Polcari, AM and Teicher, MH (2009) Preliminary evidence for white matter tract abnormalities in young adults exposed to parental verbal abuse. Biological Psychiatry 65, 227234.
Cicchetti, D and Curtis, W (2005) An event-related potential study of the processing of affective facial expressions in young children who experienced maltreatment during the first year of life. Development and Psychopathology 17, 641677.
Cooke, BM and Weathington, JM (2014) Human and animal research into sex-specific effects of child abuse. Hormones and Behavior 65, 416426.
Cooney, RE, Atlas, LY, Joormann, J, Eugène, F and Gotlib, IH (2006) Amygdala activation in the processing of neutral faces in social anxiety disorder: is neutral really neutral? Psychiatry Research: Neuroimaging 148, 5559.
Currie, C, Molcho, M, Boyce, W, Holstein, B, Torsheim, T and Richter, M (2008) Researching health inequalities in adolescents: the development of the Health Behaviour in School-Aged Children (HBSC) Family Affluence Scale. Social Science & Medicine 66, 14291436.
Dannlowski, U, Kugel, H, Huber, F, Stuhrmann, A, Redlich, R, Grotegerd, D et al. (2013) Childhood maltreatment is associated with an automatic negative emotion processing bias in the amygdala. Human Brain Mapping 34, 28992909.
Dannlowski, U, Stuhrmann, A, Beutelmann, V, Zwanzger, P, Lenzen, T, Grotegerd, D et al. (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.
De Bellis, MD, Hooper, SR, Spratt, EG and Woolley, DP (2009) Neuropsychological findings in childhood neglect and their relationships to pediatric PTSD. Journal of the International Neuropsychological Society 15, 868878.
de Graaf-Peters, VB and Hadders-Algra, M (2006) Ontogeny of the human central nervous system: what is happening when? Early Human Development 82, 257266.
Dennis, M, Francis, DJ, Cirino, PT, Schachar, R, Barnes, MA and Fletcher, JM (2009) Why IQ is not a covariate in cognitive studies of neurodevelopmental disorders. Journal of the International Neuropsychological Society 15, 331343.
Edmiston, EK and Blackford, JU (2013) Childhood maltreatment and response to novel face stimuli presented during functional magnetic resonance imaging in adults. Psychiatry Research: Neuroimaging 212, 3642.
Edwards, VJ, Holden, GW, Felitti, VJ and Anda, RF (2003) Relationship between multiple forms of childhood maltreatment and adult mental health in community respondents: results from the adverse childhood experiences study. American Journal of Psychiatry 160, 14531460.
Eluvathingal, TJ, Chugani, HT, Behen, ME, Juhasz, C, Muzik, O, Maqbool, M et al. (2006) Abnormal brain connectivity in children after early severe socioemotional deprivation: a diffusion tensor imaging study. Pediatrics 117, 20932100.
Etkin, A, Egner, T and Kalisch, R (2011) Emotional processing in anterior cingulate and medial prefrontal cortex. Trends in Cognitive Sciences 15, 8593.
Fonzo, GA, Flagan, TM, Sullivan, S, Allard, CB, Grimes, EM, Simmons, AN et al. (2013) Neural functional and structural correlates of childhood maltreatment in women with intimate-partner violence-related posttraumatic stress disorder. Psychiatry Research: Neuroimaging 211, 93103.
Forman, SD, Cohen, JD, Fitzgerald, M, Eddy, WF, Mintun, MA and Noll, DC (1995) Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster size threshold. Magnetic Resonance in Medicine 33, 636647.
Fornari, RV, Wichmann, R, Atucha, E, Desprez, T, Eggens-Meijer, E and Roozendaal, B (2012) Involvement of the insular cortex in regulating glucocorticoid effects on memory consolidation of inhibitory avoidance training. Memory and Motivational/Emotional Processes 119129.
Fries, AW and Pollak, SD (2004) Emotion understanding in postinstitutionalized Eastern European children. Development and Psychopathology 16, 355370.
Friston, KJ, Rotshtein, P, Geng, JJ, Sterzer, P and Henson, RN (2006) A critique of functional localisers. Neuroimage 30, 10771087.
Ghashghaei, H, Hilgetag, C and Barbas, H (2007) Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala. Neuroimage 34, 905923.
Goodman, R, Ford, T, Richards, H, Gatward, R and Meltzer, H (2000) The development and well-being assessment: description and initial validation of an integrated assessment of child and adolescent psychopathology. Journal of Child Psychology and Psychiatry 41, 645655.
Hansel, A and von Kanel, R (2008) The ventro-medial prefrontal cortex: a major link between the autonomic nervous system, regulation of emotion, and stress reactivity? BioPsychoSocial Medicine 2, 21.
Hart, H and Rubia, K (2012) Neuroimaging of child abuse: a critical review. Frontiers in Human Neuroscience 6, Article 52, pp. 124.
Heim, CM, Mayberg, HS, Mletzko, T, Nemeroff, CB and Pruessner, JC (2013) Decreased cortical representation of genital somatosensory field after childhood sexual abuse. American Journal of Psychiatry 170, 616623.
Herrenkohl, RC, Herrenkohl, EC, Egolf, BP, Wu, P (1991). The developmental consequences of child abuse: the lehigh longitudinal study. The Effects of Child Abuse and Neglect: Issues and Research 57, 81.
Lebel, C, Walker, L, Leemans, A, Phillips, L and Beaulieu, C (2008) Microstructural maturation of the human brain from childhood to adulthood. Neuroimage 40, 10441055.
Lim, L, Radua, J and Rubia, K (2014) Gray matter abnormalities in childhood maltreatment: a voxel-wise meta-analysis. American Journal of Psychiatry 171, 854863.
Lupien, SJ, McEwen, BS, Gunnar, MR and Heim, C (2009) Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nature Reviews Neuroscience 10, 434445.
Maheu, FS, Dozier, M, Guyer, AE, Mandell, D, Peloso, E, Poeth, K et al. (2010) A preliminary study of medial temporal lobe function in youths with a history of caregiver deprivation and emotional neglect. Cognitive, Affective, & Behavioral Neuroscience 10, 3449.
Maniglio, R, Gusciglio, F, Lofrese, V, Murri, MB, Tamburello, A and Innamorati, M (2014) Biased processing of neutral facial expressions is associated with depressive symptoms and suicide ideation in individuals at risk for major depression due to affective temperaments. Comprehensive Psychiatry 55, 518525.
Marsh, R, Gerber, AJ and Peterson, BS (2008) Neuroimaging studies of normal brain development and their relevance for understanding childhood neuropsychiatric disorders. Journal of the American Academy of Child & Adolescent Psychiatry 47, 12331251.
McCrory, E, De Brito, SA and Viding, E (2011) The impact of childhood maltreatment: a review of neurobiological and genetic factors. Frontiers in Psychiatry 2, 48.
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. British Journal of Psychiatry 202, 269276.
Milad, MR, Quirk, GJ, Pitman, RK, Orr, SP, Fischl, B and Rauch, SL (2007) A role for the human dorsal anterior cingulate cortex in fear expression. Biological Psychiatry 62, 11911194.
Miller, G and Chapman, J (2001) Misunderstanding analysis of covariance. Journal of Abnormal Psychology 110, 4048.
Morris, JS, Scott, SK and Dolan, RJ (1999) Saying it with feeling: neural responses to emotional vocalizations. Neuropsychologia 37, 11551163.
Mullen, PE, Martin, JL, Anderson, JC, Romans, SE and Herbison, GP (1996) The long-term impact of the physical, emotional, and sexual abuse of children: a community study. Child Abuse & Neglect 20, 721.
Ney, PG, Fung, T and Wickett, AR (1994) The worst combinations of child abuse and neglect. Child Abuse & Neglect 18, 705714.
Ochsner, KN and Gross, JJ (2005) The cognitive control of emotion. Trends in Cognitive Sciences 9, 242249.
Oliveira, L, Ladouceur, CD, Phillips, ML, Brammer, M and Mourao-Miranda, J (2013) What does brain response to neutral faces tell us about major depression? Evidence from machine learning and fMRI. PLoS ONE 8, e60121.
Parker, SW and Nelson, CA (2005) The impact of early institutional rearing on the ability to discriminate facial expressions of emotion: an event-related potential study. Child Development 76, 5472.
Phelps, EA, Delgado, MR, Nearing, KI and LeDoux, JE (2004) Extinction learning in humans: role of the amygdala and vmPFC. Neuron 43, 897905.
Phelps, EA, O'Connor, KJ, Gatenby, JC, Gore, JC, Grillon, C and Davis, M (2001) Activation of the left amygdala to a cognitive representation of fear. Nature Neuroscience 4, 437441.
Pine, DS, Mogg, K, Bradley, BP, Montgomery, L, Monk, CS, McClure, E et al. (2005) Attention bias to threat in maltreated children: implications for vulnerability to stress-related psychopathology. American Journal of Psychiatry 162, 291296.
Pollak, SD, Cicchetti, D, Hornung, K and Reed, A (2000) Recognizing emotion in faces: developmental effects of child abuse and neglect. Developmental Psychology 36, 679688.
Pollak, SD, Klorman, R, Thatcher, JE and Cicchetti, D (2001) P3b reflects maltreated children's reactions to facial displays of emotion. Psychophysiology 38, 267274.
Pollak, SD and Sinha, P (2002) Effects of early experience on children's recognition of facial displays of emotion. Developmental Psychology 38, 784791.
Pollak, SD and Tolley-Schell, SA (2003) Selective attention to facial emotion in physically abused children. Journal of Abnormal Psychology 112, 323338.
Radford, L, Corral, S, Bradley, C and Fisher, HL (2013) The prevalence and impact of child maltreatment and other types of victimization in the UK: findings from a population survey of caregivers, children and young people and young adults. Child Abuse & Neglect 37, 801813.
Rubia, K, Lim, L, Ecker, C, Halari, R, Giampietro, V, Simmons, A et al. (2013) Effects of age and gender on neural networks of motor response inhibition: from adolescence to mid-adulthood. Neuroimage 83, 690703.
Schienle, A, Stark, R, Walter, B, Blecker, C, Ott, U, Kirsch, P et al. (2002) The insula is not specifically involved in disgust processing: an fMRI study. Neuroreport 13, 20232026.
Sehlmeyer, C, Schoning, S, Zwitserlood, P, Pfleiderer, B, Kircher, T, Arolt, V et al. (2009) Human fear conditioning and extinction in neuroimaging: a systematic review. PLoS ONE 4, e5865.
Shackman, JE, Shackman, AJ and Pollak, SD (2007) Physical abuse amplifies attention to threat and increases anxiety in children. Emotion 7, 838.
Simon, D, Craig, KD, Gosselin, F, Belin, P and Rainville, P (2008) Recognition and discrimination of prototypical dynamic expressions of pain and emotions. Pain 135, 5564.
Sowell, ER, Peterson, BS, Thompson, PM, Welcome, SE, Henkenius, AL and Toga, AW (2003) Mapping cortical change across the human life span. Nature Neuroscience 6, 309315.
Taylor, SE, Eisenberger, NI, Saxbe, D, Lehman, BJ and Lieberman, MD (2006) Neural responses to emotional stimuli are associated with childhood family stress. Biological Psychiatry 60, 296301.
Teicher, MH, Andersen, SL, Polcari, A, Anderson, CM, Navalta, CP and Kim, DM (2003) The neurobiological consequences of early stress and childhood maltreatment. Neuroscience & Biobehavioral Reviews 27, 3344.
Tottenham, N, Hare, T, Millner, A, Gilhooly, T, Zevin, J and Casey, B (2011) Elevated amygdala response to faces following early deprivation. Developmental Science 14, 190204.
Trickett, PK, Kim, K and Prindle, J (2011) Variations in emotional abuse experiences among multiply maltreated young adolescents and relations with developmental outcomes. Child Abuse & Neglect 35, 876886.
Trickett, PK and McBride-Chang, C (1995) The developmental impact of different forms of child abuse and neglect. Developmental Review 15, 311337.
Velanova, K, Wheeler, ME and Luna, B (2008) Maturational changes in anterior cingulate and frontoparietal recruitment support the development of error processing and inhibitory control. Cerebral Cortex, 18, 25052522.
Vorria, P, Papaligoura, Z, Sarafidou, J, Kopakaki, M, Dunn, J, Van IJzendoorn, MH et al. (2006) The development of adopted children after institutional care: a follow-up study. Journal of Child Psychology and Psychiatry 47, 12461253.
Wechsler, D (1999) Wechsler Abbreviated Scale of Intelligence. San Antonio, Texas: The Psychological Corporation.

Keywords

Type Description Title
WORD
Supplementary materials

Hart et al. supplementary material
Hart et al. supplementary material 1

 Word (7.8 MB)
7.8 MB

Altered fear processing in adolescents with a history of severe childhood maltreatment: an fMRI study

  • H. Hart (a1), L. Lim (a1), M. A. Mehta (a2), A. Simmons (a3), K. A. H. Mirza (a4) and K. Rubia (a1)...

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed