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

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          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.

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          Most cited references44

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          Emotional processing in anterior cingulate and medial prefrontal cortex.

          Negative emotional stimuli activate a broad network of brain regions, including the medial prefrontal (mPFC) and anterior cingulate (ACC) cortices. An early influential view dichotomized these regions into dorsal-caudal cognitive and ventral-rostral affective subdivisions. In this review, we examine a wealth of recent research on negative emotions in animals and humans, using the example of fear or anxiety, and conclude that, contrary to the traditional dichotomy, both subdivisions make key contributions to emotional processing. Specifically, dorsal-caudal regions of the ACC and mPFC are involved in appraisal and expression of negative emotion, whereas ventral-rostral portions of the ACC and mPFC have a regulatory role with respect to limbic regions involved in generating emotional responses. Moreover, this new framework is broadly consistent with emerging data on other negative and positive emotions. Published by Elsevier Ltd.
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            Microstructural maturation of the human brain from childhood to adulthood.

            Brain maturation is a complex process that continues well beyond infancy, and adolescence is thought to be a key period of brain rewiring. To assess structural brain maturation from childhood to adulthood, we charted brain development in subjects aged 5 to 30 years using diffusion tensor magnetic resonance imaging, a novel brain imaging technique that is sensitive to axonal packing and myelination and is particularly adept at virtually extracting white matter connections. Age-related changes were seen in major white matter tracts, deep gray matter, and subcortical white matter, in our large (n=202), age-distributed sample. These diffusion changes followed an exponential pattern of maturation with considerable regional variation. Differences observed in developmental timing suggest a pattern of maturation in which areas with fronto-temporal connections develop more slowly than other regions. These in vivo results expand upon previous postmortem and imaging studies and provide quantitative measures indicative of the progression and magnitude of regional human brain maturation.
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              Relationship between multiple forms of childhood maltreatment and adult mental health in community respondents: results from the adverse childhood experiences study.

              This study examined the prevalence of a history of various combinations of childhood maltreatment types (physical abuse, sexual abuse, and witnessing of maternal battering) among adult members of a health maintenance organization (HMO) and explored the relationship with adult mental health of the combinations of types of childhood maltreatment and emotional abuse in the childhood family environment. A total of 8,667 adult members of an HMO completed measures of childhood exposure to family dysfunction, which included items on physical and sexual abuse, witnessing of maternal battering, and emotional abuse in the childhood family environment. The adults' current mental health was assessed by using the mental health scale of the Medical Outcomes Study 36-item Short-Form Health Survey. The prevalences of sexual abuse, physical abuse, and witnessing of maternal violence were 21.6%, 20.6%, and 14.0%, respectively, when the maltreatment types were considered separately. Among respondents reporting any of the maltreatment types, 34.6% reported more than one type of maltreatment. Lower mean mental health scores were associated with higher numbers of abuse categories (mean=78.5, 75.5, 72.8, and 69.9 for respondents with no, one, two, and three abuse types, respectively). Both an emotionally abusive family environment and the interaction of an emotionally abusive family environment with the various maltreatment types had a significant effect on mental health scores. Childhood physical and sexual abuse, as well as witnessing of maternal battering, were common among the adult members of an HMO in this study. Among those reporting any maltreatment, more than one-third had experienced more than one type of maltreatment. A dose-response relation was found between the number of types of maltreatment reported and mental health scores. In addition, an emotionally abusive family environment accentuated the decrements in mental health scores. Future research examining the effects of childhood maltreatment on adult mental health should include assessments of a wide range of abusive experiences, as well as the family atmosphere in which they occur.
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                Author and article information

                Journal
                Psychol Med
                Psychol Med
                PSM
                Psychological Medicine
                Cambridge University Press (Cambridge, UK )
                0033-2917
                1469-8978
                May 2018
                12 February 2018
                : 48
                : 7
                : 1092-1101
                Affiliations
                [1 ]Department of Child & Adolescent Psychiatry, Institute of Psychiatry , Psychology and Neuroscience, King's College London, UK
                [2 ]Department of Neuroimaging, Institute of Psychiatry , Psychology and Neuroscience, King's College London, London, UK
                [3 ]NIHR Biomedical Research Centre at South London and Maudsley Foundation NHS Trust and King's College London, Institute of Psychiatry , Psychology and Neuroscience, London, UK
                [4 ]SLAM NHS Trust , Kennington, London, UK
                Author notes
                Author for correspondence: Dr H. Hart, E-mail: heledd.hart@ 123456kcl.ac.uk
                [*]

                These authors contributed equally as joint first authors.

                Article
                S0033291716003585 00358
                10.1017/S0033291716003585
                6088776
                29429419
                2f4ba4d6-9d84-430d-868e-333220ab3f85
                © Cambridge University Press 2018

                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.

                History
                : 03 March 2016
                : 08 December 2016
                : 15 December 2016
                Page count
                Figures: 3, Tables: 3, References: 71, Pages: 10
                Categories
                Original Articles

                Clinical Psychology & Psychiatry
                child abuse,childhood maltreatment,fear processing,functional connectivity,insula,limbic,prefrontal

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