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      In the face of threat: neural and endocrine correlates of impaired facial emotion recognition in cocaine dependence

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          Abstract

          The ability to recognize facial expressions of emotion in others is a cornerstone of human interaction. Selective impairments in the recognition of facial expressions of fear have frequently been reported in chronic cocaine users, but the nature of these impairments remains poorly understood. We used the multivariate method of partial least squares and structural magnetic resonance imaging to identify gray matter brain networks that underlie facial affect processing in both cocaine-dependent ( n=29) and healthy male volunteers ( n=29). We hypothesized that disruptions in neuroendocrine function in cocaine-dependent individuals would explain their impairments in fear recognition by modulating the relationship with the underlying gray matter networks. We found that cocaine-dependent individuals not only exhibited significant impairments in the recognition of fear, but also for facial expressions of anger. Although recognition accuracy of threatening expressions co-varied in all participants with distinctive gray matter networks implicated in fear and anger processing, in cocaine users it was less well predicted by these networks than in controls. The weaker brain-behavior relationships for threat processing were also mediated by distinctly different factors. Fear recognition impairments were influenced by variations in intelligence levels, whereas anger recognition impairments were associated with comorbid opiate dependence and related reduction in testosterone levels. We also observed an inverse relationship between testosterone levels and the duration of crack and opiate use. Our data provide novel insight into the neurobiological basis of abnormal threat processing in cocaine dependence, which may shed light on new opportunities facilitating the psychosocial integration of these patients.

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          Most cited references76

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          Cognitive neuroscience of human social behaviour.

          We are an intensely social species--it has been argued that our social nature defines what makes us human, what makes us conscious or what gave us our large brains. As a new field, the social brain sciences are probing the neural underpinnings of social behaviour and have produced a banquet of data that are both tantalizing and deeply puzzling. We are finding new links between emotion and reason, between action and perception, and between representations of other people and ourselves. No less important are the links that are also being established across disciplines to understand social behaviour, as neuroscientists, social psychologists, anthropologists, ethologists and philosophers forge new collaborations.
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            Amygdala and ventromedial prefrontal cortex are inversely coupled during regulation of negative affect and predict the diurnal pattern of cortisol secretion among older adults.

            Among younger adults, the ability to willfully regulate negative affect, enabling effective responses to stressful experiences, engages regions of prefrontal cortex (PFC) and the amygdala. Because regions of PFC and the amygdala are known to influence the hypothalamic-pituitary-adrenal axis, here we test whether PFC and amygdala responses during emotion regulation predict the diurnal pattern of salivary cortisol secretion. We also test whether PFC and amygdala regions are engaged during emotion regulation in older (62- to 64-year-old) rather than younger individuals. We measured brain activity using functional magnetic resonance imaging as participants regulated (increased or decreased) their affective responses or attended to negative picture stimuli. We also collected saliva samples for 1 week at home for cortisol assay. Consistent with previous work in younger samples, increasing negative affect resulted in ventral lateral, dorsolateral, and dorsomedial regions of PFC and amygdala activation. In contrast to previous work, decreasing negative affect did not produce the predicted robust pattern of higher PFC and lower amygdala activation. Individuals demonstrating the predicted effect (decrease < attend in the amygdala), however, exhibited higher signal in ventromedial prefrontal cortex (VMPFC) for the same contrast. Furthermore, participants displaying higher VMPFC and lower amygdala signal when decreasing compared with the attention control condition evidenced steeper, more normative declines in cortisol over the course of the day. Individual differences yielded the predicted link between brain function while reducing negative affect in the laboratory and diurnal regulation of endocrine activity in the home environment.
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              Social learning of fear.

              Research across species highlights the critical role of the amygdala in fear conditioning. However, fear conditioning, involving direct aversive experience, is only one means by which fears can be acquired. Exploiting aversive experiences of other individuals through social fear learning is less risky. Behavioral research provides important insights into the workings of social fear learning, and the neural mechanisms are beginning to be understood. We review research suggesting that an amygdala-centered model of fear conditioning can help to explain social learning of fear through observation and instruction. We also describe how observational and instructed fear is distinguished by involvement of additional neural systems implicated in social-emotional behavior, language and explicit memory, and propose a modified conditioning model to account for social fear learning. A better understanding of social fear learning promotes integration of biological principles of learning with cultural evolution.
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                Author and article information

                Journal
                Transl Psychiatry
                Transl Psychiatry
                Translational Psychiatry
                Nature Publishing Group
                2158-3188
                May 2015
                26 May 2015
                1 May 2015
                : 5
                : 5
                : e570
                Affiliations
                [1 ]Department of Psychiatry, University of Cambridge , Cambridge, UK
                [2 ]Behavioural and Clinical Neuroscience Institute, University of Cambridge , Cambridge, UK
                [3 ]Department of Psychology, University of Cambridge , Cambridge, UK
                [4 ]Medical Research Council Cognition and Brain Sciences Unit , Cambridge, UK
                [5 ]Wolfson Brain Imaging Centre, University of Cambridge , Cambridge, UK
                Author notes
                [* ]Department of Psychiatry, University of Cambridge, Herchel Smith Building for Brain and Mind Sciences , Cambridge Biomedical Campus, Cambridge CB2 0SZ, UK. E-mail: ke220@ 123456cam.ac.uk
                [✠]

                Deceased.

                Article
                tp201558
                10.1038/tp.2015.58
                4471289
                26080087
                bddedffd-5ca7-41e2-8b68-af90935b5639
                Copyright © 2015 Macmillan Publishers Limited

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 02 November 2014
                : 27 February 2015
                : 24 March 2015
                Categories
                Original Article

                Clinical Psychology & Psychiatry
                Clinical Psychology & Psychiatry

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