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      Dissociative part-dependent biopsychosocial reactions to backward masked angry and neutral faces: An fMRI study of dissociative identity disorder

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          Abstract

          Objective

          The Theory of Structural Dissociation of the Personality (TSDP) proposes that dissociative identity disorder (DID) patients are fixed in traumatic memories as “Emotional Parts” (EP), but mentally avoid these as “Apparently Normal Parts” of the personality (ANP). We tested the hypotheses that ANP and EP have different biopsychosocial reactions to subliminally presented angry and neutral faces, and that actors instructed and motivated to simulate ANP and EP react differently.

          Methods

          Women with DID and matched healthy female actors (CON) were as ANP and EP (DIDanp, DIDep, CONanp, CONep) consecutively exposed to masked neutral and angry faces. Their brain activation was monitored using functional magnetic resonance imaging. The black-and-white dotted masks preceding and following the faces each had a centered colored dot, but in a different color. Participants were instructed to immediately press a button after a perceived color change. State anxiety was assessed after each run using the STAI-S. Final statistical analyses were conducted on 11 DID patients and 15 controls for differences in neural activity, and 13 DID patients and 15 controls for differences in behavior and psychometric measures.

          Results

          Differences between ANP and EP in DID patients and between DID and CON in the two dissociative parts of the personality were generally larger for neutral than for angry faces. The longest reaction times (RTs) existed for DIDep when exposed to neutral faces. Compared to DIDanp, DIDep was associated with more activation of the parahippocampal gyrus. Following neutral faces and compared to CONep, DIDep had more activation in the brainstem, face-sensitive regions, and motor-related areas. DIDanp showed a decreased activity all over the brain in the neutral and angry face condition. There were neither significant within differences nor significant between group differences in state anxiety. CON was not able to simulate genuine ANP and EP biopsychosocially.

          Conclusions

          DID patients have dissociative part-dependent biopsychosocial reactions to masked neutral and angry faces. As EP, they are overactivated, and as ANP underactivated. The findings support TSDP. Major clinical implications are discussed.

          Highlights

          • Neural/behavioral differences between EP and ANP exist at a preconscious level.

          • EP but not ANP showed a positive attentional bias to masked facial stimuli.

          • Masked neutral faces elicited dorsal brainstem and occipitotemporal activity in EP.

          • EP’s reaction pattern suggests preconscious fixation particularly on neutral faces.

          • Actors were unable to mimic the neural/behavioral reactions of DID patients.

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          Most cited references92

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          Pain and emotion interactions in subregions of the cingulate gyrus.

          Brent Vogt (2005)
          Acute pain and emotion are processed in two forebrain networks, and the cingulate cortex is involved in both. Although Brodmann's cingulate gyrus had two divisions and was not based on any functional criteria, functional imaging studies still use this model. However, recent cytoarchitectural studies of the cingulate gyrus support a four-region model, with subregions, that is based on connections and qualitatively unique functions. Although the activity evoked by pain and emotion has been widely reported, some view them as emergent products of the brain rather than of small aggregates of neurons. Here, we assess pain and emotion in each cingulate subregion, and assess whether pain is co-localized with negative affect. Amazingly, these activation patterns do not simply overlap.
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            Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies.

            Most of our social interactions involve perception of emotional information from the faces of other people. Furthermore, such emotional processes are thought to be aberrant in a range of clinical disorders, including psychosis and depression. However, the exact neurofunctional maps underlying emotional facial processing are not well defined. Two independent researchers conducted separate comprehensive PubMed (1990 to May 2008) searches to find all functional magnetic resonance imaging (fMRI) studies using a variant of the emotional faces paradigm in healthy participants. The search terms were: "fMRI AND happy faces," "fMRI AND sad faces," "fMRI AND fearful faces," "fMRI AND angry faces," "fMRI AND disgusted faces" and "fMRI AND neutral faces." We extracted spatial coordinates and inserted them in an electronic database. We performed activation likelihood estimation analysis for voxel-based meta-analyses. Of the originally identified studies, 105 met our inclusion criteria. The overall database consisted of 1785 brain coordinates that yielded an overall sample of 1600 healthy participants. Quantitative voxel-based meta-analysis of brain activation provided neurofunctional maps for 1) main effect of human faces; 2) main effect of emotional valence; and 3) modulatory effect of age, sex, explicit versus implicit processing and magnetic field strength. Processing of emotional faces was associated with increased activation in a number of visual, limbic, temporoparietal and prefrontal areas; the putamen; and the cerebellum. Happy, fearful and sad faces specifically activated the amygdala, whereas angry or disgusted faces had no effect on this brain region. Furthermore, amygdala sensitivity was greater for fearful than for happy or sad faces. Insular activation was selectively reported during processing of disgusted and angry faces. However, insular sensitivity was greater for disgusted than for angry faces. Conversely, neural response in the visual cortex and cerebellum was observable across all emotional conditions. Although the activation likelihood estimation approach is currently one of the most powerful and reliable meta-analytical methods in neuroimaging research, it is insensitive to effect sizes. Our study has detailed neurofunctional maps to use as normative references in future fMRI studies of emotional facial processing in psychiatric populations. We found selective differences between neural networks underlying the basic emotions in limbic and insular brain regions.
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              Conscious and unconscious emotional learning in the human amygdala.

              If subjects are shown an angry face as a target visual stimulus for less than forty milliseconds and are then immediately shown an expressionless mask, these subjects report seeing the mask but not the target. However, an aversively conditioned masked target can elicit an emotional response from subjects without being consciously perceived. Here we study the mechanism of this unconsciously mediated emotional learning. We measured neural activity in volunteer subjects who were presented with two angry faces, one of which, through previous classical conditioning, was associated with a burst of white noise. In half of the trials, the subjects' awareness of the angry faces was prevented by backward masking with a neutral face. A significant neural response was elicited in the right, but not left, amygdala to masked presentations of the conditioned angry face. Unmasked presentations of the same face produced enhanced neural activity in the left, but not right, amygdala. Our results indicate that, first, the human amygdala can discriminate between stimuli solely on the basis of their acquired behavioural significance, and second, this response is lateralized according to the subjects' level of awareness of the stimuli.
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                Author and article information

                Contributors
                Journal
                Neuroimage (Amst)
                Neuroimage (Amst)
                NeuroImage : Clinical
                Elsevier
                2213-1582
                12 July 2013
                12 July 2013
                2013
                : 3
                : 54-64
                Affiliations
                [a ]Division of Neuropsychology, Institute of Psychology, University of Zurich, Switzerland
                [b ]Top Referent Trauma Center Mental Health Care Drenthe, Assen, The Netherlands
                [c ]Department of Neuroscience, University Medical Center Groningen, and BCN Neuroimaging Center, University of Groningen, Groningen, The Netherlands
                [d ]Private Practice, Eschen, Liechtenstein
                [e ]Fribourg General Hospital, Fribourg, Switzerland
                [f ]Institute for Biomedical Engineering, University and ETH Zurich, Switzerland
                [g ]Division Clinical Psychology and Psychotherapy, Institute of Psychology, University of Zurich, Switzerland
                [h ]Department of Psychosis Studies, Institute of Psychiatry, King's College London, London, UK
                [i ]International Normal Aging and Plasticity Imaging Center, University of Zurich, Switzerland
                Author notes
                [* ]Corresponding author at: Institute of Psychology, Division Neuropsychology, University of Zurich, Binzmühlestrasse 14/25, CH-8050 Zurich, Switzerland. Tel.: + 41 44 635 7404; fax: + 41 44 635 7409. y.schlumpf@ 123456psychologie.uzh.ch
                Article
                S2213-1582(13)00089-2
                10.1016/j.nicl.2013.07.002
                3791283
                24179849
                2a86b6a7-9e2c-4f31-ae10-03d8b8778e3b
                © 2013 The Authors

                This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial-No Derivative Works License, which permits non-commercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 6 March 2013
                : 28 June 2013
                : 3 July 2013
                Categories
                Article

                dissociative identity disorder,neuroimaging,backward masking,face perception,emotional ambiguity,hypervigilance

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