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      Discrete Neural Correlates for the Recognition of Negative Emotions: Insights from Frontotemporal Dementia

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          Abstract

          Patients with frontotemporal dementia have pervasive changes in emotion recognition and social cognition, yet the neural changes underlying these emotion processing deficits remain unclear. The multimodal system model of emotion proposes that basic emotions are dependent on distinct brain regions, which undergo significant pathological changes in frontotemporal dementia. As such, this syndrome may provide important insight into the impact of neural network degeneration upon the innate ability to recognise emotions. This study used voxel-based morphometry to identify discrete neural correlates involved in the recognition of basic emotions (anger, disgust, fear, sadness, surprise and happiness) in frontotemporal dementia. Forty frontotemporal dementia patients (18 behavioural-variant, 11 semantic dementia, 11 progressive nonfluent aphasia) and 27 healthy controls were tested on two facial emotion recognition tasks: The Ekman 60 and Ekman Caricatures. Although each frontotemporal dementia group showed impaired recognition of negative emotions, distinct associations between emotion-specific task performance and changes in grey matter intensity emerged. Fear recognition was associated with the right amygdala; disgust recognition with the left insula; anger recognition with the left middle and superior temporal gyrus; and sadness recognition with the left subcallosal cingulate, indicating that discrete neural substrates are necessary for emotion recognition in frontotemporal dementia. The erosion of emotion-specific neural networks in neurodegenerative disorders may produce distinct profiles of performance that are relevant to understanding the neurobiological basis of emotion processing.

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          Most cited references40

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          The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology.

          The human orbitofrontal cortex is an important brain region for the processing of rewards and punishments, which is a prerequisite for the complex and flexible emotional and social behaviour which contributes to the evolutionary success of humans. Yet much remains to be discovered about the functions of this key brain region, and new evidence from functional neuroimaging and clinical neuropsychology is affording new insights into the different functions of the human orbitofrontal cortex. We review the neuroanatomical and neuropsychological literature on the human orbitofrontal cortex, and propose two distinct trends of neural activity based on a meta-analysis of neuroimaging studies. One is a mediolateral distinction, whereby medial orbitofrontal cortex activity is related to monitoring the reward value of many different reinforcers, whereas lateral orbitofrontal cortex activity is related to the evaluation of punishers which may lead to a change in ongoing behaviour. The second is a posterior-anterior distinction with more complex or abstract reinforcers (such as monetary gain and loss) represented more anteriorly in the orbitofrontal cortex than simpler reinforcers such as taste or pain. Finally, we propose new neuroimaging methods for obtaining further evidence on the localisation of function in the human orbitofrontal cortex.
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            Neural systems for recognizing emotion.

            Recognition of emotion draws on a distributed set of structures that include the occipitotemporal neocortex, amygdala, orbitofrontal cortex and right frontoparietal cortices. Recognition of fear may draw especially on the amygdala and the detection of disgust may rely on the insula and basal ganglia. Two important mechanisms for recognition of emotions are the construction of a simulation of the observed emotion in the perceiver, and the modulation of sensory cortices via top-down influences.
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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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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2013
                21 June 2013
                : 8
                : 6
                : e67457
                Affiliations
                [1 ]Neuroscience Research Australia, Sydney, Australia
                [2 ]School of Medical Sciences, the University of New South Wales, Sydney, Australia
                [3 ]ARC Centre of Excellence in Cognition and its Disorders, the University of New South Wales, Sydney, Australia
                [4 ]School of Psychology, the University of New South Wales, Sydney, Australia
                University College London, United Kingdom
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: FK MI JRH OP. Analyzed the data: FK MI OP. Wrote the paper: FK MI JRH OP.

                Article
                PONE-D-13-04256
                10.1371/journal.pone.0067457
                3689735
                23805313
                f63a5321-f12d-4848-b449-dd81a8ec2029
                Copyright @ 2013

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 30 January 2013
                : 17 May 2013
                Page count
                Pages: 11
                Funding
                This work was supported by a National Health and Medical Research Council (NHMRC), of Australia project grant [510106]; the Australian Research Council (ARC) Centre of Excellence in Cognition and its Disorders [CE110001021]; an Australian Postgraduate Award (to FK); an ARC Federation Fellowship [FF0776229 to JRH]; and an NHMRC of Australia Career Development Fellowship [APP1022684 to OP]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Neuroscience
                Neuropsychology
                Medicine
                Mental Health
                Psychology
                Behavior
                Emotions
                Neurology
                Dementia
                Neuroimaging
                Social and Behavioral Sciences
                Psychology
                Behavior
                Emotions

                Uncategorized
                Uncategorized

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