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      Impaired cortico-limbic functional connectivity in schizophrenia patients during emotion processing

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          Abstract

          Functional dysconnection is increasingly recognized as a core pathological feature in schizophrenia. Aberrant interactions between regions of the cortico-limbic circuit may underpin the abnormal emotional processing associated with this illness. We used a functional magnetic resonance imaging paradigm designed to dissociate the various components of the cortico-limbic circuit (i.e. a ventral automatic circuit that is intertwined with a dorsal cognitive circuit), to explore bottom-up appraisal as well as top-down control during emotion processing. In schizophrenia patients compared with healthy controls, bottom-up processes were associated with reduced interaction between the amygdala and both the anterior cingulate cortex (ACC) and the dorsolateral prefrontal cortex. Contrariwise, top-down control processes led to stronger connectivity between the ventral affective and the dorsal cognitive circuits, i.e. heightened interactions between the ventral ACC and the dorsolateral prefrontal cortex as well as between dorsal and ventral ACC. These findings offer a comprehensive view of the cortico-limbic dysfunction in schizophrenia. They confirm previous results of impaired propagation of information between the amygdala and the prefrontal cortex and suggest a defective functional segregation in the dorsal cognitive part of the cortico-limbic circuit.

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          Most cited references73

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          The neural bases of emotion regulation: reappraisal and suppression of negative emotion.

          Emotion regulation strategies are thought to differ in when and how they influence the emotion-generative process. However, no study to date has directly probed the neural bases of two contrasting (e.g., cognitive versus behavioral) emotion regulation strategies. This study used functional magnetic resonance imaging (fMRI) to examine cognitive reappraisal (a cognitive strategy thought to have its impact early in the emotion-generative process) and expressive suppression (a behavioral strategy thought to have its impact later in the emotion-generative process). Seventeen women viewed 15 sec neutral and negative emotion-eliciting films under four conditions--watch-neutral, watch-negative, reappraise-negative, and suppress-negative--while providing emotion experience ratings and having their facial expressions videotaped. Reappraisal resulted in early (0-4.5 sec) prefrontal cortex (PFC) responses, decreased negative emotion experience, and decreased amygdala and insular responses. Suppression produced late (10.5-15 sec) PFC responses, decreased negative emotion behavior and experience, but increased amygdala and insular responses. These findings demonstrate the differential efficacy of reappraisal and suppression on emotional experience, facial behavior, and neural response and highlight intriguing differences in the temporal dynamics of these two emotion regulation strategies.
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            Neurobiology of emotion perception I: The neural basis of normal emotion perception.

            There is at present limited understanding of the neurobiological basis of the different processes underlying emotion perception. We have aimed to identify potential neural correlates of three processes suggested by appraisalist theories as important for emotion perception: 1) the identification of the emotional significance of a stimulus; 2) the production of an affective state in response to 1; and 3) the regulation of the affective state. In a critical review, we have examined findings from recent animal, human lesion, and functional neuroimaging studies. Findings from these studies indicate that these processes may be dependent upon the functioning of two neural systems: a ventral system, including the amygdala, insula, ventral striatum, and ventral regions of the anterior cingulate gyrus and prefrontal cortex, predominantly important for processes 1 and 2 and automatic regulation of emotional responses; and a dorsal system, including the hippocampus and dorsal regions of anterior cingulate gyrus and prefrontal cortex, predominantly important for process 3. We suggest that the extent to which a stimulus is identified as emotive and is associated with the production of an affective state may be dependent upon levels of activity within these two neural systems.
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              Cognitive and emotional influences in anterior cingulate cortex.

              Bush, Luu, Posner (2000)
              Anterior cingulate cortex (ACC) is a part of the brain's limbic system. Classically, this region has been related to affect, on the basis of lesion studies in humans and in animals. In the late 1980s, neuroimaging research indicated that ACC was active in many studies of cognition. The findings from EEG studies of a focal area of negativity in scalp electrodes following an error response led to the idea that ACC might be the brain's error detection and correction device. In this article, these various findings are reviewed in relation to the idea that ACC is a part of a circuit involved in a form of attention that serves to regulate both cognitive and emotional processing. Neuroimaging studies showing that separate areas of ACC are involved in cognition and emotion are discussed and related to results showing that the error negativity is influenced by affect and motivation. In addition, the development of the emotional and cognitive roles of ACC are discussed, and how the success of this regulation in controlling responses might be correlated with cingulate size. Finally, some theories are considered about how the different subdivisions of ACC might interact with other cortical structures as a part of the circuits involved in the regulation of mental and emotional activity.
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                Author and article information

                Journal
                Soc Cogn Affect Neurosci
                Soc Cogn Affect Neurosci
                scan
                Social Cognitive and Affective Neuroscience
                Oxford University Press
                1749-5016
                1749-5024
                April 2018
                23 October 2017
                23 October 2017
                : 13
                : 4
                : 381-390
                Affiliations
                [1 ]Timone Institute of Neuroscience, UMR 7289, CNRS and Aix-Marseille University, Marseille, France
                [2 ]Department of Psychiatry, La Conception University Hospital, Marseille, France
                [3 ]Cognitive Neurosciences Laboratory, UMR 7291, CNRS and Aix-Marseille University, Marseille, France
                [4 ]Department of Psychiatry, University Hospital of Saint-Etienne, Saint-Etienne, France
                [5 ]Inserm U1059, University of Lyon, Saint-Etienne F-42023, France
                [6 ]Neuroradiology Unit, University Hospital of Saint-Etienne, Saint-Etienne, France
                [7 ]Clinic of Mental Health, L’escale, Orpea-Clinéa, Saint-Victoret, France
                [8 ]Department of Psychiatry, Sainte Marguerite University Hospital, Marseille, France
                [9 ]Intersector Clinical Psychiatric Research Unit, Psychobiology of Compulsive Disorders Team, Experimental and Clinical Neurosciences Laboratory, Henri Laborit Hospital, INSERM U 1084, University of Poitiers; Experimental and Clinical Neurosciences Laboratory, CIC INSERM U 802, Poitiers, France
                [10 ]CRN2M-UMR7286, CNRS and Aix-Marseille University, Marseille, France
                [11 ]FondaMental Fundation, Fundation of Research and of Mental Health Care, Créteil, France
                [12 ]Unit for Clinical Pharmacology and Therapeutic Evaluation (CIC-UPCET), Timone Hospital, Public Assistance for Marseille Hospitals (APHM), Marseille, France
                Author notes
                Correspondence should be addressed to Pr. Eric Fakra, CHU Saint-Etienne, Pôle Universitaire de Psychiatrie, 5 Chemin de la Marendière, 42055 Saint-priest-en-jarez Cedex 2, France. E-mail: Eric.Fakra@ 123456chu-st-etienne.fr
                Article
                nsx083
                10.1093/scan/nsx083
                5928402
                29069508
                83f88896-04d7-41ac-900b-4a71e1d693ea
                © The Author (2017). Published by Oxford University Press.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com

                History
                : 06 November 2016
                : 8 June 2017
                : 19 June 2017
                Page count
                Pages: 10
                Categories
                Original Articles

                Neurosciences
                affect,functional magnetic resonance imaging,amygdala,anterior cingulate cortex,prefrontal cortex,schizophrenia

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