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      Dissociation of Neural Substrates of Response Inhibition to Negative Information between Implicit and Explicit Facial Go/Nogo Tasks: Evidence from an Electrophysiological Study

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          Abstract

          Background

          Although ample evidence suggests that emotion and response inhibition are interrelated at the behavioral and neural levels, neural substrates of response inhibition to negative facial information remain unclear. Thus we used event-related potential (ERP) methods to explore the effects of explicit and implicit facial expression processing in response inhibition.

          Methods

          We used implicit (gender categorization) and explicit emotional Go/Nogo tasks (emotion categorization) in which neutral and sad faces were presented. Electrophysiological markers at the scalp and the voxel level were analyzed during the two tasks.

          Results

          We detected a task, emotion and trial type interaction effect in the Nogo-P3 stage. Larger Nogo-P3 amplitudes during sad conditions versus neutral conditions were detected with explicit tasks. However, the amplitude differences between the two conditions were not significant for implicit tasks. Source analyses on P3 component revealed that right inferior frontal junction (rIFJ) was involved during this stage. The current source density (CSD) of rIFJ was higher with sad conditions compared to neutral conditions for explicit tasks, rather than for implicit tasks.

          Conclusions

          The findings indicated that response inhibition was modulated by sad facial information at the action inhibition stage when facial expressions were processed explicitly rather than implicitly. The rIFJ may be a key brain region in emotion regulation.

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          Most cited references63

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          Influence of cognitive control and mismatch on the N2 component of the ERP: a review.

          Recent years have seen an explosion of research on the N2 component of the event-related potential, a negative wave peaking between 200 and 350 ms after stimulus onset. This research has focused on the influence of "cognitive control," a concept that covers strategic monitoring and control of motor responses. However, rich research traditions focus on attention and novelty or mismatch as determinants of N2 amplitude. We focus on paradigms that elicit N2 components with an anterior scalp distribution, namely, cognitive control, novelty, and sequential matching, and argue that the anterior N2 should be divided into separate control- and mismatch-related subcomponents. We also argue that the oddball N2 belongs in the family of attention-related N2 components that, in the visual modality, have a posterior scalp distribution. We focus on the visual modality for which components with frontocentral and more posterior scalp distributions can be readily distinguished.
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            Failure to regulate: counterproductive recruitment of top-down prefrontal-subcortical circuitry in major depression.

            Although depressed mood is a normal occurrence in response to adversity in all individuals, what distinguishes those who are vulnerable to major depressive disorder (MDD) is their inability to effectively regulate negative mood when it arises. Investigating the neural underpinnings of adaptive emotion regulation and the extent to which such processes are compromised in MDD may be helpful in understanding the pathophysiology of depression. We report results from a functional magnetic resonance imaging study demonstrating left-lateralized activation in the prefrontal cortex (PFC) when downregulating negative affect in nondepressed individuals, whereas depressed individuals showed bilateral PFC activation. Furthermore, during an effortful affective reappraisal task, nondepressed individuals showed an inverse relationship between activation in left ventrolateral PFC and the amygdala that is mediated by the ventromedial PFC (VMPFC). No such relationship was found for depressed individuals, who instead show a positive association between VMPFC and amygdala. Pupil dilation data suggest that those depressed patients who expend more effort to reappraise negative stimuli are characterized by accentuated activation in the amygdala, insula, and thalamus, whereas nondepressed individuals exhibit the opposite pattern. These findings indicate that a key feature underlying the pathophysiology of major depression is the counterproductive engagement of right prefrontal cortex and the lack of engagement of left lateral-ventromedial prefrontal circuitry important for the downregulation of amygdala responses to negative stimuli.
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              Neural processing of emotional faces requires attention.

              Attention gates the processing of stimuli relatively early in visual cortex. Yet, existing data suggest that emotional stimuli activate brain regions automatically, largely immune from attentional control. To resolve this puzzle, we used functional magnetic resonance imaging to first measure activation in regions that responded differentially to faces with emotional expressions (fearful and happy) compared with neutral faces. We then measured the modulation of these responses by attention, using a competing task with a high attentional load. Contrary to the prevailing view, all brain regions responding differentially to emotional faces, including the amygdala, did so only when sufficient attentional resources were available to process the faces. Thus, the processing of facial expression appears to be under top-down control.
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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
                2014
                16 October 2014
                : 9
                : 10
                : e109839
                Affiliations
                [1 ]Laboratory of Cognitive Neuropsychology, Department of Medical Psychology, Anhui Medical University, Hefei, China
                [2 ]School of Humanities and Social Sciences, Beijing Forestry University, Beijing, China
                [3 ]Faculty of Psychology, Universidad Autónoma de Madrid, Madrid, Spain
                [4 ]Department of Neurology, the First Affiliated Hospital of Anhui Medical University, Hefei, China
                [5 ]Anhui Mental Health Center, Hefei, China
                [6 ]Institute of Social and affective Neuroscience, Shenzhen University, Shenzhen, China
                University of Rome, Italy
                Author notes

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

                Conceived and designed the experiments: FQY RY YJL KW. Performed the experiments: LZ. Analyzed the data: FQY RY SYS LC. Contributed reagents/materials/analysis tools: RY SYS CYZ YD. Wrote the paper: FQY RY KW.

                Article
                PONE-D-14-26227
                10.1371/journal.pone.0109839
                4199673
                25330212
                98772143-9b2c-4d47-b74c-0ebe589df344
                Copyright @ 2014

                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
                : 12 June 2014
                : 3 September 2014
                Page count
                Pages: 10
                Funding
                This research was supported by the National Natural Science Foundation of China (31000503, 91232717, 31100812, 81301176, and 81300944) and the Ministry of Science and Technology (2011CB707805). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Neuroscience
                Cognitive Neuroscience
                Cognitive Neurology
                Working Memory
                Cognitive Science
                Cognitive Psychology
                Attention
                Social Cognition
                Behavioral Neuroscience
                Psychology
                Behavior
                Inhibitions
                Clinical Psychology
                Emotions
                Social Psychology
                Social Sciences
                Custom metadata
                The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper and its Supporting Information files.

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                Uncategorized

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