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      Dynamic human and avatar facial expressions elicit differential brain responses

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          Abstract

          Computer-generated characters, so-called avatars, are widely used in advertising, entertainment, human–computer interaction or as research tools to investigate human emotion perception. However, brain responses to avatar and human faces have scarcely been studied to date. As such, it remains unclear whether dynamic facial expressions of avatars evoke different brain responses than dynamic facial expressions of humans. In this study, we designed anthropomorphic avatars animated with motion tracking and tested whether the human brain processes fearful and neutral expressions in human and avatar faces differently. Our fMRI results showed that fearful human expressions evoked stronger responses than fearful avatar expressions in the ventral anterior and posterior cingulate gyrus, the anterior insula, the anterior and posterior superior temporal sulcus, and the inferior frontal gyrus. Fearful expressions in human and avatar faces evoked similar responses in the amygdala. We did not find different responses to neutral human and avatar expressions. Our results highlight differences, but also similarities in the processing of fearful human expressions and fearful avatar expressions even if they are designed to be highly anthropomorphic and animated with motion tracking. This has important consequences for research using dynamic avatars, especially when processes are investigated that involve cortical and subcortical regions.

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          Most cited references48

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          The neural bases of emotion regulation.

          Emotions are powerful determinants of behaviour, thought and experience, and they may be regulated in various ways. Neuroimaging studies have implicated several brain regions in emotion regulation, including the ventral anterior cingulate and ventromedial prefrontal cortices, as well as the lateral prefrontal and parietal cortices. Drawing on computational approaches to value-based decision-making and reinforcement learning, we propose a unifying conceptual framework for understanding the neural bases of diverse forms of emotion regulation.
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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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              Effects of attention and emotion on face processing in the human brain: an event-related fMRI study.

              We used event-related fMRI to assess whether brain responses to fearful versus neutral faces are modulated by spatial attention. Subjects performed a demanding matching task for pairs of stimuli at prespecified locations, in the presence of task-irrelevant stimuli at other locations. Faces or houses unpredictably appeared at the relevant or irrelevant locations, while the faces had either fearful or neutral expressions. Activation of fusiform gyri by faces was strongly affected by attentional condition, but the left amygdala response to fearful faces was not. Right fusiform activity was greater for fearful than neutral faces, independently of the attention effect on this region. These results reveal differential influences on face processing from attention and emotion, with the amygdala response to threat-related expressions unaffected by a manipulation of attention that strongly modulates the fusiform response to faces.
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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
                March 2020
                30 March 2020
                30 March 2020
                : 15
                : 3
                : 303-317
                Affiliations
                [1 ] Swiss Epilepsy Center , CH-8008 Zurich, Switzerland
                [2 ] Department of Psychology , University of Zurich, Zurich, Switzerland
                [3 ] Neuropsychology Unit , Valens Rehabilitation Centre, Valens, Switzerland
                [4 ] Institute for the Performing Arts and Film , Zurich University of the Arts, Zurich, Switzerland
                [5 ] Institute for Critical Theory , Zurich University of the Arts, Zurich, Switzerland
                [6 ] Department of Psychiatry , Psychotherapy, and Psychosomatics, University Hospital of Psychiatry Zurich, Zurich, Switzerland
                [7 ] Department of Psychology , University of Bern, Bern, Switzerland
                Author notes
                Correspondence should be addressed to Lorena C. Kegel, Swiss Epilepsy Center, Bleulerstrasse 60, CH-8008 Zurich, Switzerland. E-mail: lorenakegel@ 123456gmail.com
                Article
                nsaa039
                10.1093/scan/nsaa039
                7235958
                32232359
                a8f7d22c-fe98-4d6f-a652-7adf64898ecc
                © The Author(s) 2020. Published by Oxford University Press.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 13 December 2019
                : 2 March 2020
                : 18 March 2020
                : 24 March 2020
                Page count
                Pages: 12
                Funding
                Funded by: Swiss National Science Foundation, DOI 10.13039/501100001711;
                Award ID: 166416
                Categories
                Original Manuscript

                Neurosciences
                face,emotion,avatar,computer-generated character,fmri
                Neurosciences
                face, emotion, avatar, computer-generated character, fmri

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