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      The Role of the Amygdala in Facial Trustworthiness Processing: A Systematic Review and Meta-Analyses of fMRI Studies

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          Abstract

          Background

          Faces play a key role in signaling social cues such as signals of trustworthiness. Although several studies identify the amygdala as a core brain region in social cognition, quantitative approaches evaluating its role are scarce.

          Objectives

          This review aimed to assess the role of the amygdala in the processing of facial trustworthiness, by analyzing its amplitude BOLD response polarity to untrustworthy versus trustworthy facial signals under fMRI tasks through a Meta-analysis of effect sizes (MA). Activation Likelihood Estimation (ALE) analyses were also conducted.

          Data sources

          Articles were retrieved from MEDLINE, ScienceDirect and Web-of-Science in January 2016. Following the PRISMA statement guidelines, a systematic review of original research articles in English language using the search string “(face OR facial) AND (trustworthiness OR trustworthy OR untrustworthy OR trustee) AND fMRI” was conducted.

          Study selection and data extraction

          The MA concerned amygdala responses to facial trustworthiness for the contrast Untrustworthy vs. trustworthy faces, and included whole-brain and ROI studies. To prevent potential bias, results were considered even when at the single study level they did not survive correction for multiple comparisons or provided non-significant results. ALE considered whole-brain studies, using the same methodology to prevent bias. A summary of the methodological options (design and analysis) described in the articles was finally used to get further insight into the characteristics of the studies and to perform a subgroup analysis. Data were extracted by two authors and checked independently.

          Data synthesis

          Twenty fMRI studies were considered for systematic review. An MA of effect sizes with 11 articles (12 studies) showed high heterogeneity between studies [Q(11) = 265.68, p < .0001; I 2 = 95.86%, 94.20% to 97.05%, with 95% confidence interval, CI]. Random effects analysis [RE(183) = 0.851, .422 to .969, 95% CI] supported the evidence that the (right) amygdala responds preferentially to untrustworthy faces. Moreover, two ALE analyses performed with 6 articles (7 studies) identified the amygdala, insula and medial dorsal nuclei of thalamus as structures with negative correlation with trustworthiness. Six articles/studies showed that posterior cingulate and medial frontal gyrus present positive correlations with increasing facial trustworthiness levels. Significant effects considering subgroup analysis based on methodological criteria were found for experiments using spatial smoothing, categorization of trustworthiness in 2 or 3 categories and paradigms which involve both explicit and implicit tasks.

          Limitations

          Significant heterogeneity between studies was found in MA, which might have arisen from inclusion of studies with smaller sample sizes and differences in methodological options. Studies using ROI analysis / small volume correction methods were more often devoted specifically to the amygdala region, with some results reporting uncorrected p-values based on mainly clinical a priori evidence of amygdala involvement in these processes. Nevertheless, we did not find significant evidence for publication bias.

          Conclusions and implications of key findings

          Our results support the role of amygdala in facial trustworthiness judgment, emphasizing its predominant role during processing of negative social signals in (untrustworthy) faces. This systematic review suggests that little consistency exists among studies’ methodology, and that larger sample sizes should be preferred.

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          Most cited references41

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          • Abstract: found
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          Cognitive neuroscience of human social behaviour.

          We are an intensely social species--it has been argued that our social nature defines what makes us human, what makes us conscious or what gave us our large brains. As a new field, the social brain sciences are probing the neural underpinnings of social behaviour and have produced a banquet of data that are both tantalizing and deeply puzzling. We are finding new links between emotion and reason, between action and perception, and between representations of other people and ourselves. No less important are the links that are also being established across disciplines to understand social behaviour, as neuroscientists, social psychologists, anthropologists, ethologists and philosophers forge new collaborations.
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            Neural bases of the non-conscious perception of emotional signals.

            Many emotional stimuli are processed without being consciously perceived. Recent evidence indicates that subcortical structures have a substantial role in this processing. These structures are part of a phylogenetically ancient pathway that has specific functional properties and that interacts with cortical processes. There is now increasing evidence that non-consciously perceived emotional stimuli induce distinct neurophysiological changes and influence behaviour towards the consciously perceived world. Understanding the neural bases of the non-conscious perception of emotional signals will clarify the phylogenetic continuity of emotion systems across species and the integration of cortical and subcortical activity in the human brain.
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              Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge.

              Functional magnetic resonance imaging (fMRI) of the human brain was used to study whether the amygdala is activated in response to emotional stimuli, even in the absence of explicit knowledge that such stimuli were presented. Pictures of human faces bearing fearful or happy expressions were presented to 10 normal, healthy subjects by using a backward masking procedure that resulted in 8 of 10 subjects reporting that they had not seen these facial expressions. The backward masking procedure consisted of 33 msec presentations of fearful or happy facial expressions, their offset coincident with the onset of 167 msec presentations of neutral facial expressions. Although subjects reported seeing only neutral faces, blood oxygen level-dependent (BOLD) fMRI signal in the amygdala was significantly higher during viewing of masked fearful faces than during the viewing of masked happy faces. This difference was composed of significant signal increases in the amygdala to masked fearful faces as well as significant signal decreases to masked happy faces, consistent with the notion that the level of amygdala activation is affected differentially by the emotional valence of external stimuli. In addition, these facial expressions activated the sublenticular substantia innominata (SI), where signal increases were observed to both fearful and happy faces--suggesting a spatial dissociation of territories that respond to emotional valence versus salience or arousal value. This study, using fMRI in conjunction with masked stimulus presentations, represents an initial step toward determining the role of the amygdala in nonconscious processing.
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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, CA USA )
                1932-6203
                29 November 2016
                2016
                : 11
                : 11
                : e0167276
                Affiliations
                [1 ]Visual Neuroscience Laboratory, Institute for Biomedical Imaging and Life Sciences (CNC.IBILI), Faculty of Medicine, University of Coimbra (UC), Coimbra, Portugal
                [2 ]Laboratory of Biostatistics and Medical Informatics, Institute for Biomedical Imaging and Life Sciences (CNC.IBILI), Faculty of Medicine, University of Coimbra (UC), Coimbra, Portugal
                [3 ]Institute for Nuclear Sciences Applied to Health (ICNAS), Brain Imaging Network of Portugal, Coimbra, Portugal
                University of Toyama, JAPAN
                Author notes

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

                • Conceptualization: SS IA MCB.

                • Formal analysis: SS IA BO.

                • Funding acquisition: MCB.

                • Investigation: SS IA.

                • Methodology: BO.

                • Project administration: MCB.

                • Resources: SS IA BO MCB.

                • Supervision: MCB.

                • Writing – original draft: SS IA.

                • Writing – review & editing: SS IA BO MCB.

                Author information
                http://orcid.org/0000-0003-4364-6373
                Article
                PONE-D-16-29527
                10.1371/journal.pone.0167276
                5127572
                27898705
                c093deda-de88-4a97-83e2-fe3f8df4610e
                © 2016 Santos et al

                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
                : 23 July 2016
                : 8 November 2016
                Page count
                Figures: 6, Tables: 5, Pages: 28
                Funding
                Funded by: Foundation for Science and Technology (FCT) (PT)
                Award ID: UID/NEU/04539/2013, Strategic Project and POCI-01-0145-FEDER-007440
                Award Recipient :
                Funded by: Bial Foundation (PT)
                Award ID: 132/12 and 373/14
                Award Recipient :
                Funded by: Bial Foundation (PT)
                Award ID: 133/12
                Award Recipient :
                Funded by: European Commission (BE); European Regional Development Fund (ERDF) (BE)
                Award ID: QREN Centro-07-ST24-FEDER-002005
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100004963, Seventh Framework Programme;
                Award ID: FP7-HEALTH-2013-INNOVATION-1 - 602186 – BRAINTRAIN
                Award Recipient :
                This work was funded by Bial Foundation Grants 132/12 and 133/12, Projeto UID/NEU/04539/2013, Strategic Project and POCI-01-0145-FEDER-007440 of the Foundation for Science and Technology (FCT) (Portugal), “Projecto Operacional Regional do Centro” (QREN Centro-07-ST24-FEDER-002005), funded by the European Commission and the program Mais Centro (Portugal), and FP7-HEALTH-2013-INNOVATION-1 - 602186 – BRAINTRAIN, funded by the European Commission in their Seventh Framework Program. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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