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

Abstract

BackgroundFaces 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.ObjectivesThis 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 sourcesArticles 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 extractionThe 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 synthesisTwenty 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; I2 = 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.LimitationsSignificant 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...

The Older Adult Positivity Effect in Evaluations of Trustworthiness: Emotion Regulation or Cognitive Capacity?

“…Indeed, previous research has shown that compared with faces average or high in attractiveness, very ugly or disfigured faces, like those shown in Study 1, elicit greater amygdala activation [44, 45]. Similarly, a recent meta-analyses revealed that even normal faces that are low in trustworthiness, like those shown in Study 2, elicit greater amygdala activation than do high trustworthy faces [46]. …”

“…Future research should employ additional measures of cognitive capacity to further investigate its contribution to age differences in the positivity of stimulus evaluations. It is possible that the previously demonstrated OA positivity effect in memory also may reflect age-related declines in cognitive capacity, as recent evidence showed that it was mediated by more effortful processing of the negative stimuli by OA than YA [46]. On the other hand, a negative relationship between cognitive capacity and OA memory positivity runs contrary to evidence that OA with higher scores on tests of cognitive control showed stronger positivity effects in memory tasks than those with lower scores [16].…”

Linking resting‐state networks and social cognition in schizophrenia and bipolar disorder

“…This may be due to the fact that the empirical link between DMN and social cognition is mainly based on task-based fMRI studies (e.g., Mahy et al, 2014;Santos et al, 2016;Schilbach et al, 2008), as opposed to resting state as used here. This may be due to the fact that the empirical link between DMN and social cognition is mainly based on task-based fMRI studies (e.g., Mahy et al, 2014;Santos et al, 2016;Schilbach et al, 2008), as opposed to resting state as used here.…”

“…Functional connectivity analysis of resting-state functional magnetic resonance imaging (rsfMRI) offers insight into the intrinsic activity of these networks, and allows for examination of their relationship to social cognitive performance (Doruyter, Dupont, Stein, & Warwick, 2017). For recent topical reviews, see (e.g., Eisenberger, 2013;Jankowski & Takahashi, 2014;Mahy, Moses, & Pfeifer, 2014;Rotge et al, 2015;Santos, Almeida, Oliveiros, & Castelo-Branco, 2016). For recent topical reviews, see (e.g., Eisenberger, 2013;Jankowski & Takahashi, 2014;Mahy, Moses, & Pfeifer, 2014;Rotge et al, 2015;Santos, Almeida, Oliveiros, & Castelo-Branco, 2016).…”

Approach or avoidance: Neural correlates of intelligence evaluation from faces

“…Positive face evaluations corresponded to regular activation in the mOFC, caudate nucleus, anterior insula, inferior frontal gyrus, thalamus, and anterior cingulate cortex: areas largely overlapping with reward‐related regions (Liu, Hairston, Schrier, & Fan, ; Sescousse, Caldú, Segura, & Dreher, ). However, another meta‐analysis on facial trustworthiness reported that the thalamus and the insula exhibited a negative correlation with facial trustworthiness (Santos, Almeida, Oliveiros, & Castelo‐Branco, ). Recent studies have further shown that activity in the amygdala depended on face atypicality (i.e., the degree of difference between the presented face and average faces in terms of facial structure), regardless of the presented face's social meaning (Mattavelli, Andrews, Asghar, Towler, & Young, ; Said, Dotsch, & Todorov, ).…”