Should perception of emotions be classified according to threat detection rather than emotional valence? An updated meta-analysis for a whole-brain atlas of emotional faces processing

Abstract

Background: Human navigation of social interactions relies on the processing of emotion on faces. This meta-analysis aimed to produce an updated brain atlas of emotional face processing from whole-brain studies based on a single emotional face-viewing paradigm (PROSPERO CRD42022251548).

Methods: We conducted a systematic literature search of Embase, MEDLINE and PsycINFO from May 2008 to October 2021. We used seed-based d mapping with permutation of subject images to conduct a quantitative meta-analysis of functional neuroimaging contrasts between emotional (e.g., angry, happy) and neutral faces. We conducted agglomerative hierarchical clustering of meta-analytic map contrasts of emotional faces relative to neutral faces. We investigated lateralization of emotional face processing.

Results: From 5549 studies identified, 55 data sets (1489 healthy participants) met our inclusion criteria. Relative to neutral faces, we found extensive activation clusters by fearful faces in the right inferior temporal gyrus, right fusiform area, left putamen and amygdala, right parahippocampalgyrus and cerebellum; we found smaller activation clusters by angry faces in the right cerebellum and right middle temporal gyrus (MTG) and by disgusted faces in the left MTG. Happy and sad faces did not reach statistical significance. Clustering analyses showed similar activation patterns of fearful and angry faces; activation patterns of happy and sad faces showed the least correlation with other emotional faces. Emotional face processing was predominantly left-lateralized in the amygdala and anterior insula, and right-lateralized in the ventromedial prefrontal cortex.

Limitations: Reliance on discretized effect sizes based on peak coordinate location instead of statistical brain maps, and the varying level of statistical threshold reporting from original studies, could lead to underdetection of smaller clusters of activation.

Conclusion: Processing of emotional faces appeared to be oriented toward identifying threats on faces, from highest (i.e., angry or fearful faces) to lowest level (i.e., happy or sad faces), with a more complex lateralization pattern than previously theorized. Emotional faces may be processed in latent grouping but organized by threat content rather than emotional valence.

Figure 1

Preferred Reporting Items for Systematic Review and Meta-Analysis (PRISMA) flow diagram of study selection, obtained from http://www.prisma-statement.org/PRISMAStatement/FlowDiagram.

Figure 2

(A) Meta-analytic activation clusters in each emotional face category, contrasted with neutral faces (activation clusters for fearful, angry and disgusted faces were significant at p_FWE = 0.05; clusters for happy faces were significant at p = 0.005, uncorrected). (B) Meta-analytic maps and clustering dendrogram showed that fearful and angry faces were most similar among other emotional categories. (C) Meta-analytic grouping of negative emotions (i.e., fearful, angry, disgusted and sad faces), and of threatening faces (i.e., fearful and angry faces), contrasted with neutral faces. FFA = fusiform face area; IFG = inferior frontal gyrus; ITG = inferior temporal gyrus; MOG = middle occipital gyrus; MTG = middle temporal gyrus; PHG = parahippocampal gyrus; SFG = superior frontal gyrus; STG = superior temporal gyrus.

Figure 3

Hemispheric laterality of brain activation in the (A) amygdala, (B) anterior insula and (C) ventromedial prefrontal cortex (vmPFC). The laterality index approaches −1 (blue) when it is left-lateralized and approaches 1 (red) when it is right-lateralized. L = left hemisphere; R = right hemisphere.