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

Steve Lukito*, Lydia Fortea, Federica Groppi, Ksenia Zuzanna Wykret, Eleonora Tosi, Vincenzo Oliva, Stefano Damiani, Joaquim Radua, Paolo Fusar-Poli

*Corresponding author for this work

Research output: Contribution to journalReview articlepeer-review

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Abstract

Background: Human navigation of social interactions relies on the processing of emotion on faces. Previous theories of emotional processing on human faces were based on a mixture of studies of emotional experiences during observation of emotional scenes and perception of emotional faces, which have led to a variety of views. This meta-analysis aimed to produce an updated brain atlas of emotional face processing of whole-brain studies based on a single emotional face viewing paradigm and to contribute to the theorization of emotional face processing in human (PROSPERO CRD42022251548).

Methods: A systematic literature search using the databases EMBASE, MEDLINE, and APA PsycINFO took place from May 2008 to October 2021. Seed-based d mapping with permutation of subject images quantitatively voxel-based meta-analyzed functional neuroimaging contrasts between emotional (e.g., angry, happy) and neutral faces. Agglomerative hierarchical clustering of meta-analytic map contrasts of emotional relative to neutral faces examined the processing similarity across emotions. Lateralization of emotional face processing was examined in amygdala, anterior insula, and ventromedial prefrontal cortex (vmPFC) regions.

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

Conclusion: Processing of emotional faces in the human brain appeared to be oriented towards identifying threats on the faces, from the highest (i.e., angry or fearful faces) to the lowest level (i.e., happy or sad faces), with a more complex lateralization pattern than previously theorized. Emotional faces may thus be processed in latent grouping but organized by threat content rather than emotional valence.
Original languageEnglish
JournalJournal of Psychiatry and Neuroscience
Publication statusAccepted/In press - 1 Aug 2023

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