Abstract
Understanding emotion is critical for a science of healthy and disordered brain function, but the neurophysiological basis of emotional experience is still poorly understood. We analyzed human brain activity patterns from 148 studies of emotion categories (2159 total participants) using a novel hierarchical Bayesian model. The model allowed us to classify which of five categories—fear, anger, disgust, sadness, or happiness—is engaged by a study with 66% accuracy (43-86% across categories). Analyses of the activity patterns encoded in the model revealed that each emotion category is associated with unique, prototypical patterns of activity across multiple brain systems including the cortex, thalamus, amygdala, and other structures. The results indicate that emotion categories are not contained within any one region or system, but are represented as configurations across multiple brain networks. The model provides a precise summary of the prototypical patterns for each emotion category, and demonstrates that a sufficient characterization of emotion categories relies on (a) differential patterns of involvement in neocortical systems that differ between humans and other species, and (b) distinctive patterns of cortical-subcortical interactions. Thus, these findings are incompatible with several contemporary theories of emotion, including those that emphasize emotion-dedicated brain systems and those that propose emotion is localized primarily in subcortical activity. They are consistent with componential and constructionist views, which propose that emotions are differentiated by a combination of perceptual, mnemonic, prospective, and motivational elements. Such brain-based models of emotion provide a foundation for new translational and clinical approaches.
Highlights
Emotions are at the center of human life
We investigate the anatomical nature of the patterns that are diagnostic of emotion categories, and find that they are distributed across many brain systems associated with diverse cognitive, perceptual, and motor functions
Among other systems, information diagnostic of emotion category was found in both large, multi-functional cortical networks and in the thalamus, a small region composed of functionally dedicated sub-nuclei
Summary
Emotions play a crucial role in forging and maintaining social relationships, which is a major adaptation of our species. They are central in the diagnosis and treatment of virtually every mental disorder [1]. The autonomic and neuroendocrine changes that accompany emotional episodes may play an important role in physical health via peripheral gene expression and other pathways (e.g., [2]) Because of their broad relevance, developing models of brain function to characterize and predict emotional experience is of paramount importance in the study of health and behavior. A specific emotion category, like fear, can involve a range of behaviors, including freezing, flight, aggression, as well as complex social interactions. In spite of groundbreaking advances in understanding the circuitry underlying basic behavioral adaptations for safety and reproduction (including ‘threat’ behaviors; [11]), there is no comprehensive model of the neurophysiological basis of emotional experience in humans
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