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National Academy of Sciences, Proceedings of the National Academy of Sciences, 24(109), p. 9599-9604, 2012

DOI: 10.1073/pnas.1206095109

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Emotions promote social interaction by synchronizing brain activity across individuals

This paper is made freely available by the publisher.
This paper is made freely available by the publisher.

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Abstract

Sharing others' emotional states may facilitate understanding their intentions and actions. Here we show that networks of brain areas "tick together" in participants who are viewing similar emo-tional events in a movie. Participants' brain activity was measured with functional MRI while they watched movies depicting unpleas-ant, neutral, and pleasant emotions. After scanning, participants watched the movies again and continuously rated their experience of pleasantness–unpleasantness (i.e., valence) and of arousal–calm-ness. Pearson's correlation coefficient was used to derive multisub-ject voxelwise similarity measures [intersubject correlations (ISCs)] of functional MRI data. Valence and arousal time series were used to predict the moment-to-moment ISCs computed using a 17-s mov-ing average. During movie viewing, participants' brain activity was synchronized in lower-and higher-order sensory areas and in cor-ticolimbic emotion circuits. Negative valence was associated with increased ISC in the emotion-processing network (thalamus, ven-tral striatum, insula) and in the default-mode network (precuneus, temporoparietal junction, medial prefrontal cortex, posterior supe-rior temporal sulcus). High arousal was associated with increased ISC in the somatosensory cortices and visual and dorsal attention networks comprising the visual cortex, bilateral intraparietal sulci, and frontal eye fields. Seed-voxel–based correlation analysis con-firmed that these sets of regions constitute dissociable, functional networks. We propose that negative valence synchronizes individ-uals' brain areas supporting emotional sensations and understand-ing of another's actions, whereas high arousal directs individuals' attention to similar features of the environment. By enhancing the synchrony of brain activity across individuals, emotions may pro-mote social interaction and facilitate interpersonal understanding. synchronization | feeling | empathy | somatosensation H uman emotions are highly contagious. Feelings of anger and hatred may spread rapidly throughout a peaceful protest demonstration and turn it into a violent riot, whereas intense feelings of excitement and joy can sweep promptly from players to spectators in an ever-so-important football final. It is well docu-mented that observation of others in a particular emotional state rapidly and automatically triggers the corresponding behavioral and physiological representation of that emotional state in the observer (1–3). Neuroimaging studies also have revealed com-mon neural activation for perception and experience of states such as pain (4–6), disgust (7), and pleasure (8). This automated mapping of others' emotional states in one's own body and brain has been proposed to support social interaction via contextual understanding: Sharing others' emotional states provides the observers with a somatosensory framework that facilitates un-derstanding their intentions and actions and allows the observers to "tune in" or "sync" with other individuals (9–11). Recent evidence suggests that during social situations, such synchronization of two individuals' brain activity actually may occur in the literal sense. Prolonged natural stimulation, such as viewing a movie or listening to a narrative, results in time-locked and functionally selective response time courses (i.e., intersubject correlation, ISC) in a multitude of brain areas. This synchroni-zation of brain activity extends from the early projection cortices to areas involved in higher-order vision and attention and has been interpreted as reflecting similarity of cerebral information processing across individuals (12–16). In addition to reflecting sensory-driven neuronal responses, synchronized neural activity also could facilitate humans in assuming the mental and bodily perspectives of others and predicting their actions (17). Indeed, speaker–listener neural synchronization is associated with suc-cessful comprehension of a verbal message (18), and communi-cation by hand gestures (19) and facial expressions (20) enhances neural synchronization between the communicating persons in a brain-region–selective manner. Because emotions make individ-uals to feel, act, and view the world in a similar fashion (9), emotion-dependent ISC in the limbic emotion systems, as well as in the networks supporting visual attention and simulating others' mental states, could form a crucial mechanism to facilitate in-terpersonal understanding during emotionally intense events. In the present study, we used ISC analysis to test whether emotions triggered by affect-laden events in movies are associ-ated with synchronization of viewers' brain activity. Rather than studying how emotions flow from one brain to another (e.g., ref 20), we focused on the tendency for emotional brain responses to become synchronized across the members of a group exposed to similar emotional events (21). Participants watched a set of un-pleasant, neutral, and pleasant movies while their brain activity was measured with functional MRI (fMRI) (Fig. 1). After scanning, the participants viewed the movies again and evaluated online their subjective experiences of valence (pleasantness– unpleasantness) and arousal (calmness–activation). These va-lence and arousal time series then were used in the general linear model (GLM) to predict moment-to-moment ISC of brain ac-tivity during movie viewing. We demonstrate that emotions are associated with enhanced intersubject synchronization that extends beyond the sensory cortices to the limbic system and to visual attention and mental simulation networks. We propose that such synchronization of brain activation during emotional encounters supports enhanced contextual understanding across individuals.