Temporal and spatial neural dynamics in the perception of basic emotions from complex scenes

Abstract

The different temporal dynamics of emotions are critical to understand their evolutionary role in the regulation of interactions with the surrounding environment. Here, we investigated the temporal dynamics underlying the perception of four basic emotions from complex scenes varying in valence and arousal (fear, disgust, happiness and sadness) with the millisecond time resolution of Electroencephalography (EEG). Event-related potentials were computed and each emotion showed a specific temporal profile, as revealed by distinct time segments of significant differences from the neutral scenes. Fear perception elicited significant activity at the earliest time segments, followed by disgust, happiness and sadness. Moreover, fear, disgust and happiness were characterized by two time segments of significant activity, whereas sadness showed only one long-latency time segment of activity. Multidimensional scaling was used to assess the correspondence between neural temporal dynamics and the subjective experience elicited by the four emotions in a subsequent behavioral task. We found a high coherence between these two classes of data, indicating that psychological categories defining emotions have a close correspondence at the brain level in terms of neural temporal dynamics. Finally, we localized the brain regions of time-dependent activity for each emotion and time segment with the low-resolution brain electromagnetic tomography. Fear and disgust showed widely distributed activations, predominantly in the right hemisphere. Happiness activated a number of areas mostly in the left hemisphere, whereas sadness showed a limited number of active areas at late latency. The present findings indicate that the neural signature of basic emotions can emerge as the byproduct of dynamic spatiotemporal brain networks as investigated with millisecond-range resolution, rather than in time-independent areas involved uniquely in the processing one specific emotion.