Temporal Dynamics of Natural Static Emotional Facial Expressions Decoding: A Study Using Event- and Eye Fixation-Related Potentials

Anne Guérin-Dugué, Raphaëlle N. Roy, Emmanuelle Kristensen, Bertrand Rivet, Laurent Vercueil, Anna Tcherkassof

This study aims at examining the precise temporal dynamics of the emotional facial decoding as it unfolds in the brain, according to the emotions displayed. To characterize this processing as it occurs in ecological settings, we focused on unconstrained visual explorations of natural emotional faces (i.e., free eye movements). The General Linear Model (GLM; Smith and Kutas, 2015a,b; Kristensen et al., 2017a) enables such a depiction. It allows deconvolving adjacent overlapping responses of the eye fixation-related potentials (EFRPs) elicited by the subsequent fixations and the event-related potentials (ERPs) elicited at the stimuli onset. Nineteen participants were displayed with spontaneous static facial expressions of emotions (Neutral, Disgust, Surprise, and Happiness) from the DynEmo database (Tcherkassof et al., 2013). Behavioral results on participants' eye movements show that the usual diagnostic features in emotional decoding (eyes for negative facial displays and mouth for positive ones) are consistent with the literature. The impact of emotional category on both the ERPs and the EFRPs elicited by the free exploration of the emotional faces is observed upon the temporal dynamics of the emotional facial expression processing. Regarding the ERP at stimulus onset, there is a significant emotion-dependent modulation of the P2-P3 complex and LPP components' amplitude at the left frontal site for the ERPs computed by averaging. Yet, the GLM reveals the impact of subsequent fixations on the ERPs time-locked on stimulus onset. Results are also in line with the valence hypothesis. The observed differences between the two estimation methods (Average vs. GLM) suggest the predominance of the right hemisphere at the stimulus onset and the implication of the left hemisphere in the processing of the information encoded by subsequent fixations. Concerning the first EFRP, the Lambda response and the P2 component are modulated by the emotion of surprise compared to the neutral emotion, suggesting an impact of high-level factors, in parieto-occipital sites. Moreover, no difference is observed on the second and subsequent EFRP. Taken together, the results stress the significant gain obtained in analyzing the EFRPs using the GLM method and pave the way toward efficient ecological emotional dynamic stimuli analyses.