EEG alpha band functional connectivity reveals distinct cortical dynamics for overt and covert emotional face processing.

Current knowledge regarding how the focus of our attention during face processing influences neural responses largely comes from neuroimaging studies reporting on regional brain activations. The present study was designed to add novel insights to this research by studying how attention can differentially impact the way cortical regions interact during emotional face processing. High-density electroencephalogram was recorded in a sample of fifty-two healthy participants during an emotional face processing task. The task required participants to either attend to the expressions (i.e., overt processing) or attend to a perceptual distractor, which rendered the expressions task-irrelevant (i.e., covert processing). Functional connectivity in the alpha band was estimated in source space and modeled using graph theory to quantify whole-brain integration and segregation. Results revealed that overt processing of facial expressions is linked to reduced cortical segregation and increased cortical integration, this latter specifically for negative expressions of fear and sadness. Furthermore, we observed increased communication efficiency during overt processing of negative expressions between the core and the extended face processing systems. Overall, these findings reveal that attention makes the interaction among the nodes involved in face processing more efficient, also uncovering a connectivity signature of the prioritized processing mechanism of negative expressions, that is an increased cross-communication within the nodes of the face processing network.

Spatiotemporal Dynamics of Covert vs. Overt Emotional Face Processing in Dysphoria.

People at risk of developing clinical depression exhibit attentional biases for emotional faces. To clarify whether such effects occur at an early, automatic, or at a late, deliberate processing stage of emotional processing, the present study used high-density electroencephalography during both covert and overt processing of sad, fearful, happy, and neutral expressions in healthy participants with high dysphoria (n = 16) and with low dysphoria (n = 19). A state-of-the-art non-parametric permutation-based statistical approach was then used to explore the effects of emotion, attentional task demands, and group. Behaviorally, participants responded faster and more accurately when overtly categorizing happy faces and they were slower and less accurate when categorizing sad and fearful faces, independent of the dysphoria group. Electrophysiologically, in an early time-window (N170: 140-180 ms), there was a significant main effect for the dysphoria group, with greater negative voltage for the high vs. low dysphoria group over the left-sided temporo-occipital scalp. Furthermore, there was a significant group by emotional interaction, with the high dysphoria group displaying greater negative amplitude N170 for happy than fearful faces. Attentional task demands did not influence such early effects. In contrast, in an intermediate time-window (EPN: 200-400 ms) and in a late time-window (LPP: 500-750 ms) there were no significant main effects nor interactions involving the dysphoria Group. The LPP results paralleled the behavioral results, with greater LPP voltages for sad and fearful relative to happy faces only in the overt task, but similarly so in the two dysphoria groups. This study provides novel evidence that alterations in face processing in dysphoric individuals can be seen at the early stages of face perception, as indexed by the N170, although not in the form of a typical pattern of mood-congruent attentional bias. In contrast, intermediate (EPN) and late (LPP) stages of emotional face processing appear unaffected by dysphoria. Importantly, the early dysphoria effect appears to be independent of the top-down allocation of attention, further supporting the idea that dysphoria may influence a stage of automatic emotional appraisal. It is proposed that it may be a consequence of a shift from holistic to feature-based processing of facial expressions, or may be due to the influence of negative schemas acting as a negative context for emotional facial processing.

Spatiotemporal Dynamics of Covert Versus Overt Processing of Happy, Fearful and Sad Facial Expressions.

Behavioral and electrophysiological correlates of the influence of task demands on the processing of happy, sad, and fearful expressions were investigated in a within-subjects study that compared a perceptual distraction condition with task-irrelevant faces (e.g., covert emotion task) to an emotion task-relevant categorization condition (e.g., overt emotion task). A state-of-the-art non-parametric mass univariate analysis method was used to address the limitations of previous studies. Behaviorally, participants responded faster to overtly categorized happy faces and were slower and less accurate to categorize sad and fearful faces; there were no behavioral differences in the covert task. Event-related potential (ERP) responses to the emotional expressions included the N170 (140-180 ms), which was enhanced by emotion irrespective of task, with happy and sad expressions eliciting greater amplitudes than neutral expressions. EPN (200-400 ms) amplitude was modulated by task, with greater voltages in the overt condition, and by emotion, however, there was no interaction of emotion and task. ERP activity was modulated by emotion as a function of task only at a late processing stage, which included the LPP (500-800 ms), with fearful and sad faces showing greater amplitude enhancements than happy faces. This study reveals that affective content does not necessarily require attention in the early stages of face processing, supporting recent evidence that the core and extended parts of the face processing system act in parallel, rather than serially. The role of voluntary attention starts at an intermediate stage, and fully modulates the response to emotional content in the final stage of processing.