Emotional face processing and attention performance in three domains: neurophysiological mechanisms and moderating effects of trait anxiety.

The rapid processing of emotional information adaptively regulates the allocation of attention, but may also divert resources away from attention performance, particularly for those showing elevated anxiety. The temporal organization of rapid emotional processing and its implications for attention performance, however, remain unclear. Participants were 18 healthy adults (12 females) who reported on trait anxiety. Tasks-irrelevant fearful, sad, and neutral faces were presented for 50 ms prior to each trial of a cued attention task measuring alerting, orienting, and executive attention. Electroencephalographic recordings were made from 64 scalp electrodes to generate event-related potentials (ERPs) to faces. Emotional face type and trait anxiety modulated ERP responses at three early stages around 200 ms, 250 ms, and 320 ms. Although behavioral findings showed enhanced orienting and executive attention following presentation of fearful and sad faces, the degree to which these faces modulated ERP responses, particularly around 250 ms, interfered with orienting and executive attention in the high trait anxiety group, and enhanced alerting in the low trait anxiety group. Results are discussed in terms of mechanisms in the emotional capture of attention and implications for understanding attentional processes in anxiety.     

Emotional Face Processing and Emotion Regulation in Children: An ERP Study

Emotion regulation is a critical component of healthy development, yet few studies examine neural correlates of emotion regulation in childhood. In the present study, we assessed whether children's neurophysiological responses to salient and socially significant emotional distracters—emotional faces—were related to broader emotion regulation capacities. Emotion regulation was measured as attention performance following emotional distracters and as maternal report of child emotional dysregulation. Electroencephalography was recorded while participants (15 children aged 5–9) performed an attention task. Scalp-recorded event related potentials (ERPs) were time-locked to emotional distracters (fearful, sad, and neutral faces) and reflected a range of rapid attentional and face processing operations (P1, N1, N170, and Nc). P1 latencies were faster whereas N1 amplitudes were reduced to fearful compared to sad faces. Larger P1 and Nc amplitudes to fearful and sad faces were correlated with more effective emotion regulation. Results are discussed in terms of mechanisms in emotion regulation and the use of ERPs to detect early risk for psychopathology and inform intervention efforts.     

Attentional capture by task-irrelevant fearful faces is revealed by the N2pc component

We measured the N2pc component as an electrophysiological indicator of attentional selection to investigate whether fearful faces can attract attention even when they are entirely task-irrelevant and attention is focused on another demanding visual monitoring task. Participants had to detect infrequent luminance changes of the fixation cross, while ignoring stimulus arrays containing a face singleton (a fearful face among neutral faces, or neutral face among fearful faces) to the left or right of fixation. On trials without a target luminance change, an N2pc was elicited by fearful faces presented next to fixation, irrespective of whether they were singletons or not, demonstrating that irrelevant fearful faces can bias the spatial distribution of attention. The N2pc to fearful faces was attenuated when face arrays were presented simultaneously with a target luminance change, suggesting that concurrent target processing reduces attentional capture by emotional salient events.     

Differential modulations of reward expectation on implicit facial emotion processing: ERP evidence

Implicit emotional processing refers to the preferential processing of emotional content even if it is task irrelevant. Given that motivation enhances executive control by biasing attentional resources toward target stimuli, here we investigated the effects of reward expectation on implicit facial emotional processing in two experiments using ERPs. A precue signaling additional monetary reward for fast and accurate response for the upcoming trial (incentive condition; relative to a cue indicating no such additional reward, i.e., nonincentive condition) was followed by the presentation of a happy, angry, or neutral face. Participants had to determine the gender of the face in Experiment 1 and decide whether a number superimposed on the face was even or odd in Experiment 2. In both experiments, incentive cues elicited larger P3 and contingent negative variation responses, and the targets following incentive cues elicited more positive‐going ERPs (200–700 ms), compared with the nonincentive condition. Importantly, the N2 responses (200–280 ms) to the target exhibited differential patterns of Reward × Emotion interaction: relative to the nonincentive condition, the N2 amplitude differences between emotional (i.e., happy and/or angry) and neutral faces increased in the incentive condition in Experiment 1, but diminished in Experiment 2. These results indicate that reward expectation can differentially modulate implicit processing of facial expressions, with increased sensitivity to emotions when the processing of whole faces is required, but with reduced sensitivity when the processing of faces is distractive. This study enriches the evidence for interactions between reward‐related executive control and implicit emotional processing.     

ERPs reveal subliminal processing of fearful faces

To investigate whether facial expression is processed in the absence of conscious awareness, ERPs were recorded in a task in which participants had to identify the expression of masked fearful and neutral target faces. On supraliminal trials (200 ms target duration), in which identification performance was high, a sustained positivity to fearful versus neutral target faces started 140 ms after target face onset. On subliminal trials (8 ms target duration), identification performance was at chance level, but ERPs still showed systematic fear-specific effects. An early positivity to fearful target faces was present but smaller than on supraliminal trials. A subsequent enhanced N2 to fearful faces was only present for subliminal trials. In contrast, a P3 enhancement to fearful faces was observed on supraliminal but not subliminal trials. Results demonstrate rapid emotional expression processing in the absence of awareness.     

Attention modulates the processing of emotional expression triggered by foveal faces

To investigate whether the processing of emotional expression for faces presented within foveal vision is modulated by spatial attention, event-related potentials (ERPs) were recorded in response to stimulus arrays containing one fearful or neutral face at fixation, which was flanked by a pair of peripheral bilateral lines. When attention was focused on the central face, an enhanced positivity was elicited by fearful as compared to neutral faces. This effect started at 160 ms post-stimulus, and remained present for the remainder of the 700 ms analysis interval. When attention was directed away from the face towards the line pair, the initial phase of this emotional positivity remained present, but emotional expression effects beyond 220 ms post-stimulus were completely eliminated. These results demonstrate that when faces are presented foveally, the initial rapid stage of emotional expression processing is unaffected by attention. In contrast, attentional task instructions are effective in inhibiting later, more controlled stages of expression analysis.     

The spatial frequency spectrum of fearful faces modulates early and mid-latency ERPs but not the N170

Prioritized processing of fearful compared to neutral faces is reflected in behavioral advantages such as lower detection thresholds, but also in enhanced early and late event-related potentials (ERPs). Behavioral advantages have recently been associated with the spatial frequency spectrum of fearful faces, better fitting the human contrast sensitivity function than the spectrum of neutral faces. However, it is unclear whether and to which extent early and late ERP differences are due to low-level spatial frequency spectrum information or high-level representations of the facial expression. In this pre-registered EEG study (N = 38), the effects of fearful-specific spatial frequencies on event-related ERPs were investigated by presenting faces with fearful and neutral expressions whose spatial frequency spectra were manipulated so as to contain either the average power spectra of neutral, fearful, or both expressions combined. We found an enlarged N170 to fearful versus neutral faces, not interacting with spatial frequency. Interactions of emotional expression and spatial frequencies were observed for the P1 and Early Posterior Negativity (EPN). For both components, larger emotion differences were observed when the spectrum contained neutral as opposed to fearful frequencies. Importantly, for the EPN, fearful and neutral expressions did not differ anymore when inserting fearful frequencies into neutral expressions, whereas typical emotion differences were found when faces contained average or neutral frequencies. Our findings show that N170 emotional modulations are unaffected by expression-specific spatial frequencies. However, expression-specific spatial frequencies alter early and mid-latency ERPs. Most notably, the EPN to neutral expressions is boosted by adding fearful spectra—but not vice versa.     

Anxiety and orienting of gaze to angry and fearful faces

Neuroscience research indicates that individual differences in anxiety may be attributable to a neural system for threat-processing, involving the amygdala, which modulates attentional vigilance, and which is more sensitive to fearful than angry faces. Complementary cognitive studies indicate that high-anxious individuals show enhanced visuospatial orienting towards angry faces, but it is unclear whether fearful faces elicit a similar attentional bias. This study compared biases in initial orienting of gaze to fearful and angry faces, which varied in emotional intensity, in high- and low-anxious individuals. Gaze was monitored whilst participants viewed a series of face-pairs. Results showed that fearful and angry faces elicited similar attentional biases. High-anxious individuals were more likely to direct gaze at intense negative facial expressions, than low-anxious individuals, whereas the groups did not differ in orienting to mild negative expressions. Implications of the findings for research into the neural and cognitive bases of emotion processing are discussed.     

P3b reflects maltreated children's reactions to facial displays of emotion

Processing of emotion information by maltreated and control children was assessed with event-related brain potentials (ERPs). Maltreated children, for whom negative facial displays may be especially salient, and demographically comparable peers were tested to increase knowledge of differential processing of emotion information. ERPs were measured while children responded to pictures depicting facial displays of anger, fear, and happiness. Maltreated children showed larger P3b amplitude when angry faces appeared as targets than did control children; the two groups did not differ when targets were either happy or fearful facial expressions or for nontargets of any emotional content. These results indicate that aberrant emotional experiences associated with maltreatment may alter the allocation of attention and sensitivity that children develop to process specific emotion information.     

The effect of emotionally valenced eye region images on visuocortical processing of surprised faces

In this study, we presented pictorial representations of happy, neutral, and fearful expressions projected in the eye regions to determine whether the eye region alone is sufficient to produce a context effect. Participants were asked to judge the valence of surprised faces that had been preceded by a picture of an eye region. Behavioral results showed that affective ratings of surprised faces were context dependent. Prime‐related ERPs with presentation of happy eyes elicited a larger P1 than those for neutral and fearful eyes, likely due to the recognition advantage provided by a happy expression. Target‐related ERPs showed that surprised faces in the context of fearful and happy eyes elicited dramatically larger C1 than those in the neutral context, which reflected the modulation by predictions during the earliest stages of face processing. There were larger N170 with neutral and fearful eye contexts compared to the happy context, suggesting faces were being integrated with contextual threat information. The P3 component exhibited enhanced brain activity in response to faces preceded by happy and fearful eyes compared with neutral eyes, indicating motivated attention processing may be involved at this stage. Altogether, these results indicate for the first time that the influence of isolated eye regions on the perception of surprised faces involves preferential processing at the early stages and elaborate processing at the late stages. Moreover, higher cognitive processes such as predictions and attention can modulate face processing from the earliest stages in a top‐down manner.     

Fearful faces grab attention in the absence of late affective cortical responses

Previous studies utilizing the N2pc, an ERP correlate of attentional focusing, demonstrated that fearful faces grab attention regardless of their relevance to the current task. We tested whether this apparent automaticity was susceptible to high concurrent task demand, which is known to suppress other cortical and subcortical emotional evaluations. Our data revealed that the affective attentional capture occurred even under high task load, by which the late cortical affective activity (the LPP modulation) was entirely suppressed. We also confirmed that this effect did not occur to inverted faces and therefore required a holistic perception of facial expression. These results show that, given an intact processing of facial expression, attention is attracted by fearful faces in a relatively automatic fashion as compared to other cortical affective processes.     

Expectation decreases brain susceptibility to fearful stimuli: ERP evidence from a modified emotion evaluation task

Expectation decreased the susceptibility to fearful stimuli in prior studies using distracting tasks. The present study tests whether expectation remains effective in decreasing this susceptibility, when subjects focus attention on emotional properties. Event-related potentials were recorded for fearful and neutral faces, while subjects performed a modified emotion evaluation task during unpredictable and predictable conditions. Behavioral data showed faster response latencies during predictable versus unpredictable conditions. ERP data showed prolonged peak latencies in N1 (80–130 ms) and larger amplitudes in P2 (130–180 ms) and N200-300 components, for unpredictable fearful versus neutral faces. Conversely, all these components showed similar responses to predictable fearful and neutral faces. Source analysis suggested that medial temporal lobe mediated ERPs elicited by unpredictable fearful faces, while ventromedial prefrontal cortex mediated those elicited by predictable fearful faces, in the 130–180 ms interval. Thus, we propose emotional expectation as a cognitive regulation strategy that reliably dampens human susceptibility to fearful stimuli.     

Trait anxiety and conflict monitoring following threat: An ERP study

Threat-related attentional disruptions in anxiety may relate to changes in cognitive control during task processing. The present study examined this question using the N2 event-related brain potential. It was predicted that threat stimuli will selectively influence the N2 for those showing elevated trait anxiety and that reduced N2 may reflect a compensatory process predicting better attention performance. EEG was recorded while 36 participants completed a cued flanker task with threat or nonthreat distracters. N2 amplitudes were greater to incongruent versus congruent flankers. Following threat, high trait anxious participants showed reduced modulation of the N2 by flanker type and greater N2 amplitudes to congruent flankers. Reduced N2 was associated with better attention performance. This study was among the first documenting the emotional modulation of the N2 related to the threat bias and its links with attention interference in anxiety.     

Effects of anxiety on the processing of fearful and happy faces: an event-related potential study

This study investigated the influence of trait anxiety on event-related potentials (ERPs) to fearful, happy, and neutral faces. Fearful faces, relative to neutral, elicited a range of effects in the low-trait anxiety (LTA) group: an enhanced visual P1 component, an early posterior negativity (EPN), and a sustained fronto-central positivity. Emotional expression effects were generally weaker for happy faces. The enhanced fronto-central positivity and EPN triggered by fearful stimuli in LTA participants were less pronounced in the high-trait anxiety (HTA) group, while the enhancement of the visual P1 seen in the LTA group was further augmented in the HTA group. This represents a clear dissociation across anxiety groups between rapid attentional processing as reflected by the visual P1 and later strategic processing as reflected by fronto-central and EPN components. These effects of high-trait anxiety in potentiating initial threat evaluation but attenuating later cognitive processing are discussed in the context of the possible roles of neural systems underlying threat evaluation, cognitive avoidance, and differentiated affective responses.     

Trait anxiety and involuntary processing of facial emotions

There is suggestion that trait anxiety influences the processing of threat-related information. To test this hypothesis we recorded ERPs in response to subliminally presented and backward masked fearful and neutral faces, and non-face objects, in the preselected low- and high-anxious individuals. The amplitude of N170 was found to be larger when elicited by faces in comparison to non-faces, however it was not found to be emotion-sensitive or modulated by anxiety level. Differences between low- and high-anxious individuals appeared in a time window of the P1 component. At later stages, within the EPN component, stronger negativity specific for fearful faces was recorded exclusively in the low-anxious participants. Our findings indicate that anxiety level modulates early stages of information processing, as reflected in the P1 component. This leads to anxiety-related differences in involuntary emotional expression detection at later stages (EPN component).     

You don’t like me,do you? Enhanced ERP responses to averted eye gaze in social anxiety

Social anxiety is associated with an attentional bias toward angry and fearful faces, along with an enhanced processing of faces per se. However, little is known about the processing of gaze direction, a subtle but important social cue. Participants with high or low social anxiety (HSA/LSA) observed eye pairs with direct or averted gaze while subjective ratings and event-related potentials (ERPs) were measured. Behaviorally, all participants rated averted gaze as more unpleasant than direct gaze. Neurally, only HSA participants showed a trend for higher P100 amplitudes to averted gaze and significantly enhanced processing at late latencies (Late positive potential [LPP]), indicative of a specific processing bias for averted gaze. Furthermore, HSA individuals showed enhanced processing of both direct and averted gaze relative to the LSA group at intermediate latencies (Early posterior negativity [EPN]). Both general and specific attentional biases play a role in social anxiety. Averted gaze - a potential sign of disinterest - deserves more attention in the attentional bias literature.     

Attentional modulations of event-related brain potentials sensitive to faces

Event-related brain potentials (ERPs) were recorded in response to centrally and peripherally presented faces and chairs under conditions where one stimulus category was attended and the other unattended. It was studied whether selective attention affects ERP components sensitive to the presence of faces. When compared with chairs, faces elicited larger N1 amplitudes at lateral temporal electrodes and a midline positivity in the same latency range. The latter effect was only found for central faces. Attention to centrally presented faces was reflected in enhanced posterior N1 amplitudes. This effect may be related to an attentional modulation of processing within face-specific brain areas. It was not elicited by chairs or peripheral faces. Beyond 200msec post-stimulus, a category-unspecific attentional negativity was found at all recording sites for centrally and peripherally presented face and nonface stimuli.     

Enhanced neural reactivity and selective attention to threat in anxiety

Attentional bias towards threat is implicated in the etiology and maintenance of anxiety disorders. We examined the neural correlates of threat bias in anxious and nonanxious participants to shed light on the neural chronometry of this cognitive bias. In this study, event-related potentials (ERPs) were recorded while anxious (n = 23) and nonanxious (n = 23) young adults performed a probe-discrimination task measuring attentional bias towards threat (angry) and positive (happy) face stimuli. Results showed an attention bias towards threat among anxious participants, but not among nonanxious participants. No bias to positive faces was found. ERP data revealed enhanced C1 amplitude (∼80 ms following threat onset) in anxious relative to nonanxious participants when cue displays contained threat faces. Additionally, P2 amplitude to the faces display was higher in the anxious relative to the nonanxious group regardless of emotion condition (angry/happy/neutral). None of the ERP analyses associated with target processing were significant. In conclusion, our data suggest that a core feature of threat processing in anxiety lies in functional perturbations of a brain circuitry that reacts rapidly and vigorously to threat. It is this over-activation that may set the stage for the attention bias towards threat observed in anxious individuals.     

ATTENTIONAL MODULATIONS OF EVENT-RELATED BRAIN POTENTIALS SENSITIVE TO FACES

Event-related brain potentials (ERPs) were recorded in response to centrally and peripherally presented faces and chairs under conditions where one stimulus category was attended and the other unattended. It was studied whether selective attention affects ERP components sensitive to the presence of faces. When compared with chairs, faces elicited larger N1 amplitudes at lateral temporal electrodes and a midline positivity in the same latency range. The latter effect was only found for central faces. Attention to centrally presented faces was reflected in enhanced posterior N1 amplitudes. This effect may be related to an attentional modulation of processing within face-specific brain areas. It was not elicited by chairs or peripheral faces. Beyond 200msec post-stimulus, a category-unspecific attentional negativity was found at all recording sites for centrally and peripherally presented face and nonface stimuli.     

The perception of fearful and happy facial expression is modulated by anxiety: an event-related potential study

Anxiety is supposed to interfere with cognitive and emotional processing and high level of trait-anxiety has been associated with an attentional bias for fearful faces, even in sub-clinical anxiety. On the basis of the Spielberger State and Trait Anxiety Inventory (STAI), twenty students were grouped as low vs. high anxious. Pictures from the Ekman and Friesen series were used in an event-related potentials study to investigate the neurophysiological correlates of the emotional processing of fear and happiness in sub-clinical anxiety. Subjects were confronted with a visual oddball design, in which they had to detect, as quickly as possible, deviant happy or fearful faces amongst a train of standard stimuli (neutral faces). Anxiety does not modify early perceptual (N100, P100, N170, VPP) or attentional (N2b) component, but later components are affected. Indeed, high anxious subjects are faster to detect deviant faces as suggested by earlier reaction times and P3b component. However, they show a reduced ability to process the emotional content of faces, this deficit being indexed by a decreased N300 component. Indeed, N300 is supposed to be particularly sensitive to affective features of stimuli rather than to physical characteristics. We propose that the earlier P3b observed in high anxious subjects could be interpreted as a way to overcome the deficient emotional appraisal by a more salient conscious processing.