Frontal and parietal EEG asymmetries interact to predict attentional bias to threat

Frontal and parietal electroencephalographic (EEG) asymmetries mark vulnerability to depression and anxiety. Drawing on cognitive theories of vulnerability, we hypothesise that cortical asymmetries predict attention to threat. Participants completed a dot-probe task in which bilateral face displays were followed by lateralised targets at either short (300 ms) or long (1050 ms) SOA. We also measured N2pc to face onset as an index of early attentional capture. At long SOA only, frontal and parietal asymmetry interacted to predict attentional bias to angry faces. Those with leftward frontal asymmetry showed no attentional bias. Among those with rightward frontal asymmetry those with low right parietal activity showed vigilance for threat, and those with high right parietal activity showed avoidance. Asymmetry was not related to the N2pc or to attentional bias at the short SOA. Findings suggest that trait asymmetries reflect function in a fronto-parietal network that controls attention to threat.     

Negative affectivity and EEG asymmetry interact to predict emotional interference on attention in early school-aged children

Negative affectivity (NA) is a broad construct that has been associated with the development of psychopathologies, such as anxiety, and with exaggerated attention to threatening stimuli. EEG asymmetry reflects biological individual differences in emotional reactivity that may underlie the association between NA and attention to threat. The present study included a sample of 31 five-seven year olds (M age in months = 74.39, SD = 6.57) to test the hypothesis that greater NA, combined with greater right anterior and posterior asymmetries, predicts increased attention interference following threat stimuli. Children completed an executive attention task which presented task-irrelevant threat (angry) and non-threat (neutral) faces prior to each trial. EEG asymmetry was measured at baseline for anterior, anterior-temporal and posterior scalp regions and child NA was measured via maternal report. As predicted, children showing greater NA and greater right anterior-temporal asymmetry showed more attention interference following angry faces. Additionally, two trend-level effects emerged: children showing greater NA and greater left anterior-temporal asymmetry showed less attention interference following angry faces, and children showing greater NA and greater left posterior asymmetry showed less attention interference, but only following neutral faces. Discussion focuses on the utility of using EEG asymmetry in the study of temperament, attentional biases, and the biological processes by which temperament confers risk for psychopathology.     

The influence of maternal anxiety and depression symptoms on fNIRS brain responses to emotional faces in 5- and 7-month-old infants

Greater relative right (versus left) frontal cortical activation to emotional faces as measured with alpha power in the electroencephalogram (EEG), has been considered a promising neural marker of increased vulnerability to psychopathology and emotional disorders. We set out to explore multichannel fNIRS as a tool to investigate infants’ frontal asymmetry responses (hypothesizing greater right versus left frontal cortex activation) to emotional faces as influenced by maternal anxiety and depression symptoms during the postnatal period. We also explored activation differences in fronto-temporal regions associated with facial emotion processing. Ninety-one typically developing 5- and 7-month-old infants were shown photographs of women portraying happy, fearful and angry expressions. Hemodynamic brain responses were analyzed over two frontopolar and seven bilateral cortical regions subdivided into frontal, temporal and parietal areas, defined by age-appropriate MRI templates. Infants of mothers reporting higher negative affect had greater oxyhemoglobin (oxyHb) activation across all emotions over the left inferior frontal gyrus, a region implicated in emotional communication. Follow-up analyses indicated that associations were driven by maternal depression, but not anxiety symptoms. Overall, we found no support for greater right versus left frontal cortex activation in association with maternal negative affect. Findings point to the potential utility of fNIRS as a method for identifying altered neural substrates associated with exposure to maternal depression in infancy.     

When does the brain distinguish between genuine and ambiguous smiles? An ERP study

Event-related brain potentials (ERPs) were recorded to assess the processing time course of ambiguous facial expressions with a smiling mouth but neutral, fearful, or angry eyes, in comparison with genuinely happy faces (a smile and happy eyes) and non-happy faces (neutral, fearful, or angry mouth and eyes). Participants judged whether the faces looked truly happy or not. Electroencephalographic recordings were made from 64 scalp electrodes to generate ERPs. The neural activation patterns showed early P200 sensitivity (differences between negative and positive or neutral expressions) and EPN sensitivity (differences between positive and neutral expressions) to emotional valence. In contrast, sensitivity to ambiguity (differences between genuine and ambiguous expressions) emerged only in later LPP components. Discrimination of emotional vs. neutral affect occurs between 180 and 430 ms from stimulus onset, whereas the detection and resolution of ambiguity takes place between 470 and 720 ms. In addition, while blended expressions involving a smile with angry eyes can be identified as not happy in the P200 (175–240 ms) component, smiles with fearful or neutral eyes produce the same ERP pattern as genuinely happy faces, thus revealing poor discrimination.     

Selective attention to angry faces in clinical social phobia

This study investigated the time course of attentional responses to emotional facial expressions in a clinical sample with social phobia. With a visual probe task, photographs of angry, happy, and neutral faces were presented at 2 exposure durations: 500 and 1250 ms. At 500 ms, the social phobia group showed enhanced vigilance for angry faces, relative to happy and neutral faces, in comparison with normal controls. In the 1250-ms condition, there were no significant attentional biases in the social phobia group. Results are consistent with a bias in initial orienting to threat cues in social anxiety. Findings are discussed in relation to recent cognitive models of anxiety disorders.     

Attentional bias to angry faces using the dot-probe task? It depends when you look for it

A number of studies using the dot-probe task now report the existence of an attentional bias to angry faces in participants who rate highly on scales of anxiety; however, no equivalent bias has been observed in non-anxious populations, despite evidence to the contrary from studies using other tasks. One reason for this discrepancy may be that researchers using the dot-probe task have rarely investigated any effects which might emerge earlier than 500 ms following presentation of the threat-related faces. Accordingly, in the current study we presented pairs of face stimuli with emotional and neutral expressions and probed the allocation of attention to these stimuli for presentation times of 100 and 500 ms. Results showed that at 100 ms there was an attentional bias towards the location of the relatively threatening stimulus (the angry face in angry/neutral pairs and the neutral face in neutral/happy pairs) and this pattern reversed by 500 ms. Comparisons of reaction time (RT) scores with an appropriate baseline suggested that the early bias toward threatening faces may actually arise through inhibition of the relatively least threatening member of a face pair rather than through facilitation of, or vigilance towards, the more threatening stimulus. However the mechanisms governing the observed biases are interpreted, these data provide evidence that probing for the location of spatial attention at 500 ms is not necessarily indicative of the initial allocation of attention between competing emotional facial stimuli.     

Memory for Angry Faces,Impulsivity, and Problematic Behavior in Adolescence

Research has shown that cognitive processes like the attribution of hostile intention or angry emotion to others contribute to the development and maintenance of conduct problems. However, the role of memory has been understudied in comparison with attribution biases. The aim of this study was thus to test if a memory bias for angry faces was related to conduct problems in youth. Adolescents from a junior secondary school were presented with angry and happy faces and were later asked to recognize the same faces with a neutral expression. They also completed an impulsivity questionnaire. A teacher assessed their behavior. The results showed that a better recognition of angry faces than happy faces predicted conduct problems and hyperactivity/inattention as reported by the teacher. The memory bias effect was more pronounced for impulsive adolescents. It is suggested that a memory bias for angry faces favors disruptive behavior but that a good ability to control impulses may moderate the negative impact of this bias.     

More than just another face in the crowd: superior detection of threatening facial expressions in children and adults

Threatening facial expressions can signal the approach of someone or something potentially dangerous. Past research has established that adults have an attentional bias for angry faces, visually detecting their presence more quickly than happy or neutral faces. Two new findings are reported here. First, evidence is presented that young children share this attentional bias. In five experiments, young children and adults were asked to find a picture of a target face among an array of eight distracter faces. Both age groups detected threat‐relevant faces – angry and frightened – more rapidly than non‐threat‐relevant faces (happy and sad). Second, evidence is presented that both adults and children have an attentional bias for negative stimuli overall. All negative faces were detected more quickly than positive ones in both age groups. As the first evidence that young children exhibit the same superior detection of threatening facial expressions as adults, this research provides important support for the existence of an evolved attentional bias for threatening stimuli.     

Memory-based attentional biases: Anxiety is linked to threat avoidance

The purpose of the present research was to examine if anxiety is linked to a memory-based attentional bias, in which attention to threat is thought to depend on implicit learning. Memory-based attentional biases were defined and also demonstrated in two experiments. A total of 168 university students were shown a pair of faces that varied in their emotional $ content (angry, neutral, and happy), with each type of emotion being consistently preceded by a particular neutral cue face, appearing in the same position. Eye movements were measured during these cue faces and during the emotional faces. The results of two experiments indicated that anxiety was connected with a tendency to avert one's gaze from the positions of angry faces to the positions of happy faces, before these were shown on the screen. This, in turn, caused a reduced perception of angry relative to happy faces. In Experiment 2, participants were also not aware of having a memory-based attentional bias.     

Memory for emotional faces in naturally occurring dysphoria and induced sadness

The aim was to establish if the memory bias for sad faces, reported in clinically depressed patients (Gilboa-Schechtman, Erhard Weiss, & Jeczemien, 2002; Ridout, Astell, Reid, Glen, & O'Carroll, 2003) generalises to sub-clinical depression (dysphoria) and experimentally induced sadness. Study 1: dysphoric (n = 24) and non-dysphoric (n = 20) participants were presented with facial stimuli, asked to identify the emotion portrayed and then given a recognition memory test for these faces. At encoding, dysphoric participants (DP) exhibited impaired identification of sadness and neutral affect relative to the non-dysphoric group (ND). At memory testing, DP exhibited superior memory for sad faces relative to happy and neutral. They also exhibited enhanced memory for sad faces and impaired memory for happy relative to the ND. Study 2: non-depressed participants underwent a positive (n = 24) or negative (n = 24) mood induction (MI) and were assessed on the same tests as Study 1. At encoding, negative MI participants showed superior identification of sadness, relative to neutral affect and compared to the positive MI group. At memory testing, the negative MI group exhibited enhanced memory for the sad faces relative to happy or neutral and compared to the positive MI group. Conclusion: MCM bias for sad faces generalises from clinical depression to these sub-clinical affective states.     

Don’t make me angry,you wouldn’t like me when I’m angry: Volitional choices to act or inhibit are modulated by subliminal perception of emotional faces

Volitional action and self-control—feelings of acting according to one’s own intentions and in being control of one’s own actions—are fundamental aspects of human conscious experience. However, it is unknown whether high-level cognitive control mechanisms are affected by socially salient but nonconscious emotional cues. In this study, we manipulated free choice decisions to act or withhold an action by subliminally presenting emotional faces: In a novel version of the Go/NoGo paradigm, participants made speeded button-press responses to Go targets, withheld responses to NoGo targets, and made spontaneous, free choices to execute or withhold the response for Choice targets. Before each target, we presented emotional faces, backwards masked to render them nonconscious. In Intentional trials, subliminal angry faces made participants more likely to voluntarily withhold the action, whereas fearful and happy faces had no effects. In a second experiment, the faces were made supraliminal, which eliminated the effects of angry faces on volitional choices. A third experiment measured neural correlates of the effects of subliminal angry faces on intentional choice using EEG. After replicating the behavioural results found in Experiment 1, we identified a frontal-midline theta component—associated with cognitive control processes—which is present for volitional decisions, and is modulated by subliminal angry faces. This suggests a mechanism whereby subliminally presented “threat” stimuli affect conscious control processes. In summary, nonconscious perception of angry faces increases choices to inhibit, and subliminal influences on volitional action are deep seated and ecologically embedded.     

Individual differences in emotional reactivity moderate the strength of the relationship between attentional and implicit-memory biases towards threat-related stimuli

The study investigated whether the strength of the relationship between attentional and implicit-memory biases for threat-related material can be moderated by individual differences in temperament and personality. A spatial cueing task, where task-irrelevant angry, happy, and neutral faces acted as spatial cues preceding a target, was immediately followed by an unexpected “old/new” task involving previously presented faces. Temperament-based emotional reactivity (ER; one's typical response strength to emotional stimuli) predicted improved memory performance for angry faces in the “old/new” task. Critically, the relationship between the attentional bias towards threat (indexed by a cue validity index, i.e., a difference in response times on trials where cues with angry expression were presented in the same versus different location to the subsequent target) and enhanced implicit-memory for previously presented task-irrelevant threat-related information was found to be moderated by ER. The current findings provide the first evidence that temperament traits can offer novel insights into the mechanisms enhancing cognitive biases towards threat in the typical population.     

Rapid facial reactions to emotional facial expressions in typically developing children and children with autism spectrum disorder

Typical adults mimic facial expressions within 1000 ms, but adults with autism spectrum disorder (ASD) do not. These rapid facial reactions (RFRs) are associated with the development of social-emotional abilities. Such interpersonal matching may be caused by motor mirroring or emotional responses. Using facial electromyography (EMG), this study evaluated mechanisms underlying RFRs during childhood and examined possible impairment in children with ASD. Experiment 1 found RFRs to happy and angry faces (not fear faces) in 15 typically developing children from 7 to 12 years of age. RFRs of fear (not anger) in response to angry faces indicated an emotional mechanism. In 11 children (8-13 years of age) with ASD, Experiment 2 found undifferentiated RFRs to fear expressions and no consistent RFRs to happy or angry faces. However, as children with ASD aged, matching RFRs to happy faces increased significantly, suggesting the development of processes underlying matching RFRs during this period in ASD.     

Neural correlates of facial emotion processing in infancy

In the present study we examined the neural correlates of facial emotion processing in the first year of life using ERP measures and cortical source analysis. EEG data were collected cross‐sectionally from 5‐ (N = 49), 7‐ (N = 50), and 12‐month‐old (N = 51) infants while they were viewing images of angry, fearful, and happy faces. The N290 component was found to be larger in amplitude in response to fearful and happy than angry faces in all posterior clusters and showed largest response to fear than the other two emotions only over the right occipital area. The P400 and Nc components were found to be larger in amplitude in response to angry than happy and fearful faces over central and frontal scalp. Cortical source analysis of the N290 component revealed greater cortical activation in the right fusiform face area in response to fearful faces. This effect started to emerge at 5 months and became well established at 7 months, but it disappeared at 12 months. The P400 and Nc components were primarily localized to the PCC/Precuneus where heightened responses to angry faces were observed. The current results suggest the detection of a fearful face in infants’ brain can happen shortly (~200–290 ms) after the stimulus onset, and this process may rely on the face network and develop substantially between 5 to 7 months of age. The current findings also suggest the differential processing of angry faces occurred later in the P400/Nc time window, which recruits the PCC/Precuneus and is associated with the allocation of infants’ attention.     

Interacting effects of worry and anxiety on attentional disengagement from threat

Recent work suggests that the ability to disengage attention from threatening information is impaired in people who suffer from anxiety and dysphoria. It has been suggested that this impaired ability to disengage from threat might specifically be associated with the tendency to perseverate about threat (i.e., worry), which is a main characteristic of anxiety disorders and a wide range of other psychopathologies. However, no studies have yet addressed this issue. The present study examined whether trait worry as well as worry intensity after experimental worry induction are associated with impaired ability to disengage attention from threatening cues (angry faces), independently from or in conjunction with anxiety. Sixty-one participants performed a visual cueing experiment that required detection of a target stimulus at one of two possible locations. Prior to the target neutral, happy or angry facial cues appeared at one of these two locations; when there is a relatively long period between the cue and the target (>300 ms), an overall faster responding to invalidly cued trials relative to validly cued trials is believed to indicate inhibition of return (IOR) to a recently attended location. A reduced IOR for angry faces was only found when both trait worry and anxiety were high. When anxiety was kept constant, both trait worry and state worry were associated with enhanced IOR for neutral faces instead. The results seem to suggest that specific threat-related deficiencies in IOR may be a function of the co-occurrence of worry and anxiety.     

Attentional Biases for Facial Expressions in Social Phobia: The Face-in-the-Crowd Paradigm

The present study examines the attentional bias hypothesis for individuals with generalised social phobia (GSPs). Socially phobic individuals were hypothesised to exhibit attentional bias towards threat stimuli relevant to interpersonal situations. This hypothesis was tested using the face-in-the-crowd paradigm. GSPs and nonanxious controls (NACs) detected an angry, happy, neutral, or disgust target face in a crowd of 12 distracter photographs. Results indicated that, compared to NACs, GSPs exhibited greater attentional biases for angry than for happy faces in a neutral crowd. GSPs were more slowed down in their performance by happy and angry versus neutral distracters; NACs did not exhibit such sensitivity to distracter type. Finally, GSPs were faster in detecting anger than disgust expressions; NACs detected both types of faces equally quickly. Implications of these findings for the maintenance of social phobia are discussed.     

Attention biases and habituation of attention biases are associated with 5-HTTLPR and COMTval158met

Fundamental biases in affective information processing are modulated by individual differences in the emotional response to environmental stimuli that may be partly based on the individual’s genetic make-up. To extend prior dot probe studies on attention genetics, we used a visual-search paradigm (VSP) with pictures of angry and happy faces of both sexes as targets, neutral faces as distractors, and a varying set size. Participants were selected a priori depending on their 5-HTTLPR (s/s, s/l, l/l; on a constant rs25531 A-allele background) and COMTval158met (val/val, valmet, met/met) genotypes and were matched for sex and age. We demonstrate a bias towards angry male faces (as opposed to happy male faces) irrespective of 5-HTTLPR genotype in the first experimental block that was maintained during the second experimental block only in carriers of the s-allele, which implies differential habituation processes. While a bias towards angry male faces was observed irrespective of COMTval158met genotype, only individuals with the val/val genotype exhibited a bias towards a happy female face (as opposed to an angry female face). In sum, our results both replicate and extend prior findings in the field of attention genetics and add important pieces of information to the research on attentional biases in emotion processing.     

Event-related potentials to schematic faces in social phobia

Social phobia has been associated with an attentional bias for angry faces. This study aimed at further characterising this attentional bias by investigating reaction times, heart rates, and ERPs while social phobics, spider phobics, and controls identified either the colour or the emotional quality of angry, happy, or neutral schematic faces. The emotional expression of angry faces did not interfere with the processing of their colour in social phobics, and heart rate, N170 amplitude and parietal late positive potentials (LPPs) of these subjects were also no different from those of non-phobic subjects. However, social phobics showed generally larger P1 amplitudes than non-phobic controls with spider phobic subjects in between. No general threat advantage for angry faces was found. All groups identified neutral schematic faces faster and showed larger late positive amplitudes to neutral than to emotional faces. Furthermore, in all groups the N170 was modulated by the emotional quality of faces. This effect was most pronounced in the emotion identification task.     

The time-course of visual threat processing: High trait anxious individuals eventually avert their gaze from angry faces

Several experiments have shown that anxious individuals have an attentional bias towards threat cues. It is also known, however, that exposure to a subjectively threatening but relatively harmless stimulus tends to lead to a reduction in fear. Accordingly, some authors have hypothesised that high trait anxious individuals have a vigilant-avoidant pattern of visual attention to threatening stimuli. In the present study, 52 high trait anxious and 48 low trait anxious subjects were shown pairs of emotional faces, while their direction of gaze was continuously monitored. For 0-1000 ms, both groups were found to view angry faces more than happy faces. For 2000-3000 ms, however, only high trait anxious subjects averted their gaze from angry faces more than they did from happy faces.     

The Relationship Between Attention,Interpretation, and Memory Bias During Facial Perception in Social Anxiety

Although cognitive theories suggest the interactive nature of information processing biases in contributing to social anxiety, most studies to date have investigated these biases in isolation. This study aimed at (a) testing the association between social anxiety and each of the threat-related cognitive biases: attention, interpretation, and memory bias; and (b) examining the relationship between these cognitive biases in facial perception. We recruited an unselected sample of 188 adult participants and measured their level of social anxiety and cognitive biases using faces displaying angry, disgusted, happy, and ambiguous versions of these expressions. All bias tasks were assessed with the same set of facial stimuli. Regression analyses showed that social anxiety symptoms significantly predicted attention avoidance and poorer sensitivity in recognizing threatening faces. Social anxiety was, however, unrelated to interpretation bias in our sample. Results of path analysis suggested that attention bias influenced memory bias indirectly through interpretation bias for angry but not disgusted faces. Our findings suggest that, regardless of social anxiety level, when individuals selectively oriented to faces displaying anger, the faces were interpreted to be more negative. This, in turn, predicted better memory for the angry faces. The results provided further empirical support for the combined cognitive bias hypothesis.