Beware the eyes behind the mask: The capture and hold of selective attention by backward masked fearful eyes

Fearful facial expressions are important social indicators of environmental threat. Among the various features of a fearful face, the eyes appear to be particularly important for recognizing and responding to these social cues. One way in which fearful faces facilitate observers’ behavior is by automatically capturing attention. This is true for both consciously and nonconsciously processed fearful faces. Recent research suggests that consciously processed fearful eyes alone are sufficient to capture observers’ attention. However, it is unknown as to whether or not nonconsciously processed, backward masked, fearful eyes are sufficient to facilitate spatial attention. To test this possibility, two dot-probe experiments with masked fearful eye stimuli were performed. In Experiment 1, we found that, relative to scrambled eyes, masked fearful eyes facilitate attentional orienting and delay attentional disengagement. In Experiment 2, we replicated this effect when comparing backward masked fearful to neutral eyes. Thus, the data suggest that nonconscious fearful eyes facilitate spatial attention through facilitated orienting and delayed disengagement.     

Attending to the fear in your eyes: Facilitated orienting and delayed disengagement

Fearful facial expressions convey threat-related information and automatically elicit modulations in spatial attention. The eye-region appears to be a particularly important feature for recognising and responding to fearful faces. However, it is unknown as to whether or not fearful eyes initiate modulations in spatial attention. In the current study, three dot-probe experiments with fearful and neutral eye stimuli were performed. The results of Experiment 1 demonstrate that fearful eyes capture spatial attention through facilitated attentional orienting to threat and delayed attentional disengagement from threat. In Experiments 2 and 3, these attentional effects were replicated, while ruling out the influence of overall size/shape and brightness differences between fearful and neutral eyes, respectively. Thus, fearful eye-whites appear to be a salient feature of fearful facial expressions that elicit modulations in spatial attention.     

A time-course analysis of attentional cueing by threatening scenes

Models of attention and emotion have assigned a special status to the processing of threatening information: Facilitated attentional capture by threat and its prioritized processing would allow for swift and adequate action to potentially dangerous stimuli. In four experiments, we examined the time-course of facilitated orienting of attention to threatening scenes in the exogenous cueing paradigm. Threat value and presentation duration of the cues were systematically varied. Facilitated attentional capture by threat was limited to highly threatening pictures presented for 100 ms. No attentional effects were observed with a 28 ms cue presentation duration. At slightly longer cue presentations, 200 ms and 500 ms, results indicated no and even reduced attentional capture by threat compared with neutral information. The present results provide support for the idea that threat facilitates fast attentional orienting to its location, followed by the inhibition of attention to threat.     

Both fearful and happy expressions interact with gaze direction by 200 ms SOA to speed attention orienting

Attention orienting towards a gazed-at location is fundamental to social attention. Whether gaze cues can interact with emotional expressions other than those signalling environmental threat to modulate this gaze cueing, and whether this integration changes over time, remains unclear. With four experiments we demonstrate that, when perceived motion inherent to dynamic displays is controlled for, gaze cueing is enhanced by both fearful and happy faces compared to neutral faces. This enhancement is seen with stimulus-onset asynchronies ranging from 200–700?ms. Thus, gaze cueing can be reliably modulated by positive expressions, albeit to a smaller degree than fearful ones, and this gaze–emotion integration impacts behaviour as early as 200?ms post-cue onset.     

Do threatening stimuli draw or hold visual attention in subclinical anxiety?

Biases in information processing undoubtedly play an important role in the maintenance of emotion and emotional disorders. In an attentional cueing paradigm, threat words and angry faces had no advantage over positive or neutral words (or faces) in attracting attention to their own location, even for people who were highly state-anxious. In contrast, the presence of threatening cues (words and faces) had a strong impact on the disengagement of attention. When a threat cue was presented and a target subsequently presented in another location, high state-anxious individuals took longer to detect the target relative to when either a positive or a neutral cue was presented. It is concluded that threat-related stimuli affect attentional dwell time and the disengage component of attention, leaving the question of whether threat stimuli affect the shift component of attention open to debate.     

The flexibility of emotional attention: Accessible social identities guide rapid attentional orienting

There is extensive evidence that emotional-especially threatening-stimuli rapidly capture attention. These findings are often explained in terms of a hard-wired and relatively inflexible fear module. We propose an alternative, more flexible mechanism, arguing that motivational relevance is the crucial factor driving rapid attentional orienting. To test our hypothesis, we endowed initially neutral face stimuli with relevance by randomly assigning them to a social in-group or out-group during a 1-min learning phase, and used these faces as cues in a dot probe task to measure rapid attentional orienting. Across three experiments, we observed attentional orienting toward faces assigned to the out-group. Initial rapid orienting (after 100ms, Experiments 1 and 2) was observed only for familiar faces for which group membership was explicitly encoded, suggesting that rapid orienting may be based on affectively charged memory traces. At a later time point (after 500ms, Experiment 3), attention was deployed toward unfamiliar faces sharing a physical attribute (background color) with the familiar out-group faces, suggesting a more time-consuming on-line appraisal of the stimulus. The amount of attentional bias to out-group faces was correlated with individual differences in the accessibility of group identification. Our findings demonstrate that attentional prioritization mechanisms can be flexibly tuned by a brief learning phase of social identity. This is consistent with the idea that attention mechanisms subserving the selection and prioritization of emotional aspects of the environment are not static and hard-wired, but may rapidly adapt to recent changes in motivational contingencies.     

Feast your eyes: hunger and trait reward drive predict attentional bias for food cues

Appraisal theories of emotion predict that the relevance of a stimulus to a person's needs and goals influences attentional allocation. We used a modified visual probe task to examine the influence of hunger and trait reward drive on food-related attentional bias. Both hunger and trait reward drive predicted degree of attentional "disengagement" from food images at short (100 ms), but not long (500, 2,000 ms) stimulus durations. Effects of hunger were found for both bland and appetizing foods, while effects of reward drive were restricted to appetizing foods. Our findings extend previous research showing delayed "disengagement" from threat-related stimuli, suggesting that both organismic- and goal-relevance are key biasing factors in attentional competition.     

Attention for emotional faces under restricted awareness revisited: do emotional faces automatically attract attention?

Theoretical models of attention for affective information have assigned a special status to the cognitive processing of emotional facial expressions. One specific claim in this regard is that emotional faces automatically attract visual attention. In three experiments, the authors investigated attentional cueing by angry, happy, and neutral facial expressions that were presented under conditions of limited awareness. In these experiments, facial expressions were presented in a masked (14 ms or 34 ms, masked by a neutral face) and unmasked fashion (34 ms or 100 ms). Compared with trials containing neutral cues, delayed responding was found on trials with emotional cues in the unmasked, 100-ms condition, suggesting stronger allocation of cognitive resources to emotional faces. However, in both masked and unmasked conditions, the hypothesized cueing of visual attention to the location of emotional facial expression was not found. In contrary, attentional cueing by emotional faces was less strong compared with neutral faces in the unmasked, 100-ms condition. These data suggest that briefly presented emotional faces influence cognitive processing but do not automatically capture visual attention.     

Effects of threat cues on attentional shifting, disengagement and response slowing in anxious individuals

According to cognitive models of anxiety, attentional biases for threat may cause or maintain anxiety states. Previous research using spatial cueing tasks has been interpreted in terms of difficulty in disengaging attention from threat in anxious individuals, as indicated by contrasts of response times (RTs) from threat cue versus neutral cue trials. However, on spatial cueing tasks, differences in RT between threat cue and neutral cue trials may stem from a slowing effect of threat on RT, as well as effects on allocation of visuospatial attention. The present study examined the effects of threat cues on both attentional cueing and response slowing. High and low anxious individuals completed a central cue task, which assessed threat-related response slowing, and a spatial cueing task, which assessed attentional biases for angry, happy and neutral faces. Results indicated that interpretation of the anxiety-related bias for threat depended on whether the effect of response slowing was taken into account. The study illustrates an important problem in using the modified spatial cueing task to assess components of threat-related attentional bias. As this experimental method may reflect both threat-related attentional cueing and response slowing effects, it cannot be assumed to provide pure measures of shift or disengagement components of attention bias.     

Processing emotional stimuli: Comparison of saccadic and manual choice-reaction times

We compared the speed of discrimination for emotional and neutral faces in four experiments, using a forced-choice saccadic and manual reaction time task. Unmasked, brief (20 ms) bilateral presentation of schematic (Exp. 1) or naturalistic (Exp. 2) emotional/neutral face pairs, led to shorter discrimination of emotional stimuli in saccadic localisation task. When the effect of interference from emotional stimuli is ruled out by showing a pairing of the emotional or neutral face with an outline face, faster saccadic discrimination was obtained for fearful facial expression only (Exp. 3). The manual discrimination reaction time was not significantly different for emotional versus neutral stimuli. To explore the absence of a manual RT effect we manipulated the stimulus duration (20 ms vs. 500 ms: Exp. 4). Faster saccadic discrimination of emotional stimuli was observed at both durations. For manual responses, emotional bias was observed only at the longest duration (500 ms). Overall, comparison of saccadic and manual responses shows that faster discrimination of emotional/neutral stimuli can be carried out within the oculomotor system. In addition, emotional stimuli are processed preferentially to neutral face stimuli.     

The spider does not always win the fight for attention: Disengagement from threat is modulated by goal set

Stimulus-driven preferential attention to threat can be modulated by goal-driven attention. However, it remains unclear how this goal-driven modulation affects specific attentional components implied in threat interference. We hypothesise that goal-driven modulation most strongly impacts delayed disengagement from threat. A spatial cueing task was used that disentangles delayed disengagement from attentional capture by tightly manipulating the locus of attention at the time of target onset. Different top-down goals were induced by instructing participants to identify bird/fish targets (Experiment 1) or spider/cat targets (Experiment 2) among animal non-targets. Delayed disengagement from a non-target spider was observed only when the spider was part of the target set, not when it was task-irrelevant. This corroborates evidence that threat stimuli do not necessarily override goal-driven attentional control and that extended processing of threatening distractors is not obligatory.     

To look or not to look: an eye movement study of hypervigilance during change detection in high and low spider fearful students

Previous eye movement studies of attentional bias in spider fear reported inconsistent results with respect to early attentional capture, suggesting that overt attentional capture only reliably occurs under specific circumstances. In addition, none of these studies explored covert attention. The present study examined attentional bias in spider phobia using a change detection paradigm that was expected to provide good conditions for documenting attentional capture. In contrast to our expectations, eye movement data showed that all participants' first fixations were fastest on general negative targets, whereas participants' first fixations on spider targets were slower in the spider fearful than in the nonfearful group. In addition, spider fearful participants made more nontarget fixations before fixating on a spider target than did nonfearful participants. Thus, we found that participants' overt attention was more quickly focused on general negative targets, whereas covert attentional processes enabled initial avoidance of fear-relevant (i.e. spider) stimuli. The present findings have important implications for research on attention and fear as they indicate that fearful individuals are not characterized by static attentional orienting toward threat but, under certain conditions, may avert attention from threat automatically.     

The initial stage of visual selection is controlled by top-down task set: new ERP evidence

Salient visual singleton stimuli produce spatial cueing effects indicative of attentional capture only when they match current task sets, suggesting that capture is subject to top-down control. However, such task-set contingent capture effects could be associated with the top-down controlled disengagement of attention from non-matching stimuli that follows their initial bottom-up salience-driven selection. Using the N2pc component as an event-related potential marker of attentional capture, we demonstrate that top-down task set already controls the initial rapid selection of salient visual singleton stimuli prior to any subsequent attentional disengagement. These findings provide new evidence for the primacy of top-down control over bottom-up salience in attentional capture.     

Early detection and avoidance of threatening faces during passive viewing

To evaluate whether there is an early attentional bias towards negative stimuli, we tracked participants' eyes while they passively viewed displays composed of four Ekman faces. In Experiment 1 each display consisted of three neutral faces and one face depicting fear or happiness. In half of the trials, all faces were inverted. Although the passive viewing task should have been very sensitive to attentional biases, we found no evidence that overt attention was biased towards fearful faces. Instead, people tended to actively avoid looking at the fearful face. This avoidance was evident very early in scene viewing, suggesting that the threat associated with the faces was evaluated rapidly. Experiment 2 replicated this effect and extended it to angry faces. In sum, our data suggest that negative facial expressions are rapidly analysed and influence visual scanning, but, rather than attract attention, such faces are actively avoided.     

Components of attentional bias to threat in high trait anxiety: Facilitated engagement, impaired disengagement, and attentional avoidance

There is a wealth of evidence demonstrating enhanced attention to threat in high trait anxious individuals (HTA) compared with low trait anxious individuals (LTA). In two experiments, we investigated whether this attentional bias is related to facilitated attentional engagement to threat or difficulties disengaging attention from threat. HTA and LTA undergraduates performed a modified exogenous cueing task, in which the location of a target was correctly or incorrectly cued by neutral, highly and mildly threatening pictures. Results indicate that at 100 ms picture presentation, HTA individuals more strongly engaged their attention with and showed impaired disengagement from highly threatening pictures than LTA individuals. In addition, HTA individuals showed a stronger tendency to attentional avoidance of threat at the 200 and 500 ms picture presentation. These data provide evidence for differential patterns of anxiety-related biases in attentive processing of threat at early versus later stages of information processing.     

Biases in eye movements to threatening facial expressions in generalized anxiety disorder and depressive disorder

The study investigated biases in selective attention to emotional face stimuli in generalized anxiety disorder (GAD) and depressive disorder, using a modified probe detection task. There were 4 face types: threatening, sad, happy, and neutral. Measures of attentional bias included (a) the direction and latency of the initial eye movement in response to the faces and (b) manual reaction time (RT) to probes replacing the face stimuli 1,000 ms after their onset. Results showed that individuals with GAD (without depressive disorder) were more likely to look first toward threat faces rather than neutral faces compared with normal controls and those with depressive disorder. They also shifted their gaze more quickly toward threat faces, rather than away from them, relative to the other two groups. There were no significant findings from the manual RT data. Implications of the results for recent theories of clinical anxiety and depression are discussed.     

The orienting of spatial attention to backward masked fearful faces is associated with variation in the serotonin transporter gene

Threat signals facilitate spatial attention, even when awareness of these signals has been restricted through the use of backward masking. However, unrestricted/unmasked threat cues tend to delay the disengagement of attention, whereas restricted/masked threat facilitates orienting, suggesting different underlying mechanisms. Within the general population, the serotonin transporter gene polymorphism (5HTTLPR) is associated with one's allocation of attention to unmasked threat signals. However, it is unclear to what extent the 5HTTLPR gene may be involved in nonconscious biases to masked threat, and whether or not such biases are driven by facilitated orienting or delayed disengagement. Participants were genotyped and performed a dot-probe task with backward masked fearful and neutral faces. Results indicate that short-allele carriers of the 5HTTLPR gene nonconsciously orient spatial attention to masked fearful faces. On the other hand, homozygous long-allele individuals tended to direct attention away from masked fearful faces. All participants' performance was at chance in a posttask assessment of awareness for the masked faces. The results add to current literature on the 5HTTLPR and attention biases, and suggest that threat signals facilitate the orienting of attention in short-allele carriers of the 5HTTLPR gene even under restricted processing conditions.     

Is there a mutual relationship between opposite attentional biases underlying anxiety?

Current models that account for attentional processes in anxiety have proposed that high-trait anxious individuals are characterized by a hypervigilant-avoidant pattern of attentional biases to threat. We adopted a laboratory conditioning procedure to induce concomitant hypervigilance and avoidance to threat, emphasizing a putative relationship between lower-level reactive and upper-level controlled attentional mechanisms as the core account of attentional processes involved in the development and maintenance of anxiety. Eighty high- and low-trait anxious participants underwent Pavlovian conditioning to a human face. Eye tracking was used to monitor attentional changes to the conditioned stimulus (CS+) face and the neutral stimulus (CS-) face, presented at 200, 500, and 800 ms durations. The high-anxious participants developed the expected attentional bias toward the CS+ at 200 ms presentation time and attentional avoidance at 500 and 800 ms durations. Hypervigilance to aversive stimuli at 200 ms and later avoidance to the same stimuli at 500 and 800 ms were associated with higher levels of galvanic skin conductance to the CS+. The low-anxious individuals developed the opposite attentional pattern with an initial tendency to orient attention away from the aversive stimuli in the 200 ms condition and to orient attention toward aversive stimuli in the remaining time. The differential modulation between hypervigilance and avoidance elicited in the two groups by the conditioning procedure suggests that vulnerability to anxiety is characterized by a latent relationship between diverse attentional mechanisms. Within this relationship, hypervigilance and avoidance to threat operate at different stages of information processing suggesting fuzzy boundaries between early reactive and later-strategic processing of threat.     

Associations between attentional biases to fearful faces and social-emotional development in infants with and without an older sibling with autism

During the first year of life, infants become increasingly attuned to facial emotion, with heightened sensitivity to faces conveying threat observed by age seven months as illustrated through attentional biases (e.g., slower shifting away from fearful faces). Individual differences in these cognitive attentional biases have been discussed in relation to broader social-emotional functioning, and the current study examines these associations in infants with an older sibling with autism spectrum disorder (ASD), a group with an elevated likelihood of a subsequent ASD diagnosis (ELA; n = 33), and a group of infants with no family history of ASD who are at low likelihood of ASD (LLA; n = 24). All infants completed a task measuring disengagement of attention from faces at 12 months (fearful, happy, neutral), and caregivers completed the Infant-Toddler Social and Emotional Assessment at 12, 18, and/or 24 months. For the full sample, greater fear bias in attention disengagement at 12 months related to more internalizing behaviors at 18 months, and this was driven by the LLA infants. When examining groups separately, findings revealed that LLA with a greater fear bias had more difficult behaviors at 12, 18, and 24 months; in contrast, ELA showed the opposite pattern, and this was most pronounced for ELA who later received an ASD diagnosis. These preliminary group-level findings suggest that heightened sensitivity to fearful faces might serve an adaptive function in children who later receive an ASD diagnosis, but in infants with no family history of ASD, increased biases might reflect a marker of social-emotional difficulties.     

Attentional capture by irrelevant emotional distractor faces

We establish attentional capture by emotional distractor faces presented as a "singleton" in a search task in which the emotion is entirely irrelevant. Participants searched for a male (or female) target face among female (or male) faces and indicated whether the target face was tilted to the left or right. The presence (vs. absence) of an irrelevant emotional singleton expression (fearful, angry, or happy) in one of the distractor faces slowed search reaction times compared to the singleton absent or singleton target conditions. Facilitation for emotional singleton targets was found for the happy expression but not for the fearful or angry expressions. These effects were found irrespective of face gender and the failure of a singleton neutral face to capture attention among emotional faces rules out a visual odd-one-out account for the emotional capture. The present study thus establishes irrelevant, emotional, attentional capture.