Neutral Face Cue Research Articles

Neural underpinnings of threat bias in relation to loss-of-control eating behaviors among adolescent girls with high weight

IntroductionLoss-of-control (LOC) eating, a key feature of binge-eating disorder, may relate attentional bias (AB) to highly salient interpersonal stimuli. The current pilot study used magnetoencephalography (MEG) to explore neural features of AB to socially threatening cues in adolescent girls with and without LOC-eating.MethodsGirls (12–17 years old) with overweight or obesity (BMI >85th percentile) completed an AB measure on an affective dot-probe AB task during MEG and evoked neural responses to angry or happy (vs. neutral) face cues were captured. A laboratory test meal paradigm measured energy intake and macronutrient consumption patterns.ResultsGirls (N = 34; Mage = 15.5 ± 1.5 years; BMI-z = 1.7 ± 0.4) showed a blunted evoked response to the presentation of angry face compared with neutral face cues in the left dorsolateral prefrontal cortex, a neural region implicated in executive control and regulation processes, during attention deployment (p < 0.01). Compared with those without LOC-eating (N = 21), girls with LOC-eating (N = 13) demonstrated a stronger evoked response to angry faces in the visual cortex during attention deployment (p < 0.001). Visual and cognitive control ROIs had trends suggesting interaction with test meal intake patterns among girls with LOC-eating (ps = 0.01).DiscussionThese findings suggest that girls with overweight or obesity may fail to adaptively engage neural regions implicated in higher-order executive processes. This difficulty may relate to disinhibited eating patterns that could lead to excess weight gain.

Bed nucleus of the stria terminalis and amygdala responses to unpredictable threat in children.

Substantial evidence from studies in humans suggests the amygdala is pivotal for anxiety. Findings from animal models and translational studies suggests the bed nucleus of the stria terminalis (BNST) is also critical for anxiety and the anticipation of unpredictable threat in adults. However, it remains unknown whether the BNST is involved in unpredictable threat anticipation in children. Forty-two 8-10-year-olds completed resting-state functional magnetic resonance imaging (fMRI) scans and an unpredictable threat fMRI task in which they were trained to associate cues with images. Intrinsic connectivity analyses were performed to establish functional BNST and amygdala networks. BNST and amygdala activation to cues and images was tested. Significant findings were followed by task-based functional connectivity analyses. Children showed evidence for BNST and amygdala intrinsic connectivity that was similar to previous patterns observed in adults. In response to unpredictable cues relative to neutral face cues, children had a significant amygdala response but no response in the BNST. The amygdala, but not the BNST, also showed a significantly greater response to fear face images relative to neutral images. Thus, unpredictable threat activated the amygdala, but not BNST, in children. This finding is contrary to studies showing robust BNST activation to unpredictable threat in adults and may suggest that the BNST's role in threat processing emerges later in development.

Attentional avoidance of emotional information in emotional eating

We investigated an attention bias (AB) for emotional faces in emotional eating (EM). A group obtaining a low score (n = 18) on the Emotional eating scale of the Dutch Eating Behavior Questionnaire and a high scoring group (n = 23) completed the Exogenous Cueing Task (ECT). The ECT experiment measured their reaction times to the location of a target dot preceded by a happy, sad, angry or neutral face cue. The Coping Inventory for Stressful Situations was administrated to collect information on participants’ coping strategies. Compared to the group with a low degree of EM, the high EM group showed significant attentional avoidance of emotional faces, particularly negative faces, in the ECT. The coping questionnaire indicated that the high EM group displayed higher levels of avoidance coping compared to the low EM group. General levels of EM and avoidance coping were also positively correlated, and avoidance coping significantly predicted the level of EM. The findings of the present study indicate that attentional avoidance of emotional content, which has previously been observed in clinical studies of eating disorders (Cardi et al., 2015a; Davies et al., 2011), is also present in subclinical samples of EM.

Measuring the emotion-specificity of rapid stimulus-driven attraction of attention to fearful faces: evidence from emotion categorization and a comparison with disgusted faces.

In the current study, we tested whether a fear advantage-rapid attraction of attention to fearful faces that is more stimulus-driven than to neutral faces-is emotion specific. We used a cueing task with face cues preceding targets. Cues were non-predictive of the target locations. In two experiments, we found enhanced cueing of saccades towards the targets with fearful face cues than with neutral face cues: Saccades towards targets were more efficient with cues and targets at the same position (under valid conditions) than at opposite positions (under invalid conditions), and this cueing effect was stronger with fearful than with neutral face cues. In addition, this cueing effect difference between fearful and neutral faces was absent with inverted faces as cues, indicating that the fear advantage is face-specific. We also show that emotion categorization of the face cues mirrored these effects: Participants were better at categorizing face cues as fearful or neutral with upright than with inverted faces (Experiment 1). Finally, in alternative blocks including disgusted faces instead of fearful faces, we found more similar cueing effects with disgusted faces and neutral faces, and with upright and inverted faces (Experiment 2). Jointly, these results demonstrate that the fear advantage is emotion-specific. Results are discussed in light of evolutionary explanations of the fear advantage.

Fearful, surprised, happy, and angry facial expressions modulate gaze-oriented attention: Behavioral and ERP evidence

The impact of emotions on gaze-oriented attention was investigated in non-anxious participants. A neutral face cue with straight gaze was presented, which then averted its gaze to the side while remaining neutral or expressing an emotion (fear/surprise in Exp.1 and anger/happiness in Exp.2). Localization of a subsequent target was faster at the gazed-at location (congruent condition) than at the non-gazed-at location (incongruent condition). This Gaze-Orienting Effect (GOE) was enhanced for fear, surprise, and anger, compared to neutral expressions which did not differ from happy expressions. In addition, Event Related Potentials (ERPs) to the target showed a congruency effect on P1 for fear and surprise and a left lateralized congruency effect on P1 for happy faces, suggesting that target visual processing was also influenced by attention to gaze and emotions. Finally, at cue presentation, early postero-lateral (Early Directing Attention Negativity (EDAN)) and later antero-lateral (Anterior Directing Attention Negativity (ADAN)) attention-related ERP components were observed, reflecting, respectively, the shift of attention and its holding at gazed-at locations. These two components were not modulated by emotions. Together, these findings show that the processing of social signals such as gaze and facial expression interact rather late and in a complex manner to modulate spatial attention.

Focus on the positive: Anxiety modulates the effects of emotional stimuli on hemispheric attention

People with high levels of trait anxiety are said to orient attention selectively to threatening stimuli (Bradley, Mogg, White, Groom, & de Bono, 1999; MacLeod, Mathews, & Tata, 1986), but this effect is sometimes difficult to replicate. We suggest a reason for this difficulty is that typical tests of the spatial attention bias in anxiety failed to consider together: (1) the differential effects of positive and threatening stimuli on attention in anxiety, (2) the separate contributions of each hemisphere to the attention bias, and (3) whether the attention bias in anxiety is restricted to orienting or can be observed more strongly in the conflict or alerting networks of attention. We compared the effects of schematic angry, happy, and neutral face cues using a lateralized version of Posner’s Attention Network Task (Lateralized Attention Network Test) which distinguishes spatial Orienting Cost (due to an invalid cue; disengagement) from spatial Orienting Benefit (due to a valid cue; hypervigilance), and which considers executive Conflict resolution and Alerting in addition to spatial Orienting in each hemisphere separately. We tested participants with high and low trait anxiety measured by the STAI-TA (Spielberger, Gorsuch, & Lushene, 1983). Surprisingly, happy face cues rather than angry face cues interacted with target visual field and participant level of anxiety. Happy face cues presented to participants with low anxiety elicited maximal Orienting Benefit and minimal Orienting Cost for targets presented to the left visual field. Anxious individuals failed to benefit from happy cues in the left visual field. We suggest that lateralized positive cues can provide a more sensitive index of attention changes in anxiety than is provided by centrally-presented threatening cues.

Cardiac vagal tone predicts inhibited attention to fearful faces.

The neurovisceral integration model (Thayer, J. F., & Lane, R. D., 2000, A model of neurovisceral integration in emotion regulation and dysregulation. Journal of Affective Disorders, 61, 201-216. doi:10.1016/S0165-0327(00)00338-4) proposes that individual differences in heart rate variability (HRV)-an index of cardiac vagal tone-are associated with attentional and emotional self-regulation. In this article, we demonstrate that individual differences in resting HRV predict the functioning of the inhibition of return (IOR), an inhibitory attentional mechanism highly adaptive to novelty search, in response to affectively significant face cues. As predicted, participants with lower HRV exhibited a smaller IOR effect to fearful versus neutral face cues than participants with higher HRV, which shows a failure to inhibit attention from affectively significant cues and instigate novelty search. In contrast, participants with higher HRV exhibited similar IOR effects to fearful and neutral face cues, which shows an ability to inhibit attention from cues and instigate novelty search. Their ability to inhibit attention was most pronounced to high spatial frequency fearful face cues, suggesting that this effect may be mediated by cortical mechanisms. The current research demonstrates that individual differences in HRV predict attentional inhibition and suggests that successful inhibition and novelty search may be mediated by cortical inhibitory mechanisms among people with high cardiac vagal tone.

Emotion potentiates response activation and inhibition in masked priming

Previous studies have shown that emotion can have 2-fold effects on perception. At the object-level, emotional stimuli benefit from a stimulus-specific boost in visual attention at the relative expense of competing stimuli. At the visual feature-level, recent findings indicate that emotion may inhibit the processing of small visual details and facilitate the processing of coarse visual features. In the present study, we investigated whether emotion can boost the activation and inhibition of automatic motor responses that are generated prior to overt perception. To investigate this, we tested whether an emotional cue affects covert motor responses in a masked priming task. We used a masked priming paradigm in which participants responded to target arrows that were preceded by invisible congruent or incongruent prime arrows. In the standard paradigm, participants react faster, and commit fewer errors responding to the directionality of target arrows, when they are preceded by congruent vs. incongruent masked prime arrows (positive congruency effect, PCE). However, as prime-target SOAs increase, this effect reverses (negative congruency effect, NCE). These findings have been explained as evidence for an initial activation and a subsequent inhibition of a partial response elicited by the masked prime arrow. Our results show that the presentation of fearful face cues, compared to neutral face cues, increased the size of both the PCE and NCE, despite the fact that the primes were invisible. This is the first demonstration that emotion prepares an individual's visuomotor system for automatic activation and inhibition of motor responses in the absence of visual awareness.

Beyond attentional bias: A perceptual bias in a dot-probe task.

Previous dot-probe studies indicate that threat-related face cues induce a bias in spatial attention. Independently of spatial attention, a recent psychophysical study suggests that a bilateral fearful face cue improves low spatial-frequency perception (LSF) and impairs high spatial-frequency perception (HSF). Here, we combine these separate lines of research within a single dot-probe paradigm. We found that a bilateral fearful face cue, compared with a bilateral neutral face cue, speeded up responses to LSF targets and slowed down responses to HSF targets. This finding is important, as it shows that emotional cues in dot-probe tasks not only bias where information is preferentially processed (i.e., an attentional bias in spatial location), but also bias what type of information is preferentially processed (i.e., a perceptual bias in spatial frequency).

Emotional cues enhance the attentional effects on spatial and temporal resolution

In the present study, we demonstrated that the emotional significance of a spatial cue enhances the effect of covert attention on spatial and temporal resolution (i.e., our ability to discriminate small spatial details and fast temporal flicker). Our results indicated that fearful face cues, as compared with neutral face cues, enhanced the attentional benefits in spatial resolution but also enhanced the attentional deficits in temporal resolution. Furthermore, we observed that the overall magnitudes of individuals’ attentional effects correlated strongly with the magnitude of the emotion × attention interaction effect. Combined, these findings provide strong support for the idea that emotion enhances the strength of a cue’s attentional response.

Emotion-induced trade-offs in spatiotemporal vision.

It is generally assumed that emotion facilitates human vision in order to promote adaptive responses to a potential threat in the environment. Surprisingly, we recently found that emotion in some cases impairs the perception of elementary visual features (Bocanegra & Zeelenberg, 2009b). Here, we demonstrate that emotion improves fast temporal vision at the expense of fine-grained spatial vision. We tested participants' threshold resolution with Landolt circles containing a small spatial or brief temporal discontinuity. The prior presentation of a fearful face cue, compared with a neutral face cue, impaired spatial resolution but improved temporal resolution. In addition, we show that these benefits and deficits were triggered selectively by the global configural properties of the faces, which were transmitted only through low spatial frequencies. Critically, the common locus of these opposite effects suggests a trade-off between magno- and parvocellular-type visual channels, which contradicts the common assumption that emotion invariably improves vision. We show that, rather than being a general "boost" for all visual features, affective neural circuits sacrifice the slower processing of small details for a coarser but faster visual signal.

Effects of Supra- and Sub-liminal Emotional Cues on Inhibition of Return

In the classical exogenous cue-target paradigm, when a target is presented in the same location as a cue within a stimulus onset asynchrony (SOA) of 250 ms or less, target detection is facilitated. However, when the SOA is extended to more than 250 ms, target detection is slowed at the cued location. This phenomenon is called inhibition of return (IOR). IOR is generally assumed to be an adaptive mechanism which enhances the chance of success or survival by maximizing the chance of detecting important information in visual search during human evolution. If so, the time course and/or magnitude of IOR may be affected by biological information of the cue. If a cue provides information relevant to individual’s survival, then attention may not be inhibited from reorienting to the cue. However, previous evidence concerning this issue is controversial. This study is to further examine whether IOR is modulated by emotional valences of face, which convey important biological and social information. We hypothesized that emotional information conveyed through supraliminally presented face cues may not differentially affect the IOR effect, because this information could be suppressed by the top-down control settings demanding no interference from emotion, whereas emotional information conveyed through subliminally presented face cues may affect pattern of the IOR effect, because this information is processed automatically and it escapes from top-down suppression. A total of 32 undergraduate students participated in Experiments 1 and 2, which manipulated the number of simultaneously cued locations. Faces with different emotional valences (happy, angry and neutral) were as uninformative peripheral cues, supraliminally in Experiment 1 and subliminally in Experiment 2, while the participants were instructed to make detection responses to the target, which was presented at one of the cued locations or at an uncued location, as quickly and accurately as possible. Experiment 1 obtained an overall IOR effect but the magnitude of this effect was not affected by the emotional valences of face cues. Experiment 2 obtained a significant IOR effect, but only for the neutral face cues. These findings are consistent with our hypothesis, suggesting that IOR can be modulated by the property of biologically important cues. The evolutionary significance of the IOR mechanism was discussed.

Interpreting neutral faces as threatening is a default mode for socially anxious individuals.

The authors of the present study used an incidental learning paradigm to investigate the interpretation of neutral facial expressions in socially anxious individuals. Participants were asked to detect the location of a target following the presentation of a facial picture (i.e., cue). Unbeknownst to participants, the target location was contingent on the valence of the cue, and participants thus learned to associate different target locations with either positive or negative facial expressions. The authors subsequently used this learned association to assess interpretive biases. If socially anxious individuals interpret neutral faces in a negative manner, they should be faster to detect a target that appears in the location that is associated with negative face cues when the target is presented after a neutral face cue. The authors also assessed whether the anticipation of a feared situation influenced interpretive biases by comparing participants with and without a speech threat on this task. Results indicate that socially anxious individuals are characterized by an interpretive bias regardless of the threat manipulation. In contrast, nonanxious individuals interpreted neutral faces in a negative manner only when they were in the threat condition.