The Representation Of Threatening Gaze Cueing And Its Cognitive And Neural Basis

Human beings can easily discern where another person's eyes are looking because the morphology of our eyes is unique among primates in that our sclera is more widely exposed and it is much paler in color than our iris or skin.This unique characteristic can be considered an adaptation that facilitates more effective social interaction using gaze signals.The direction of another person's eye gaze is correlated with potential resources(e.g.,food)and threats(e.g.,a predator),which makes it essential to respond appropriately to gaze cues.Moreover,the ability to shift attention to follow the same target that others are watching is crucial for social learning,collaboration,and understanding others' intentions,because it enables us to “share” the same idea or topic.Therefore,it is reasonable to assume that humans evolved the tendency to shift attention to follow the region and gaze direction of other people's eyes,a phenomenon that is often referred to as gaze cueing.Generally,shorter reaction times(RTs)are observed when a target appears at a spatial location congruent with that indicated by the gaze direction of a face,than when a subsequent target appears at a location that is incongruent with the direction of gaze cues,which is known as the gaze-cuing effect(GCE).Although gaze cueing has been shaped by natural selection during our evolutionary history,there is strong evidence that it is sensitive to two kinds of social modulators.The first type of social modulator was visual features of the face.For instance,angry(changeable visual features)faces have been shown to produce a greater gaze cueing effect than neutral faces.Social knowledge about individual faces,separate from their physical characteristics,is the second type of social modulator that influences gaze cuing.For example,a greater gaze cueing effect has been observed for faces of individuals who belong to a threatening group.These fingdings indicated that both visual threatening features(visual threat)and the social knowledge about threat(social threat)could modulate gaze cuing,a phenomenon named threatening gaze cuing superiority effect.Study one aims to use a standard gaze-cuing paradigm to figure out the way how visual/social threat gates social attention in humans.In other words,we want to investigate whether visual/social threatening cues draw attention faster or whether,once detected,visual-threat-related/social-threat-related facial stimuli hold attention longer,or both.In experiment 1,the greater gaze-cuing effect only emerged for visual threatening cues at the 800 ms SOA in the gaze-cuing task(a spatial orienting task).In the congruent condition,the RTs for the visual threatening gaze was shorer than for the nonthreatening gaze,which means visual threatening information did draw attention faster than nonthreatening information.Moreover,it took participants less time(shorter RTs)to disengage from the gaze direction of a visual threatening face than a nonthreatening in-group face in the incongruent condition,which suggests that the visual threatening gaze did not hold attention longer than did the nonthreatening gaze.In experiment 2,the greater gaze-cuing effect only emerged for social threatening cues at the 200 ms SOA in the gaze-cuing task.Interestingly,in the congruent condition,there was no difference between the RTs for the social threatening gaze or the nonthreatening gaze,which means intergroup threatening information did not draw attention faster than did nonthreatening information.However,it took participants more time(longer RTs)to disengage from the gaze direction of a social threatening face than a nonthreatening face in the incongruent condition,which suggests that the social threatening gaze did hold attention longer than did the nonthreatening gaze.Those results suggest that the representations of visual threanting gaze cueing and socail threatening gaze cueing were different.Study two utilized two experiments aimed to investgate the timing and magnitude of visual thteatening and social threatening gaze cueing effect with the event-related potential technique(ERP).On one hand,in study 5,greater gaze cueing effect also emerged for visual threatenging gaze at 800 ms SOA,and the representation of it was vigilance for visual threatening gaze,which is consistent with study 3.Importanly,the N2 amplitudes elicited by congruent visual threnting gaze,but not incongruent condition,were significant larger than congruent non-threnting gaze,which means visual threatening gaze cueing effect occurs at the later process of cognition.On the other hand,in study 6,greater gaze cueing effect emerged for social threatenging gaze at 200 ms SOA,and the representation of it was difficulty disengage from social threatening gaze,which is consistent with study 4.Importanly,the P1 amplitudes elicited by incongruent social threnting gaze,but not congruent condition,were significant larger than incongruent non-threnting gaze,which means social threatening gaze cueing effect occurs at the early process of cognition.We conducted study three to examine wether visual threat and social threat gate social attention by activating a network resembling that is thought to be involved in drawing or/and holding attention.Functional magnetic resonance imaging(fMRI)at 3T was performed while participants take part in the gaze cuing task.We hypothesized that either the amygdala(a central structure in a neural mechanism involved in attention vigilance to threat)or the PFC(a central structure in a neural mechanism involved in the difficulty to disengage from threat),or both of these areas,would be activated when participants were shown threatening faces.As expected,in experiment 3,the imaging data suggested that attention vigilance by visual threatening cues in the congruent trials was supported by threat detect(attention vigilance)networks only at the 800 ms SOA.Moreover,the activity of the amygdala was correlated with the gaze cueing effect of visual threat gaze in the congruent condition.In experiment 4,the imaging data suggested that attention holding by social threatening cues in the incongruent trials was supported by attention control(difficulty to disengage from threat)networks only at the 200 ms SOA.Moreover,the activity of the mPFC,right DLPFC were correlated with the reaction time of social threatening cues in the incongruent condition.In the study four,we aimed to provide reverse proof of the results of study three.Previous sudies shown that the dorsolateral prefrontal cortex(DLPFC)is involved in attention allocation,and is related to the ability to control the attentional focus in presence of threatening stimuli.In particular,the left DLPFC might reduce attentional engagement toward threat,whereas the right DLPFC might be responsible for attentional allocation on threatening stimuli.In experiment 7,the greater GCE for visual threatening faces' gaze was found,participants showed facilitated attention to visual threatening gaze and attentional avoidance of visual threatening gaze.Besides,this study assessed the effect of the transcranial direct current stimulation(tDCS)on the GCE for threatening gaze cue.To refine optimal stimulation parameters,DLPFC stimulation using a common electrode montage was compared with sham.Forty-four healthy volunteers received 20 minutes of active or sham DLPFC stimulation before completing computerized attentional processing tasks,including a cue-target paradigm.Relative to sham stimulation,participants receiving simultaneous anodal stimulation of left DLPFC and cathodal stimulation of right DLPFC(bipolar-balanced montage)showed reduced GCE to visual threatening gaze cue.In experiment 8,the greater GCE for social threatening faces' gaze was found,participants showed difficulty to disengage from social threatening gaze.Relative to sham stimulation,participants receiving simultaneous bipolar-balanced montage on DLPFC showed reduced GCE to socail threatening gaze cue.Taken together,these foundings suggest that visual and social threat affect the two path ways of gaze cuing respectively.Based on the evidences of present study,the visual threat and the social threat might affect gaze cueing through different ways.First,the representation of visual threatening gaze cueing effect was vigilance to the visual threatening cues,whreas the representation of social threatening gaze cueing was diffuclty to disengage from social threatening gaze.Second,visual threatening gaze cueing effect occurs at the later process of cognition,whreas social threatening gaze cueing effect occurs at the eraly process of cognition.Moreover,the nural basis of visual threatening gaze cueing effect was the threat detection system,whreas the nural basis of social threatening gaze cueing effect was the attention control system.