Reflexive joint attention depends on lateralized cortical connections

Joint attention, the tendency to spontaneously direct attention to where someone else is looking, has been thought to occur because eye direction provides a reliable cue to the presence of important events in the environment. We have discovered, however, that adults will shift their attention to where a schematic face is looking—even when gaze direction does not predict any events in the environment. Research with 2 split-brain patients revealed that this reflexive joint attention is lateralized to a single hemisphere. Moreover, although this phenomenon could be inhibited by inversion of a face, eyes alone produced reflexive shifts of attention. Consistent with recent functional neuroimaging studies, these results suggest that lateralized cortical connections between (a) temporal lobe subsystems specialized for processing upright faces and gaze and (b) the parietal area specialized for orienting spatial attention underlie human reflexive shifts of attention in response to gaze direction.     

Does gaze direction really trigger a reflexive shift of spatial attention?

Previous studies have found that the gaze direction of a centrally presented face facilitates response time (RT) to a lone peripheral target. The widely accepted interpretation of this finding is that gaze direction triggers a cortically mediated reflexive shift of spatial attention. In the present study we tested an alternative explanation, that a target appearing abruptly on its own in the visual field triggers a subcortically mediated reflexive shift of spatial attention, which is modulated by compatibility with gaze direction. Using central gaze cues, we compared RT to a single peripheral onset target with RT to a peripheral onset target accompanied by an equivalent distractor at the mirror opposite location. In both cases the facilitation effect was the same, demonstrating conclusively that the observed orienting is attributable to the reflexive effects of the gaze cue.     

The eyes have it!: an fMRI investigation

For the past several years it has been thought that cues, such as eye direction, can trigger reflexive shifts in attention because of their biological relevance and their specialized neural architecture. However, very recently, reported that other stimuli, such as arrows, trigger reflexive shifts in attention in a manner that is behaviourally identical to those triggered by eyes. Nevertheless these authors speculated that reflexive orienting to gaze direction may be subserved by a neural system-the superior temporal sulcus (STS)-that is specialized for processing eyes. The present study presents fMRI data that provide direct and compelling empirical support to this proposal. Subjects were presented with fixation stimuli that, based on instruction, could be perceived as eyes or as another type of directional cue. Both produced equivalent shifts in reflexive attention, replicating Ristic et al. However, the neural systems subserving the two forms of orienting were not equivalent-with the STS being engaged exceptionally when the fixation stimulus was perceived as eyes.     

The eyes have it! Reflexive orienting is triggered by nonpredictive gaze

Normal subjects were presented with a simple line drawing of a face looking left, right, or straight ahead. A target letter F or T then appeared to the left or the right of the face. All subjects participated in target detection, localization, and identification response conditions. Although subjects were told that the line drawing’s gaze direction (the cue) did not predict where the target would occur, response time in all three conditions was reliably faster when gaze was toward versus away from the target. This study provides evidence for covert, reflexive orienting to peripheral locations in response to uninformative gaze shifts presented at fixation. The implications for theories of social attention and visual orienting are discussed, and the brain mechanisms that may underlie this phenomenon are considered.     

Gaze Perception Triggers Reflexive Visuospatial Orienting

This paper seeks to bring together two previously separate research traditions: research on spatial orienting within the visual cueing paradigm and research into social cognition, addressing our tendency to attend in the direction that another person looks. Cueing methodologies from mainstream attention research were adapted to test the automaticity of orienting in the direction of seen gaze. Three studies manipulated the direction of gaze in a computerized face, which appeared centrally in a frontal view during a peripheral letter-discrimination task. Experiments 1 and 2 found faster discrimination of peripheral target letters on the side the computerized face gazed towards, even though the seen gaze did not predict target side, and despite participants being asked to ignore the face. This suggests reflexive covert and/or overt orienting in the direction of seen gaze, arising even when the observer has no motivation to orient in this way. Experiment 3 found faster letter discrimination on the side the computerized face gazed towards even when participants knew that target letters were four times as likely on the opposite side. This suggests that orienting can arise in the direction of seen gaze even when counter to intentions. The experiments illustrate that methods from mainstream attention research can be usefully applied to social cognition, and that studies of spatial attention may profit from considering its social function.     

Where a person with a squint is actually looking: Gaze-cued orienting in crossed eyes

In this study, we investigated gaze-cued attention orienting when the perceived eyes are not looking in the same direction. This condition occurs in strabismus (squint). Participants were asked to detect laterally presented reaction signals preceded by schematic faces in which the direction (left, straight, or right) of the left and right eye was independently manipulated. Consistent with earlier studies, the results showed a reliable cuing effect by two eyes with parallel gaze direction. Gaze-cued orienting was also shown in a situation when one eye was averted and the other eye was looking straight ahead. The gaze cuing was not significantly stronger in the former than in the latter situation. When both eyes were either nasally or temporally averted, no shifts of visual attention were observed. The results suggest that, if both eyes are visible, the direction of both eyes is computed and integrated for the gaze-cued orienting.     

Gaze cueing as a function of perceived gaze direction

Previous studies have found that attention is automatically oriented in the direction of other people's gaze. This study directly investigated whether the perceiving gaze direction modulates the orienting of observers' attention. Gaze perception was manipulated by changing the face context (head orientation) of the gaze cue: the perceived gaze angle was increased (or decreased) when the head and gaze are congruent (or incongruent), while the local‐feature information of the eye region was preserved for all stimuli. The results showed that gaze‐cueing effects were enhanced when the perceived gaze direction was averted more toward left or right, and reduced when the perceived gaze direction was closer to direct gaze. The results suggest that gaze‐cueing effects are based on mechanisms specialized for gaze perception, and the magnitude of gaze‐cueing effects was probably a function of the perceived gaze direction.     

Dynamic emotional messages differentially affect 6-month-old infants’ attention to eyes and gaze cues

Infants often experience interactions in which caregivers use dynamic messages to convey their affective and communicative intent. These dynamic emotional messages may shape the development of emotion discrimination skills and shared attention by influencing infants’ attention to internal facial features and their responses to eye gaze cues. However, past research examining infants’ responses to emotional faces has predominantly focused on classic, stereotyped expressions (e.g., happy, sad, angry) that may not reflect the variability that infants experience in their daily interactions. The present study therefore examined forty-two 6-month-old infants’ attention to eyes vs. mouth and gaze cueing responses across multiple dynamic emotional messages that are common to infant-directed interactions. Overall, infants looked more to the eyes during messages with negative affect, but this increased attention to the eyes during these message conditions did not directly facilitate gaze cueing. Infants instead showed reliable gaze cueing only after messages with positive and neutral affect. We additionally observed gender differences in infants’ attention to internal face features and subsequent gaze cueing responses. Female infants spent more time looking at the eyes during the dynamic emotional messages and showed increased initial orienting and longer looking to gaze-cued objects following positive messages, whereas male infants showed these gaze cueing effects following neutral messages. These results suggest that variability in caregivers' communication can shape infants’ attention to and processing of emotion and gaze information.     

Automatic attentional orienting to other people’s gaze in schizophrenia

Explicit tests of social cognition have revealed pervasive deficits in schizophrenia. Less is known of automatic social cognition in schizophrenia. We used a spatial orienting task to investigate automatic shifts of attention cued by another person’s eye gaze in 29 patients and 28 controls. Central photographic images of a face with eyes shifted left or right, or looking straight ahead, preceded targets that appeared left or right of the cue. To examine automatic effects, cue direction was non-predictive of target location. Cue–target intervals were 100, 300, and 800?ms. In non-social control trials, arrows replaced eye-gaze cues. Both groups showed automatic attentional orienting indexed by faster reaction times (RTs) when arrows were congruent with target location across all cue–target intervals. Similar congruency effects were seen for eye-shift cues at 300 and 800?ms intervals, but patients showed significantly larger congruency effects at 800?ms, which were driven by delayed responses to incongruent target locations. At short 100-ms cue–target intervals, neither group showed faster RTs for congruent than for incongruent eye-shift cues, but patients were significantly slower to detect targets after direct-gaze cues. These findings conflict with previous studies using schematic line drawings of eye-shifts that have found automatic attentional orienting to be reduced in schizophrenia. Instead, our data indicate that patients display abnormalities in responding to gaze direction at various stages of gaze processing—reflected by a stronger preferential capture of attention by another person’s direct eye contact at initial stages of gaze processing and difficulties disengaging from a gazed-at location once shared attention is established.     

Anxiety and sensitivity to gaze direction in emotionally expressive faces

This study investigated the role of neutral, happy, fearful, and angry facial expressions in enhancing orienting to the direction of eye gaze. Photographs of faces with either direct or averted gaze were presented. A target letter (T or L) appeared unpredictably to the left or the right of the face, either 300 ms or 700 ms after gaze direction changed. Response times were faster in congruent conditions (i.e., when the eyes gazed toward the target) relative to incongruent conditions (when the eyes gazed away from the target letter). Facial expression did influence reaction times, but these effects were qualified by individual differences in self-reported anxiety. High trait-anxious participants showed an enhanced orienting to the eye gaze of faces with fearful expressions relative to all other expressions. In contrast, when the eyes stared straight ahead, trait anxiety was associated with slower responding when the facial expressions depicted anger. Thus, in anxiety-prone people attention is more likely to be held by an expression of anger, whereas attention is guided more potently by fearful facial expressions.     

Crossmodal spatial attention shift produced by centrally presented gaze cues1

Abstract: Despite previous failures to identify visual‐upon‐auditory spatial‐cuing effects, recent studies have demonstrated that the abrupt onset of a lateralized visual stimulus triggers a shift of spatial attention in response to auditory judgment. Nevertheless, whether a centrally presented visual stimulus orients auditory attention remained unclear. The present study investigated whether centrally presented gaze cues trigger a reflexive shift of attention in response to auditory judgment. Participants fixated on a schematic face in which the eyes looked left or right (the cue). A target sound was then presented to the left or right of the cue. Participants judged the direction of the target as quickly as possible. Even though participants were told that the gaze direction did not predict the direction of the target, the response time was significantly faster when the gaze was in the target direction than when it was in the non‐target direction. These findings provide initial evidence for visual‐upon‐auditory spatial‐cuing effects produced by centrally presented cues, suggesting that a reflexive crossmodal shift of attention does occur with a centrally presented visual stimulus.     

眼睛注视的知觉及其线索效应

对眼睛注视知觉、眼睛注视线索效应及其影响因素等相关研究进行了总结和分析。结果发现:(1)婴儿从一出生就对眼睛注视线索表现出强烈的敏感性,眼睛注视知觉对语言和社会等能力的发展有很大影响;(2)颞上沟是加工眼睛注视线索的特异神经结构,它与实时监控情绪和情感的杏仁核存在神经联结,成为社会认知神经系统的重要组成部分;(3)对眼睛注视线索的早期加工显示出特异的脑电活动模式;(4)眼睛注视线索效应与外周线索的反射式效应相类似,但持续时间较长;(5)眼睛注视线索效应不仅受面部结构信息的影响,也受自上而下加工等高水平认知因素的调节,并显示出明显的个体差异。对眼睛注视线索效应的进一步研究应涉及人格判断、喜好评价和心理理论等高级社会认知活动。     

Spatial interference between gaze direction and gaze location: A study on the eye contact effect

Perceived gaze in faces is an important social cue that influences spatial orienting of attention. In three experiments, we examined whether the social relevance of gaze direction modulated spatial interference in response selection, using three different stimuli: faces, isolated eyes, and symbolic eyes (Experiments 1, 2, and 3, respectively). Each experiment employed a variant of the spatial Stroop paradigm in which face location and gaze direction were put into conflict. Results showed a reverse congruency effect between face location to the right or left of fixation and gaze direction only for stimuli with a social meaning to participants (Experiments 1 and 2). The opposite was observed for the nonsocial stimuli used in Experiment 3. Results are explained as facilitation in response to eye contact.     

Driven from distraction: how infants respond to parents' attempts to elicit and re-direct their attention

This experiment examined how parents' verbal and non-verbal behavioral cues cause infants to shift and share attention within environments where many objects compete for infants' attention. Fifteen- and 21-month-old infants played with toys while their parent periodically shifted attention to a distal object within a larger array. Parents' attention-shifts were indicated by a change in direction of gaze, a pointing gesture, and/or verbalizations. Verbalizations were either attention-eliciting or attention-directing. In some trials parents covered their eyes to occlude line-of-gaze. Both ages seldom followed simple gaze shifts, but frequently followed gaze with-points or gaze-with-directing verbalizations. Attention-eliciting verbalizations increased infants' looks to the parent. Gaze occlusion reduced infants' responses to directing verbalizations. Responses to eliciting verbalizations increased with age. Infant receptive vocabulary did not predict attention-sharing, even when parents named objects (i.e., directing verbalizations). Implications for development of attention-sharing, language and understanding of visual attention are discussed.     

Spatial interference between gaze direction and gaze location: a study on the eye contact effect

Perceived gaze in faces is an important social cue that influences spatial orienting of attention. In three experiments, we examined whether the social relevance of gaze direction modulated spatial interference in response selection, using three different stimuli: faces, isolated eyes, and symbolic eyes (Experiments 1, 2, and 3, respectively). Each experiment employed a variant of the spatial Stroop paradigm in which face location and gaze direction were put into conflict. Results showed a reverse congruency effect between face location to the right or left of fixation and gaze direction only for stimuli with a social meaning to participants (Experiments 1 and 2). The opposite was observed for the nonsocial stimuli used in Experiment 3. Results are explained as facilitation in response to eye contact.     

Contrast polarity of eyes modulates gaze‐cueing effect1

Two experiments using a modified Posner‐type visual cueing paradigm tested the prediction that detecting the darker region of the eyes of another's gaze triggers a reflexive orienting of the observer in the direction of the gaze. A target was presented in the left or right visual‐field following a gaze‐cue with positive or negative‐image polarity (Experiment 1). In Experiment 2, the polarity of the eyes was manipulated independently of the negative polarity of the face (eye‐positive or eye‐negative‐image polarity conditions). The results showed that the response to the target presented at the side the eyes gazed toward was faster than for the target presented at the other side in the positive polarity condition (Experiment 1), whereas, in the negative polarity condition, the gaze‐cuing effect was not found. In Experiment 2, in the eye‐negative condition, a reversed gaze‐cueing effect appeared, whereas in the eye‐positive polarity condition, a typical gaze‐cueing effect was obtained. These findings suggested that the reflexive orienting of the observer shifts toward the position indicated by the darker region of the other's eyes.     

Do the eyes have it? Cues to the direction of social attention

The face communicates an impressive amount of visual information. We use it to identify its owner, how they are feeling and to help us understand what they are saying. Models of face processing have considered how we extract such meaning from the face but have ignored another important signal - eye gaze. In this article we begin by reviewing evidence from recent neurophysiological studies that suggests that the eyes constitute a special stimulus in at least two senses. First, the structure of the eyes is such that it provides us with a particularly powerful signal to the direction of another person's gaze, and second, we may have evolved neural mechanisms devoted to gaze processing. As a result, gaze direction is analysed rapidly and automatically, and is able to trigger reflexive shifts of an observer's visual attention. However, understanding where another individual is directing their attention involves more than simply analysing their gaze direction. We go on to describe research with adult participants, children and non-human primates that suggests that other cues such as head orientation and pointing gestures make significant contributions to the computation of another's direction of attention.     

Anxiety and sensitivity to eye gaze in emotional faces

This paper reports three studies in which stronger orienting to perceived eye gaze direction was revealed when observers viewed faces showing fearful or angry, compared with happy or neutral, emotional expressions. Gaze-related spatial cueing effects to laterally presented fearful faces and centrally presented angry faces were also modulated by the anxiety level of participants, with high- but not low-state anxious individuals revealing enhanced shifts of attention. In contrast, both high- and low-state anxious individuals demonstrated enhanced orienting to averted gaze when viewing laterally presented angry faces. These results provide novel evidence for the rapid integration of facial expression and gaze direction information, and for the regulation of gaze-cued attention by both the emotion conveyed in the perceived face and the degree of anxiety experienced by the observer.     

Sex differences in eye gaze and symbolic cueing of attention.

Observing a face with averted eyes results in a reflexive shift of attention to the gazed-at location. Here we present results that show that this effect is weaker in males than in females (Experiment 1). This result is predicted by the 'extreme male brain' theory of autism (Baron-Cohen, 2003), which suggests that males in the normal population should display more autism-like traits than females (e.g., poor joint attention). Indeed, participants' scores on the Autism-Spectrum Quotient (Baron-Cohen, Wheelwright, Stott, Bolton, & Goodyear, 2001) negatively correlated with cueing magnitude. Furthermore, exogenous orienting did not differ between the sexes in two peripheral cueing experiments (Experiments 2a and 2b). However, a final experiment showed that using nonpredictive arrows instead of eyes as a central cue also revealed a large gender difference. This demonstrates that reduced orienting from central cues in males generalizes beyond gaze cues. These results show that while peripheral cueing is equivalent in the male and female brains, the attention systems of the two sexes treat noninformative symbolic cues very differently.     

Gaze cueing elicited by emotional faces is influenced by affective context

When we observe someone shift their gaze to a peripheral event or object, a corresponding shift in our own attention often follows. This social orienting response, joint attention, has been studied in the laboratory using the gaze cueing paradigm. Here, we investigate the combined influence of the emotional content displayed in two critical components of a joint attention episode: The facial expression of the cue face, and the affective nature of the to-be-localized target object. Hence, we presented participants with happy and disgusted faces as cueing stimuli, and neutral (Experiment 1), pleasant and unpleasant (Experiment 2) pictures as target stimuli. The findings demonstrate an effect of ‘emotional context’ confined to participants viewing pleasant pictures. Specifically, gaze cueing was boosted when the emotion of the gazing face (i.e., happy) matched that of the targets (pleasant). Demonstrating modulation by emotional context highlights the vital flexibility that a successful joint attention system requires in order to assist our navigation of the social world.