The neural correlates of social attention: automatic orienting to social and nonsocial cues

Previous evidence suggests that directional social cues (e.g., eye gaze) cause automatic shifts in attention toward gaze direction. It has been proposed that automatic attentional orienting driven by social cues (social orienting) involves a different neural network from automatic orienting driven by nonsocial cues. However, previous neuroimaging studies on social orienting have only compared gaze cues to symbolic cues, which typically engage top-down mechanisms. Therefore, we directly compared the neural activity involved in social orienting to that involved in purely automatic nonsocial orienting. Twenty participants performed a spatial cueing task consisting of social (gaze) cues and automatic nonsocial (peripheral squares) cues presented at short and long stimulus (cue-to-target) onset asynchronies (SOA), while undergoing fMRI. Behaviorally, a facilitation effect was found for both cue types at the short SOA, while an inhibitory effect (inhibition of return: IOR) was found only for nonsocial cues at the long SOA. Imaging results demonstrated that social and nonsocial cues recruited a largely overlapping fronto-parietal network. In addition, social cueing evoked greater activity in occipito-temporal regions at both SOAs, while nonsocial cueing recruited greater subcortical activity, but only for the long SOA (when IOR was found). A control experiment, including central arrow cues, confirmed that the occipito-temporal activity was at least in part due to the social nature of the cue and not simply to the location of presentation (central vs. peripheral). These results suggest an evolutionary trajectory for automatic orienting, from predominantly subcortical mechanisms for nonsocial orienting to predominantly cortical mechanisms for social orienting.     

Why does the gaze of others direct visual attention?

Viewing another person directing his or her gaze can produce automatic shifts of covert visual attention in the same direction. This holds true even when the task‐relevant target is much more likely to occur at the uncued location. These findings, along with other evidence, have been taken to suggest that gaze represents a “special” stimulus—the foundation of a social cognition system that can make inferences about the mental states of other people. However, gaze‐driven cueing effects could simply be due to spatial compatibility between cue and target. We compared the attentional effects of gaze shifts to a face with the tongue extended laterally to the left or right. When tongue direction was a nonpredictive cue, we found cueing effects from tongues that were indistinguishable from those produced by gaze. However, in contrast to previous findings with gaze, tongue cues did not overcome a validity manipulation in which targets were four times more likely to appear at the uncued location. We conclude that simple attentional cueing effects from gaze may be better explained by spatial compatibility, and that more complex, unique features of cueing from gaze may be better indices into perceptual systems specialized for social cognition.     

Is chimpanzee (Pan troglodytes) spatial attention reflexively triggered by gaze cue?

Humans show a reflexive shift in spatial attention triggered by gaze cues. Chimpanzees (Pan troglodytes) have an excellent ability to follow another's gaze, but they exhibit a limited capacity to engage in triadic interactions based on joint attention, suggesting the possibility of contributions of the different mechanisms underlying joint attention between humans and chimpanzees. The present study thus examined how the chimpanzee's visual spatial attention is triggered by gaze cues. Two chimpanzees showed no clear signs of attention shift triggered by various kinds of nonfacial and facial stimuli with averted gaze under the letter-discrimination tasks but showed significant cueing effects when the head-turning cue was presented in a quasi-dynamic manner. These cueing effects were, however, affected by the predictability of the gaze cue: Highly predictive gaze cues caused stronger cueing effects than less predictive cues. Thus, these results suggest that the shift in spatial attention caused by gaze cues does occur in chimpanzees, but, in contrast to humans, vulnerability against the cue predictability suggests that the voluntary mechanism contributes more dominantly than the reflexive mechanism to this attention shift.     

The role of the oculomotor system in covert social attention

Observing a change in gaze direction triggers a reflexive shift of attention and appears to engage the eye-movement system. However, the functional relationship between social attention and this oculomotor activation is unclear. One extremely influential hypothesis is that the preparation of a saccadic eye movement is necessary and sufficient for a covert, reflexive shift of attention (the premotor theory of attention; Rizzolatti et al., 1994). Surprisingly, this theory has not been directly tested with respect to reflexive gaze cueing. In order to address this issue, gaze cueing, peripheral cueing, and arrow cueing were examined under conditions in which some stimuli appeared at locations that could not become the goal of a saccadic eye movement. It was observed that peripheral cues failed to elicit reflexive attentional orienting when targets appeared beyond the range of eye movements. Similarly, nonpredictive arrow cues were ineffective when targets could not become the goal of a saccade. In contrast, significant gaze-cueing effects were still observed when targets were beyond the range of eye movements. These data demonstrate that the mechanisms involved in gaze cueing are dissociated from those involved in exogenous orienting to peripheral or arrow cues. Furthermore, the findings suggest that, unlike peripheral cueing and reflexive arrow cueing, gaze cueing is independent of oculomotor control. We conclude that the premotor theory does not offer a compelling explanation for gaze cueing.     

Not afraid to trust you: Trustworthiness moderates gaze cueing but not in highly anxious participants

Gaze cueing (i.e., the shifting of person B's attention by following person A's gaze) is closely linked with human interaction and learning. To make the most of this connection, researchers need to investigate possible moderators enhancing or reducing the extent of this attentional shifting. In this study we used a gaze cueing paradigm to demonstrate that the perceived trustworthiness of a cueing person constitutes such a moderator for female participants. Our results show a significant interaction between perceived trustworthiness and the response time trade-off between valid and invalid gaze cues [gaze cueing effect (GCE)], as manifested in greater following of a person's gaze if this person was trustworthy as opposed to the following of an untrustworthy person's gaze. An additional exploratory analysis showed potentially moderating influences of trait-anxiety on this interaction (p = .057). The affective background of the experiment (i.e., using positive or negative target stimuli) had no influence.     

Gaze and arrow cueing of attention reveals individual differences along the autism spectrum as a function of target context

Observing averted gaze results in a reflexive shift of attention to the gazed‐at location. In two experiments, participants scoring high and low on the Autism‐Spectrum Quotient questionnaire (AQ; Baron‐Cohen, Wheelwright, Skinner, Martin, & Clubley, 2001 ) observed arrow and gaze cues to investigate cueing effect magnitude as a function of the context in which peripheral targets could appear. While identical cueing effects were found with gaze and arrow cues, the more striking results concerned target stimuli. In Experiment 1, targets could appear on a peripheral face, or on scrambled face parts. Overall, greater cueing effects were found when the target appeared on a face. However, this face bias was only observed in participants with low AQ scores, whereas high AQ scorers oriented more to scrambled features. Experiment 2 found equal cueing to targets appearing on tools, as compared with tool parts. However, individual differences were again observed, where low AQ scorers showed larger cueing towards tools, while high scorers oriented more to scrambled parts, as in Experiment 1. These results support the idea that low AQ individuals orient strongly to objects attended by others. However, since the same results were found for arrow cues, this effect may generalize to all central cues to attention. High AQ scorers possessing many more autistic‐like traits tended to orient more to scrambled shapes, perhaps reflecting a bias for orienting to local details.     

A direct link between gaze perception and social attention

How information is exchanged between the cognitive mechanisms responsible for gaze perception and social attention is unclear. These systems could be independent; the "gaze cueing" effect could emerge from the activation of a general-purpose attentional mechanism that is ignorant of the social nature of the gaze cue. Alternatively, orienting to social gaze direction might be directly determined by the operation of cognitive mechanisms specifically dedicated to gaze perception. This second notion is the dominant assumption in the literature, but there is little direct support for this account. Here, we systematically manipulated observers' perception of gaze direction by implementing a gaze adaptation paradigm. Gaze cueing was reduced only in conditions where perception of specific averted gaze stimuli was impaired (Experiment 1). Adaptation to a pointing stimulus failed to impact gaze cueing (Experiment 2). Overall, these data suggest a direct link between the specific operation of gaze perception mechanisms and the consequential orienting of attention.     

Resolving conflicting views: Gaze and arrow cues do not trigger rapid reflexive shifts of attention

It has become widely accepted that the direction of another individual's eye gaze induces rapid, automatic, attentional orienting, due to it being such a vital cue as to where in our environment we should attend. This automatic orienting has also been associated with the directional-arrow cues used in studies of spatial attention. Here, we present evidence that the response-time cueing effects reported for spatially nonpredictive gaze and arrow cues are not the result of rapid, automatic shifts of attention. For both cue types, response-time effects were observed only for long-duration cue and target stimuli that overlapped temporally, were largest when the cues were presented simultaneously with the response-relevant target, and were driven by a slowing of responses for invalidly cued targets rather than speeding for validly cued ones. These results argue against automatic attention-orienting accounts and support a novel spatial-incongruency explanation for a whole class of rapid behavioural cueing effects.     

眼睛注视线索提示效应: 内源性注意还是外源性注意?

采用改进的Posner视-空间线索提示范式, 对眼睛注视线索提示效应(eyes gaze cueing effect)的加工机制进行了探讨。实验一考察注视提示线索对空间Stroop效应的影响; 实验二考察注视提示线索对特征抽取和特征整合的影响。实验结果显示: 注视线索提示有效时的空间Stroop效应显著大于提示无效的情景; 在单一特征搜索与特征联合搜索任务中, 注视线索提示效应无差别。这说明, 注视线索通过在头脑里形成空间方位表征诱导注意转移; 注视线索通过影响特征抽取、而非特征整合阶段, 对客体加工产生易化。本研究支持注视线索提示效应属于内源性注意的观点。     

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.     

Bicultural self‐defense in consumer contexts: Self‐protection motives are the basis for contrast versus assimilation to cultural cues

Studies of social judgment found that the way bicultural individuals respond to cultural cues depends on their cultural identity structure. Biculturals differ in the degree to which they represent their two cultural identities as integrated (vs. nonintegrated), which is assessed as high (vs. low) bicultural identity integration (BII), respectively. High BII individuals assimilate to cultural cues, yet low BII individuals contrast to these cues. The current studies reveal that this dynamic extends to consumer behavior and elucidate the underlying psychological mechanism. We found that high (low) BII individuals exhibit assimilation (contrast) responses to cultural cues in consumer information‐seeking and choice. Furthermore, the pattern occurs with both subliminal (study 1) and supraliminal (study 2) cultural primes, and is mediated by the experience of identity exclusion threat (study 2). Results suggest that the interactive effect of BII and cultural cues arises from nonconscious defense against the exclusion of a cultural identity. Implications for self‐protective processes, automatic behavior, and marketing are discussed.     

Spatial cueing by social versus nonsocial directional signals

A cost-benefit analysis was used to investigate whether reflexive effects in a spatial cueing task are stronger when target location is cued by another person's gaze rather than arrows because the relative contribution of attentional shifts versus automatic priming is greater in the case of gaze cues. Across four experiments, nonpredictive arrows triggered rapid facilitatory, inhibition-less priming that peaked at 300-500ms SOA and then died away; across three experiments, nonpredictive gaze cues triggered facilitation-plus-costs at SOAs of 300-400ms or more, suggesting that gaze cues trigger stronger (and longer) attentional effects. At 200 ms SOA, gaze cues triggered facilitation-without-cost, consistent with the view that facilitatory effects accrue more rapidly due to earlier automatic priming, whereas costs are manifest slightly later, when attentional effects come online. There was some evidence that nonpredictive gaze cues trigger long-lasting congruency effects so long as observers maintain their preparedness to respond. Findings support the view that gaze is a unique symbolic directional cue.     

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.     

Inhibition of return in response to gaze cues: The roles of time course and fixation cue

Recent studies have demonstrated that orienting of attention in response to nonpredictive gaze cues arises rapidly and automatically, in a similar fashion to peripheral sudden onset cueing. However, while peripheral cues consistently elicit inhibition of return (IOR) at about 300 ms following cue onset, very little is known about inhibition effects in response to gaze cues. The present experiments systematically examined the conditions under which IOR arises with such cues. Reliable inhibition effects were obtained. Importantly, IOR emerged only at long cue-target intervals and only when a second cue actively triggered attention away from the cued location. This suggests that compared to sudden onset cueing, gaze cueing results in both prolonged facilitation and a delayed onset of inhibition processes. Thus, although both types of cues elicit very similar orienting effects in terms of their basic behavioural outcomes, there are more subtle differences between gaze and peripheral cues with respect to the maintenance and quality of those cueing effects across time.     

Eye gaze versus arrows as spatial cues: two qualitatively different modes of attentional selection

This study aimed to evaluate the type of attentional selection (location- and/or object-based) triggered by two different types of central noninformative cues: eye gaze and arrows. Two rectangular objects were presented in the visual field, and subjects' attention was directed to the end of a rectangle via the observation of noninformative directional arrows or eye gaze. Similar experiments with peripheral cues have shown an object-based effect: faster target identification when the target is presented on the cued object as compared to the uncued object, even when the distance between target and cue was the same. The three reported experiments aimed to compare the location- and object-based attentional orienting observed with arrows and eye gaze, in order to dissociate the orienting mechanisms underlying the two types of orienting cues. Results showed similar cueing effects on the cued versus oppositely cued locations for the two cue types, replicating several studies with nonpredictive gaze and arrow cues. However, a pure object-based effect occurred only when an arrow cue was presented, whereas a pure location-based effect was only found for eye-gaze cues. It is suggested that attention is nonspecifically directed to nearby objects when a noninformative arrow is used as cue, whereas it is selectively directed to a specific cued location when noninformative eye gaze is used. This may be mediated by theory of mind mechanisms.     

Watch out! Directional threat-related postures cue attention and the eyes

Previous work indicates that threatening facial expressions with averted eye gaze can act as a signal of imminent danger, enhancing attentional orienting in the gazed-at direction. However, this threat-related gaze-cueing effect is only present in individuals reporting high levels of anxiety. The present study used eye tracking to investigate whether additional directional social cues, such as averted angry and fearful human body postures, not only cue attention, but also the eyes. The data show that although body direction did not predict target location, anxious individuals made faster eye movements when fearful or angry postures were facing towards (congruent condition) rather than away (incongruent condition) from peripheral targets. Our results provide evidence for attentional cueing in response to threat-related directional body postures in those with anxiety. This suggests that for such individuals, attention is guided by threatening social stimuli in ways that can influence and bias eye movement behaviour.     

The influence of social and symbolic cues on observers' gaze behaviour

Research has shown that social and symbolic cues presented in isolation and at fixation have strong effects on observers, but it is unclear how cues compare when they are presented away from fixation and embedded in natural scenes. We here compare the effects of two types of social cue (gaze and pointing gestures) and one type of symbolic cue (arrow signs) on eye movements of observers under two viewing conditions (free viewing vs. a memory task). The results suggest that social cues are looked at more quickly, for longer and more frequently than the symbolic arrow cues. An analysis of saccades initiated from the cue suggests that the pointing cue leads to stronger cueing than the gaze and the arrow cue. While the task had only a weak influence on gaze orienting to the cues, stronger cue following was found for free viewing compared to the memory task.     

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。     

The illusion of control: Sequential dependencies underlie contingent attentional capture

The degree to which humans have top-down control over which information they process remains a central debate within the attention literature. Most of the evidence supporting the top-down control of visuospatial attention has come from cueing paradigms in which target stimuli are preceded by cues that are similar or dissimilar from the target. These studies find that the cues similar to targets capture attention, but dissimilar cues do not, suggesting the top-down control of attention. Here, we used a modified cueing paradigm to investigate an alternative possibility that the cue type differences are due to sequential dependency effects occurring between cue and target processing rather than the top-down control of attention. When individuals searched for color targets, we replicated contingent capture effects in RTs, which are susceptible to sequential dependencies, but memory performance was always best at the cued locations, regardless of the cue’s identity. When individuals searched for onset targets, we observed contingent capture in both tasks. These results demonstrate the utility of the memory probe paradigm and suggest an asymmetry between how strongly onsets and color defined cues capture attention.