Reflexive orienting in response to short- and long-duration gaze cues in young,young-old,and old-old adults

Shifting visual focus on the basis of the perceived gaze direction of another person is one form of joint attention. In the present study, we investigated whether this socially relevant form of orienting is reflexive and whether it is influenced by age. Green and Woldorff (Cognition 122:96–101, 2012) argued that rapid cueing effects (i.e., faster responses to validly than to invalidly cued targets) were limited to conditions in which a cue overlapped in time with a target. They attributed slower responses following invalid cues to the time needed to resolve the incongruent spatial information provided by the concurrently presented cue and target. In the present study, we examined the orienting responses of young (18–31 years), young-old (60–74 years), and old-old (75–91 years) adults following uninformative central gaze cues that overlapped in time with the target (Exp. 1) or that were removed prior to target presentation (Exp. 2). When the cue and target overlapped, all three groups localized validly cued targets more quickly than invalidly cued targets, and validity effects emerged earlier for the two younger groups (at 100 ms post-cue-onset) than for the old-old group (at 300 ms post-cue-onset). With a short-duration cue (Exp. 2), validity effects developed rapidly (by 100 ms) for all three groups, suggesting that validity effects resulted from reflexive orienting based on the gaze cue information rather than from cue–target conflict. Thus, although old-old adults may be slow to disengage from persistent gaze cues, attention continues to be reflexively guided by gaze cues late in life.     

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.     

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.     

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.     

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.     

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.     

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.     

Reflexive orienting to gaze is not luminance dependent

In the investigation of reflexive orienting to cues, two major theories have emerged: One proposes that transients created by the cue trigger attentional shifts, whereas the other argues that object changes are responsible for instigating orienting. In the present study, we examined whether luminance transients produced by the cue can generate reflexive orienting to gaze. Using a temporal order judgment paradigm under luminant or subjectively equiluminant conditions, participants judged which of two peripheral targets onset first. An uninformative gaze cue served to reflexively shift attention toward one object location, thereby temporally prioritizing the target presented there. The results revealed that attention was successfully shifted toward the cued object, as was evidenced by the participants’ selecting the cued object as appearing first significantly more often than the uncued object, even when the two onset simultaneously. Critically, the results were comparable across luminance conditions. Our findings reveal that luminance transients are not necessary for triggering orienting to gaze cues. We suggest that the orienting observed here can be better explained via an object-based hypothesis whereby object changes, not transients, trigger reflexive orienting.     

Arrow-elicited cueing effects at short intervals: Rapid attentional orienting or cue-target stimulus conflict?

The observation of cueing effects (faster responses for cued than uncued targets) rapidly following centrally-presented arrows has led to the suggestion that arrows trigger rapid automatic shifts of spatial attention. However, these effects have primarily been observed during easy target-detection tasks when both cue and target remain on the screen until the behavioral response. We manipulated stimulus duration and task difficulty in an attention-cueing experiment to explore non-attentional explanations for rapid cueing effects. Contrary to attention-based predictions, short-interval cueing effects were observed only for long-duration cue and target stimuli, occurred even when the cue and target were presented simultaneously, and were driven by slowing of the uncued-target responses, rather than any facilitation for cued targets. We propose that, under these long-duration, short-interval conditions, the processing of the cue and target interact more extensively in the brain, and that when the cue and target convey incongruent spatial information (i.e., on invalidly cued trials) it leads to conflict-related slowing of responses.     

On the uniqueness of attentional capture by uninformative gaze cues: facilitation interacts with the Simon effect and is rarely followed by IOR.

Orienting to an uninformative peripheral cue is characterized by a brief facilitation followed by a long-lasting inhibition once attention is removed from the cued location. Although central gaze cues cause reflexive orienting, the inhibitory effect that is relatively ubiquitous following exogenous orienting to uninformative peripheral cues has been relatively rare. We hypothesized that IOR might be seen following gaze-induced orienting if attention were effectively returned to centre by a return gaze or return flash. The timecourse of gaze-directed orienting was measured by varying the interval between the gaze cue and a peripheral target requiring an orientation discrimination (permitting measurement of the Simon effect). Significant facilitation was observed at all but the longest SOA tested, 2,880 ms, by which time the facilitation had disappeared with no evidence of IOR. Gaze-induced cuing (which was unaffected by return cue condition) interacted with the Simon effect, decreasing it at the gazed-at location, a pattern that is not seen with more typical endogenous and exogenous cuing.     

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.     

Orienting of attention with eye and arrow cues and the effect of overtraining

In contrast to the classical distinction between a controlled orienting of attention induced by central cues and an automatic capture induced by peripheral cues, recent studies suggest that central cues, such as eyes and arrows, may trigger a reflexive-like attentional shift. Yet, it is not clear if the attention shifts induced by these two cues are similar or if they differ in some important aspect. To answer this question, in Experiment 1 we directly compared eye and arrow cues in a counter-predictive paradigm while in Experiment 2 we compared the above cues with a different symbolic cue. Finally, in Experiment 3 we tested the role of over-learned associations in cueing effects. The results provide evidence that eyes and arrows induce identical behavioural effects. Moreover, they show that over-learned associations between spatially neutral symbols and the cued location play an important role in yielding early attentional 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。     

Differential time course of implicit and explicit cueing by colour and orientation in visual search

Using a cued conjunction search task, Anderson, Heinke, and Humphreys (2010) demonstrated larger effects from cueing target colour than from cueing target orientation. In this study, we separated the implicit (nonexpectation-dependent) and explicit (expectation-dependent) effects of orientation and colour visual cues. In Experiment 1, we replicated the original findings for short cue durations (100–200 ms), demonstrating that cues matching the physical property of the target on 80% of trials exert a rapid effect on search. These early cueing effects on reaction times were supported by evidence of guidance from cues on early eye movements. Experiment 2 introduced a feature to the cue that randomly matched the colour or orientation of the target. When cue orientation was predictive, there were strong implicit effects based on whether the colour of the cue and target matched. When cue colour was predictive, there were only weak effects from the cue's orientation. Implicit effects from cue colour remained when orientation-predictive cues were used and colour was unlikely to predict the target (Experiment 3). The data suggest that strong effects of colour cueing result from a combination of implicit and explicit processes, whereas effects from orientation cues are largely limited to the explicit guidance of visual search.     

Visual orienting in response to attentional cues: Spatial correspondence is critical,conscious awareness is not

Three experiments examined visual orienting in response to spatial precues. In Experiments 1 and 2, attentional effects of central letters were stimulus driven: Orienting was dependent on the spatial layout of the cue display. When there were no correspondences between spatial features of the cue display and target location, attentional effects were absent, despite a conscious intention to orient in response to the symbolic information carried by the cue letters. In Experiment 3 clear orienting effects were observed when target location corresponded with spatial features of the cue display, but the magnitude of these effects was unaffected by whether participants were aware or unaware of the cue–target relationship. These findings are consistent with the view that (1) spatial correspondences between cues and targets are a critical factor driving visual orienting in cueing paradigms, and (2) attentional effects of spatial precues are largely independent of participants’ conscious awareness of the cue–target relationship.     

Testing whether gaze cues and arrow cues produce reflexive or volitional shifts of attention

It has been suggested that two types of uninformative central cues produce reflexive orienting: gaze and arrow cues. Using the criterion that voluntary shifts of attention facilitate both response speed and perceptual accuracy, whereas reflexive shifts of attention facilitate only response speed (Prinzmetal, McCool, & Park, 2005), we tested whether these cues produce reflexive or volitional shifts of attention. A cued letter discrimination task was used with both gaze (Experiments 1A and 1B) and arrow (Experiments 2A and 2B) cues, in which participants responded to the identity of the target letter. In the response time (respond speed) tasks, participants were asked to respond as quickly as possible to the target; in the accuracy (perceptual quality) tasks, participants were asked to respond as accurately as possible. For both cue types, compatible cues were found to facilitate response speed but not perceptual accuracy, indicating that both gaze and arrow cues generate reflexive shifts in attention.     

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 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.     

Poor vigilance affects attentional orienting triggered by central uninformative gaze and arrow cues

Behaviour and neuroimaging studies have shown that poor vigilance (PV) due to sleep deprivation (SD) negatively affects exogenously cued selective attention. In the current study, we assessed the impact of PV due to both partial SD and night-time hours on reflexive attentional orienting triggered by central un-informative eye-gaze and arrow cues. Subjective mood and interference performance in emotional Stroop task were also investigated. Twenty healthy participants performed spatial cueing tasks using central directional arrow and eye-gaze as a cue to orient attention. The target was a word written in different coloured inks. The participant’s task was to identify the colour of the ink while ignoring the semantic content of the word (with negative or neutral emotional valence). The experiment took place on 2 days. On the first day, each participant performed a 10-min training session of the spatial cueing task. On the second day, half of participants performed the task once at 4:30 p.m. (BSL) and once at 6:30 a.m. (PV), whereas the other half performed the task in the reversed order. Results showed that mean reaction times on the spatial cueing tasks were worsened by PV, although gaze paradigm was more resistant to this effect as compared to the arrow paradigm. Moreover, PV negatively affects attentional orienting triggered by both central un-informative gaze and arrow cues. Finally, prolonged wakefulness affects self-reported mood but does not influence interference control in emotional Stroop task.     

Automaticity and the capture of attention by a peripheral display change

The proposal that peripheral visual changes (cues) tend to summon attention automatically was tested by studying the effect of peripheral cueing on simple detection latency. Delay between cue onset and target onset, the contingent relationship between cue location and target location, and instructions to subjects were manipulated. Results showed that a peripheral display change could capture attention even when the target was far more likely to appear at an uncued location. When subjects were explicitly informed that targets were likely to appear away from the cued location they were able to suppress this effect, but were unable completely to reverse it by rapidly orienting attention towards the uncued side. Hence the process appears to be automatic in the sense that it occurs unless there are explicit instructions to the contrary. With explicit instructions the processing operation can be suppressed, but not completely reversed. This work was supported by the U.K. Admiralty Research Establishment (Research Agreement No. 53482).