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.     

Attention orienting by eye gaze and arrows reveals flexibility to environmental changes

This study aimed to evaluate the difference in non-predictive cues between gaze and arrows in attention orienting. Attention orienting was investigated with gaze or arrows as separate cues in a simple condition (i.e., block design) in Experiment 1 and in an unpredictable condition (i.e., randomized design) in Experiment 2. Two kinds of sound (voice and tone) stimuli were used as targets. Results showed that gaze and arrow cues induced enhanced attention orienting to a voice versus tone target in the block condition. However, in the randomized condition, enhanced attention orienting to a voice versus tone target was found in gaze but not arrow cues. The congruency of the meaning between a social cue (i.e., gaze) and a social target (i.e., voice) was clear in the randomized but not blocked design, because social gaze and non-social arrow cues were implemented in the same block. Thus, attention orienting might be mediated by the associated relationship of cue–target in a randomized condition, as an enhanced orienting effect was found when the associated relationship of cue–target was strong (i.e., social cue and target). The present study suggests that the difference in attention orienting between gaze and arrows is apparent in a randomized design (the unpredictable condition), and people employ a flexibly strategy of orienting to better respond to environmental changes.     

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.     

The owl and the pussycat: Gaze cues and visuospatial orienting

Recent research has shown that nonpredictive gaze cues trigger reflexive shifts in attention toward the looked-at location. But just how generalizable is this spatial cuing effect? In particular, are people especially tuned to gaze cues provided by conspecifics, or can comparable shifts in visual attention be triggered by other cue providers and directional cues? To investigate these issues, we used a standard cuing paradigm to compare the attentional orienting produced by different cue providers (i.e., animate vs. inanimate) and directional cues (i.e., eyes vs. arrows). The results of three experiments revealed that attentional orienting was insensitive to both the identity of the cue provider and the nature of the triggering cue. However, compared with arrows, gaze cues prompted a general enhancement in the efficiency of processing operations. We consider the implications of these findings for accounts of reflexive visual orienting.     

Reflexive orienting by central arrows: Evidence from the inattentional blindness task

It was demonstrated that central arrows produce orienting of attention even when they are nonpredictive as to the target location. This finding was suggested to indicate reflexive orienting of attention by central arrows. However, it is not clear whether central arrows can produce an attentional effect without awareness. In two experiments, using a variation of the inattentional blindness task, we examine whether orienting of attention by a central arrow can be demonstrated without conscious perception of the arrow. We found that attention could be directed to the cued location even when the arrow was not consciously perceived.     

Eye gaze is not unique: automatic orienting in response to uninformative arrows

Recent studies (Driver et al., 1999; Friesen & Kingstone, 1998; Langton & Bruce, 1999) have argued that the perception of eye gaze may be unique, as compared with other symbolic cues (e.g., arrows), in being able to automatically trigger attentional orienting. In Experiment 1, 17 participants took part in a visuospatial orienting task to investigate whether arrow cues might also trigger automatic orienting. Two arrow cues were presented for 75 msec to the left and right of a fixation asterisk. After an interval of either 25 or 225 msec, the letter O or X appeared. After both time intervals, mean response times were reliably faster when the arrows pointed toward, rather than away from, the location of the target letter. This occurred despite the fact that the participants were informed that the arrows did not predict where the target would appear. In Experiment 2, the same pattern of data was recorded when several adjustments had been made in an attempt to rule out alternative explanations for the cuing effects. Overall, the findings suggest that the eye gaze is not unique in automatically triggering orienting.     

Are eyes special? It depends on how you look at it

Recent behavioral data have shown that central nonpredictive gaze direction triggers reflexive shifts of attention toward the gazed-at location (e.g., Friesen & Kingstone, 1998). Friesen and Kingstone suggested that this reflexive orienting effect is unique to biologically relevant stimuli. Three experiments were conducted to test this proposal by comparing the attentional orienting produced by nonpredictive gaze cues (biologically relevant) with the attentional orienting produced by nonpredictive arrow cues (biologically irrelevant). Both types of cues produced reflexive orienting in adults (Experiment 1) and preschoolers (Experiment 2), suggesting that gaze cues are not special. However, Experiment 3 showed that nonpredictive arrows produced reflexive orienting in both hemispheres of a split-brain patient. This contrasts with Kingstone, Friesen, and Gazzaniga's (2000) finding that nonpredictive gaze cues produce reflexive orienting only in the face-processing hemisphere of split-brain patients. Therefore, although nonpredictive eyes and arrows may produce similar behavioral effects, they are not subserved by the same brain systems. Together, these data provide important insight into the nature of the representations of directional stimuli involved in reflexive attentional orienting.     

Gaze and arrow distractors influence saccade trajectories similarly

Perceiving someone's averted eye-gaze is thought to result in an automatic shift of attention and in the preparation of an oculomotor response in the direction of perceived gaze. Although gaze cues have been regarded as being special in this respect, recent studies have found evidence for automatic attention shifts with nonsocial stimuli, such as arrow cues. Here, we directly compared the effects of social and nonsocial cues on eye movement preparation by examining the modulation of saccade trajectories made in the presence of eye-gaze, arrows, or peripheral distractors. At a short stimulus onset asynchrony (SOA) between the distractor and the target, saccades deviated towards the direction of centrally presented arrow distractors, but away from the peripheral distractors. No significant trajectory deviations were found for gaze distractors. At the longer SOA, saccades deviated away from the direction of the distractor for all three distractor types, but deviations were smaller for the centrally presented gaze and arrow distractors. These effects were independent of whether line-drawings or photos of faces were used and could not be explained by differences in the spatial properties of the peripheral distractor. The results suggest that all three types of distractors (gaze, arrow, peripheral) can induce the automatic programming of an eye movement. Moreover, the findings suggest that gaze and arrow distractors affect oculomotor preparation similarly, whereas peripheral distractors, which are classically regarded as eliciting an automatic shift of attention and an oculomotor response, induce a stronger and faster acting influence on response preparation and the corresponding inhibition of that response.     

What gaze adds to arrows: Changes in attentional response to gaze versus arrows in childhood and adolescence

From early ages, gaze acts as a cue to infer the interests, behaviours, thoughts and emotions of social partners. Despite sharing attentional properties with other non-social directional stimuli, such as arrows, gaze produces unique effects. A spatial interference task revealed this dissociation. The direction of arrows was identified faster on congruent than on incongruent direction-location trials. Conversely, gaze produced a reversed congruency effect (RCE), with faster identifications on incongruent than congruent trials. To determine the emergence of these gaze-specific attentional mechanisms, 214 Spanish children (4–17 years) divided into 6 age groups, performed the aforementioned task across three experiments. Results showed stimulus-specific developmental trajectories. Whereas the standard effect of arrows was unaffected by age, gaze shifted from an arrow-like effect at age 4 to a gaze-specific RCE at age 12. The orienting mechanisms shared by gaze and arrows are already present in 4-year olds and, throughout childhood, gaze becomes a special social cue with additional attentional properties. Besides orienting attention to a direction, as arrows would do, gaze might orient attention towards a specific object that would be attentionally selected. Such additional components may not fully develop until adolescence. Understanding gaze-specific attentional mechanisms may be crucial for children with atypical socio-cognitive development.     

ERPs reveal similar effects of social gaze orienting and voluntary attention, and distinguish each from reflexive attention

Spatial attention can be reflexively captured by a physically salient stimulus, effortfully directed toward a relevant location, or involuntarily oriented in the direction of another person's gaze (i.e., social gaze orienting). Here, we used event-related potentials to compare the effects of these three types of orienting on multiple stages of subsequent target processing. Although gaze orienting has been associated more strongly with reflexive capture than with voluntary attention, the present data provide new evidence that the neural effects of social gaze orienting are markedly different from the effects of reflexive attentional capture by physically salient stimuli. Specifically, despite their similar behavioral effects, social gaze orienting and reflexive capture produce different effects on both early sensory processing (~120 ms; P1/N1 components) and later, higher-order processing (~300 ms; P3 component). In contrast, the effects of social gaze orienting were highly similar to those of voluntary orienting at these stages of target processing.     

Is “Inhibition of Return” due to the inhibition of the return of attention?

Inhibition of Return (IOR) is usually explained in terms of orienting–reorienting of attention, emphasizing an underlying mechanism that inhibits the return of attention to previously selected locations. Recent data challenge this explanation to the extent that the IOR effect is observed at the location where attention is oriented to, where no reorienting of attention is needed. To date, these studies have involved endogenous attentional selection of attention and thus indicate a dissociation between the voluntary attention of spatial attention and the IOR effect. The present work demonstrates a dissociation between the involuntary orienting of spatial attention and the IOR effect. We combined nonpredictive peripheral cues with nonpredictive central orienting cues (either arrows or gaze). The IOR effect was observed to operate independent of involuntary spatial orienting. These data speak against the “reorienting hypothesis” of IOR. We suggest an alternative explanation whereby the IOR effect reflects a cost in detecting a new event (the target) at the location where another event (a cue) was coded before.     

Spatial orienting of tactile attention induced by social cues

Several studies have established that humans orient their visual attention reflexively in response to social cues such as the direction of someone else’s gaze. However, the consequences of this kind of orienting have been addressed only for the visual system. We investigated whether visual social attention cues can induce shifts in tactile attention by combining a central noninformative eye-gaze cue with tactile targets presented to participants’ fingertips. Data from speeded detection, speeded discrimination, and signal detection tasks converged on the same conclusion: Eye-gaze-based orienting facilitates the processing of tactile targets at the location of the gazed-at body location. In addition, we examined the effects of other directional cues, such as conventional arrows, and found that they can be equally effective. This is the first demonstration that social attention cues have consequences that reach beyond their own sensory modality.     

The effect of novel distractors on performance in focused attention tasks: A cognitive-psychophysiological approach

In the present study, we examined whether or not novel stimuli affect performance in a focused attention task. Participants responded to a central target while an irrelevant distractor in the visual display was occasionally changed. In Experiment 1, both target and distractor were presented centrally within the focus of attention. In Experiment 2, a central target was presented along with an irrelevant distractor at a peripheral location, outside the focus of attention. Novel distractors were associated with longer latencies and enhanced orienting responses (as measured by skin conductance responses) only when presented at an attended location. In contrast, as is demonstrated in Experiment 3, the same peripheral novel distractors interfered with task performance when they possessed task-relevant information. These results indicate that there is a fundamental difference between novel stimuli and task-relevant stimuli. Whereas the former exert influence only within the focus of attention, the latter affect performance even when positioned in an unattended location. Our findings have important implications for the operation of visual attention.     

Look Here! The Development of Attentional Orienting to Symbolic Cues

Although much research has examined the development of orienting to social directional cues (e.g., eye gaze), little is known about the development of orienting to nonsocial directional cues, such as arrows. Arrow cues have been used in numerous studies as a means to study attentional orienting, but the development of children's understanding of such cues has not previously been examined. It remains unclear to what extent the social nature of a cue is important for directing attention; further, it is unknown whether symbolic understanding is necessary for young children to be cued by symbols such as arrows. The present investigation explored when and how arrows cue children's attention. Our results suggest that children younger than 5 years of age orient their attention using the perceptual properties of arrows, and it is not until sometime after 5 years of age that children use the conceptual meaning of arrows to orient their attention. Understanding of the directional meaning of arrows may develop through both exogenous and endogenous orienting; we discuss possible contributions of the compression-based and selection-based learning systems.     

Abrupt onsets and gaze direction cues trigger independent reflexive attentional effects

The present study investigated whether the direction of visual signals is influenced independently by two automatic visual orienting phenomena: orienting to a gazed-at location and inhibition of return (IOR) to the location of an abrupt onset. A schematic face served as both a nonpredictive gaze direction cue and an abrupt onset cue. Results indicated that target detection was facilitated at the gazed-at location, and that it was inhibited at the abrupt onset location. Importantly, these two different reflexive attention effects were triggered by the same event and exhibited overlapping time courses. Moreover, the IOR effect did not vary as a function of the facilitatory effect of gaze. These findings strongly suggest that reflexive attention to gaze direction and reflexive inhibition to an abrupt onset are independent processes, and that gaze direction does not produce IOR at the gazed-at location.     

Attentional effects of counterpredictive gaze and arrow cues

The authors used counterpredictive cues to examine reflexive and volitional orienting to eyes and arrows. Experiment 1 investigated the effects of eyes with a novel design that allowed for a comparison of gazed-at (cued) target locations and likely (predicted) target locations against baseline locations that were not cued and not predicted. Attention shifted reflexively to the cued location and volitionally to the predicted location, and these 2 forms of orienting overlapped in time. Experiment 2 discovered that another well-learned directional stimulus, an arrow, produced a different effect: Attention was shifted only volitionally to the predicted location. The authors suggest that because there is a neural architecture specialized for processing eyes, gaze-triggered attention is more strongly reflexive than orienting to arrows.     

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.     

Investigating hemispheric lateralization of reflexive attention to gaze and arrow cues

Recent studies have demonstrated that central cues, such as eyes and arrows, reflexively trigger attentional shifts. However, it is not clear whether the attentional mechanisms induced by these two cues are similar or rather differ in some important way. We investigated hemispheric lateralization of the orienting effects induced by the two cue types in a group of 48 healthy participants comparing arrows and eye gaze as central non-predictive cues in a discrimination task, in which a target stimulus was briefly presented in one of two peripheral positions (left or right of fixation). As predicted by neuropsychological data, reflexive orienting to gaze cues was only observed when the target was presented in the left visual field, whereas reflexive orienting to arrow cues occurred for targets presented in both left and right visual fields.     

The effects of unilateral pulvinar damage in humans on reflexive orienting and filtering of irrelevant information

The effects of damage to the pulvinar nucleus of the thalamus in humans on reflexive orienting and selective attention were investigated. In a spatial orienting task three patients with unilateral pulvinar damage determined the location of a visual target that followed a cue that was not informative as to the targets location. Contralesional targets were responded to more slowly than ipsilesional targets. Also, at long cue target intervals patients responses to contralesional targets that appeared at previously cued locations were slower than to non-cued locations indicating that pulvinar damage does not affect inhibition of return. In the selective attention task two of the patients identified a target that appeared at one level of a global-local hierarchical stimulus while ignoring a distractor present at the other level. The distractor indicated either the same response as the target or a different response. Response times to targets in both visual fields were similar as were interference effects from the ignored distractors. These data indicate that engaging attention contralesionally is not impaired in discrimination tasks and that filtering of irrelevant information was not impaired contralesionally.     

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.