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.     

Developmental changes in the control of saccadic eye movements in response to directional eye gaze and arrows

We investigated developmental differences in oculomotor control between 10-year-old children and adults using a central interference task. In this task, the colour of a fixation point instructed participants to saccade either to the left or to the right. These saccade directions were either congruent or incongruent with two types of distractor cue: either the direction of eye gaze of a centrally presented schematic face, or the direction of arrows. Children had greater difficulties inhibiting the distractor cues than did adults, which revealed itself in longer saccade latencies for saccades that were incongruent with the distractor cues as well as more errors on these incongruent trials than on congruent trials. Counter to our prediction, in terms of saccade latencies, both children and adults had greater difficulties inhibiting the arrow than the eye gaze distractors.     

Developmental changes in the control of saccadic eye movements in response to directional eye gaze and arrows

We investigated developmental differences in oculomotor control between 10-year-old children and adults using a central interference task. In this task, the colour of a fixation point instructed participants to saccade either to the left or to the right. These saccade directions were either congruent or incongruent with two types of distractor cue: either the direction of eye gaze of a centrally presented schematic face, or the direction of arrows. Children had greater difficulties inhibiting the distractor cues than did adults, which revealed itself in longer saccade latencies for saccades that were incongruent with the distractor cues as well as more errors on these incongruent trials than on congruent trials. Counter to our prediction, in terms of saccade latencies, both children and adults had greater difficulties inhibiting the arrow than the eye gaze distractors.     

Eye gaze cannot be ignored (but neither can arrows)

Recent studies have tried to shed light on the automaticity of attentional shifts triggered by gaze and arrows with mixed results. In the present research, we aimed at testing a strong definition of resistance to suppression for orienting of attention elicited by these two cues. In five experiments, participants were informed with 100% certainty about the future location of a target they had to react to by presentation of either a direction word at the beginning of each trial or instructions at the beginning of each block. Gaze and arrows were presented before the target as uninformative distractors irrelevant for the task. The results showed similar patterns for gaze and arrows-namely, an interference effect when the distractors were incongruent with the upcoming target location. This suggests that the orienting of attention mediated by gaze and arrows can be considered as strongly automatic.     

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.     

Controlling attention to gaze and arrows in childhood: an fMRI study of typical development and Autism Spectrum Disorders

Functional magnetic resonance imaging was used to examine functional anatomy of attention to social (eye gaze) and nonsocial (arrow) communicative stimuli in late childhood and in a disorder defined by atypical processing of social stimuli, Autism Spectrum Disorders (ASD). Children responded to a target word ('LEFT'/'RIGHT') in the context of a distracting arrow or averted gaze pointing in a direction that was congruent, incongruent, or neutral (bar without arrowheads, central gaze) relative to the target word. Despite being irrelevant to the target task, both arrow and averted gaze facilitated responses (Congruent vs. Neutral trials) to the same extent in the two groups and led to interference (Incongruent vs. Congruent trials), which was greater from arrows in ASD than control children. In the brain, interaction between group and distracter-domain was observed in frontal-temporal regions during facilitation and frontal-striatal regions during interference. During facilitation, regions associated with attention to gaze in control children (left superior temporal sulcus, premotor) were associated with attention to arrows in ASD children; gaze was associated with medial temporal involvement in ASD children. During interference, regions associated with arrows in control children (anterior cingulate, right caudate) were activated in response to gaze in ASD children; further, left dorsolateral prefrontal cortex, a region not observed in control children, was activated during gaze-interference in ASD children. Thus, functional anatomy was atypical in ASD children during spontaneous processing of social and nonsocial communicative cues.     

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.     

Attentional control and reflexive orienting to gaze and arrow cues

A wealth of data indicate that central spatially nonpredictive eyes and arrows trigger very similar reflexive spatial orienting, although the effects of eyes may be more strongly reflexive (e.g., Friesen, Ristic, & Kingstone, 2004). Pratt and Hommel (2003) recently reported that the orienting effect for arrows is sensitive to arbitrary cue-target color contingencies; for example, an attentional orienting effect for blue colored arrows is evident only for blue targets. We reasoned that if the orienting effect elicited by eye direction is more strongly reflexive than the orienting effect elicited by arrow direction, it follows that eyes, unlike arrows, may trigger orienting effects that generalize across congruent and incongruent cue-target color contingencies. Replicating Pratt and Hommel (2003), we found that the reflexive attention effect elicited by arrows is specific to color-congruent target stimuli. The attention effect triggered by eyes, however, generalizes across color-congruent and color-incongruent target stimuli. These data support the hypothesis that eye direction and arrow direction trigger similar reflexive shifts in spatial attention, but that the attention effect triggered by eye direction is more strongly reflexive.     

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.     

Arrows don’t look at you: Qualitatively different attentional mechanisms triggered by gaze and arrows

Eye gaze conveys rich information concerning the states of mind of others, playing a critical role in social interactions, signaling internal states, and guiding others’ attention. On the basis of its social significance, some researchers have proposed that eye gaze may represent a unique attentional stimulus. However, contrary to this notion, the majority of the literature has shown indistinguishable attentional effects when eye gaze and arrows have been used as cues. Taking a different approach, in this study we aimed at finding qualitative attentional differences between gazes and arrows when they were used as targets instead of as cues. We used a spatial Stroop task, in which participants were required to identify the direction of eyes or arrows presented to the left or the right of a fixation point. The results showed that the two types of stimuli led to opposite spatial interference effects, with arrows producing faster reaction times when the stimulus direction was congruent with the stimulus position (a typical spatial Stroop effect), and eye gaze producing faster reaction times when it was incongruent (a “reversed” spatial Stroop effect). This reversed Stroop is interpreted as an eye-contact effect, therefore revealing the unique nature of eyes as special social-attention stimuli.     

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.     

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.     

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.     

Covert orienting of attention in 3-month-old infants: The case of biological motion

Humans attend to different positions in the space either by moving their eyes or by moving covertly their attention. The development of covert attention occurs during the first year of life. According to Colombo’s model of attention (2001), within the first years there is a significant change in infants’ visuo-spatial orienting mechanisms, from a predominantly overt form to a covert orienting starting from 4 to 5 months of life. The use of non-invasive brain imaging techniques can shed light on the origin of such mechanisms. In particular, EEG and ERP studies can directly investigate the neural correlates of covert attention in young infants. The present study investigated the neural correlates of covert attention employing a visuo-spatial cueing paradigm in 3-month-old infants. Infants were presented with a central point-light walker (PLD) followed by a single peripheral target. The target appeared randomly at a position either congruent or incongruent with the walking direction of the cue. We examined infants’ target-locked P1 component and the saccade latencies toward the peripheral target. Results showed that the P1 component was larger in response to congruent than to incongruent targets and saccade latencies were faster for congruent rather than incongruent trials. Moreover, the facilitation in processing sensory information (priming effects) presented at the cued spatial location occurs even before the onset of the oculomotor response, suggesting that covert attention is present before 4 months of age. Overall, this study highlights how ERPs method could help researchers at investigating the neural basis of attentional mechanisms in infants.     

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.     

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.     

The neural correlates of orienting to walking direction in 6‐month‐old infants: An ERP study

The ability to detect social signals represents a first step to enter our social world. Behavioral evidence has demonstrated that 6‐month‐old infants are able to orient their attention toward the position indicated by walking direction, showing faster orienting responses toward stimuli cued by the direction of motion than toward uncued stimuli. The present study investigated the neural mechanisms underpinning this attentional priming effect by using a spatial cueing paradigm and recording EEG (Geodesic System 128 channels) from 6‐month‐old infants. Infants were presented with a central point‐light walker followed by a single peripheral target. The target appeared randomly at a position either congruent or incongruent with the walking direction of the cue. We examined infants' target‐locked event‐related potential (ERP) responses and we used cortical source analysis to explore which brain regions gave rise to the ERP responses. The P1 component and saccade latencies toward the peripheral target were modulated by the congruency between the walking direction of the cue and the position of the target. Infants' saccade latencies were faster in response to targets appearing at congruent spatial locations. The P1 component was larger in response to congruent than to incongruent targets and a similar congruency effect was found with cortical source analysis in the parahippocampal gyrus and the anterior fusiform gyrus. Overall, these findings suggest that a type of biological motion like the one of a vertebrate walking on the legs can trigger covert orienting of attention in 6‐month‐old infants, enabling enhancement of neural activity related to visual processing of potentially relevant information as well as a facilitation of oculomotor responses to stimuli appearing at the attended location.     

Age-related decline in the reflexive component of overt gaze following

Previous research has found age-related declines in social perception tasks as well as the ability to engage in joint attention and orienting covert attention (i.e., absence of eye movements) in response to an eye gaze cue. We used an overt gaze following task to explore age differences in overt gaze following whilst people searched for a target. Participants were faster to detect targets appearing at the looked-at location, and although the gaze cue biased the direction in which saccades were executed, no age differences were found in overt gaze following. There were, however, age effects relating to involuntary eye movements. In the younger adults, anticipatory saccades were biased in the direction of the gaze cue, but this bias was not observed in the older group. Moreover, in the younger adults, saccades that followed the gaze were initiated more rapidly, illustrating the reflexive nature of gaze following. No such difference was observed in the older adults. Importantly, our results showed that whilst the general levels of gaze following were age invariant, there were age-related differences in the reflexive components of overt gaze following.     

Look away! Eyes and arrows engage oculomotor responses automatically

The present study investigates how people’s voluntary saccades are influenced by where another person is looking, even when this is counterpredictive of the intended saccade direction. The color of a fixation point instructed participants to make saccades either to the left or right. These saccade directions were either congruent or incongruent with the eye gaze of a centrally presented schematic face. Participants were asked to ignore the eyes, which were congruent only 20% of the time. At short gaze—fixation-cue stimulus onset asynchronies (SOAs; 0 and 100 msec), participants made more directional errors on incongruent than on congruent trials. At a longer SOA (900 msec), the pattern tended to reverse. We demonstrate that a perceived eye gaze results in an automatic saccade following the gaze and that the gaze cue cannot be ignored, even when attending to it is detrimental to the task. Similar results were found for centrally presented arrow cues, suggesting that this interference is not unique to gazes.     

The mutual influence of gaze and head orientation in the analysis of social attention direction

Three experiments are reported that investigate the hypothesis that head orientation and gaze direction interact in the processing of another individual's direction of social attention. A Stroop-type interference paradigm was adopted, in which gaze and head cues were placed into conflict. In separate blocks of trials, participants were asked to make speeded keypress responses contingent on either the direction of gaze, or the orientation of the head displayed in a digitized photograph of a male face. In Experiments 1 and 2, head and gaze cues showed symmetrical interference effects. Compared with congruent arrangements, incongruent head cues slowed responses to gaze cues, and incongruent gaze cues slowed responses to head cues, suggesting that head and gaze are mutually influential in the analysis of social attention direction. This mutuality was also evident in a cross-modal version of the task (Experiment 3) where participants responded to spoken directional words whilst ignoring the head/gaze images. It is argued that these interference effects arise from the independent influences of gaze and head orientation on decisions concerning social attention direction.