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.     

The influence of eye-gaze and arrow pointing distractor cues on voluntary eye movements

We investigated Ricciardelli et al.'s (2002) claim, that the tendency for gaze direction to elicit automatic attentional following is unique to biologically significant information. Participants made voluntary saccades to targets on the left or the right of a display, which were either congruent or incongruent with a centrally presented distractor (eye-gaze or arrow). Contrary to Ricciardelli et al., for both distractor types, saccade latencies were slower, and participants made more directional errors, on incongruent than on congruent trials. Moreover, a cost-benefit analysis showed no difference between the two distractor types. However, latencies for erroneous saccades were faster than correctly directed saccades for the eye-gaze distractors, but not for the arrow distractors.     

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.     

Emotional attention: effects of emotion and gaze direction on overt orienting of visual attention

In the present study we considered the two factors that have been advocated for playing a role in emotional attention: perception of gaze direction and facial expression of emotions. Participants performed an oculomotor task in which they had to make a saccade towards one of the two lateral targets, depending on the colour of the fixation dot which appeared at the centre of the computer screen. At different time intervals (stimulus onset asynchronies, SOAs: 50,100,150 ms) following the onset of the dot, a picture of a human face (gazing either to the right or to the left) was presented at the centre of the screen. The gaze direction of the face could be congruent or incongruent with respect to the location of the target, and the expression could be neutral or angry. In Experiment 1 the facial expressions were presented randomly in a single block, whereas in Experiment 2 they were shown in separate blocks. Latencies for correct saccades and percentage of errors (saccade direction errors) were considered in the analyses. Results showed that incongruent trials determined a significantly higher percentage of saccade direction errors with respect to congruent trials, thus confirming that gaze direction, even when task-irrelevant, interferes with the accuracy of the observer’s oculomotor behaviour. The angry expression was found to hold attention for a longer time with respect to the neutral one, producing delayed saccade latencies. This was particularly evident at 100 ms SOA and for incongruent trials. Emotional faces may then exert a modulatory effect on overt attention mechanisms.     

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 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.     

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 and gaze shifting in dual-task and go/no-go performance with vocal responding

Evidence from go/no-go performance on the Eriksen flanker task with manual responding suggests that individuals gaze at stimuli just as long as needed to identify them (e.g., Sanders, 1998). In contrast, evidence from dual-task performance with vocal responding suggests that gaze shifts occur after response selection (e.g., Roelofs, 2008a). This difference in results may be due to the nature of the task situation (go/no-go vs. dual task) or the response modality (manual vs. vocal). We examined this by having participants vocally respond to congruent and incongruent flanker stimuli and shift gaze to left- or right-pointing arrows. The arrows required a manual response (dual task) or determined whether the vocal response to the flanker stimuli had to be given or not (go/no-go). Vocal response and gaze shift latencies were longer on incongruent than congruent trials in both dual-task and go/no-go performance. The flanker effect was also present in the manual response latencies in dual-task performance. Ex-Gaussian analyses revealed that the flanker effect on the gaze shifts consisted of a shift of the entire latency distribution. These results suggest that gaze shifts occur after response selection in both dual-task and go/no-go performance with vocal responding.     

What Stroop tasks can tell us about selective attention from childhood to adulthood

A rich body of research concerns causes of Stroop effects plus applications of Stroop. However, several questions remain. We included assessment of errors with children and adults (N = 316), who sat either a task wherein each block employed only trials of one type (unmixed task) or where every block comprised of a mix of the congruent, neutral, and incongruent trials. Children responded slower than adults and made more errors on each task. Contrary to some previous studies, interference (the difference between neutral and incongruent condition) showed no reaction time (RT) differences by group or task, although there were differences in errors. By contrast, facilitation (the difference between neutral and congruent condition) was greater in children than adults, and greater on the unmixed task than the mixed task. After considering a number of theoretical accounts, we settle on the inadvertent word‐reading hypothesis, whereby facilitation stems from children and the unmixed task promoting inadvertent reading particularly in the congruent condition. Stability of interference RT is explained by fixed semantic differences between neutral and incongruent conditions, for children versus adults and for unmixed versus mixed task. We conclude that utilizing two tasks together may reveal more about how attention is affected in other groups.     

The role of prefrontal cortex in resolving distractor interference

We investigate the hypothesis that those subregions of the prefrontal cortex (PFC) found to support proactive interference resolution may also support delay-spanning distractor interference resolution. Ten subjects performed delayed-recognition tasks requiring working memory for faces or shoes during functional MRI scanning. During the 15-sec delay interval, task-irrelevant distractors were presented. These distractors were either all faces or all shoes and were thus either congruent or incongruent with the domain of items in the working memory task. Delayed-recognition performance was slower and less accurate during congruent than during incongruent trials. Our fMRI analyses revealed significant delay interval activity for face and shoe working memory tasks within both dorsal and ventral PFC. However, only ventral PFC activity was modulated by distractor category, with greater activity for congruent than for incongruent trials. Importantly, this congruency effect was only present for correct trials. In addition to PFC, activity within the fusiform face area was investigated. During face distraction, activity was greater for face relative to shoe working memory. As in ventrolateral PFC, this congruency effect was only present for correct trials. These results suggest that the ventrolateral PFC and fusiform face area may work together to support delay-spanning interference resolution.     

Giving subjects the eye and showing them the finger: socio-biological cues and saccade generation in the anti-saccade task

Pointing with the eyes or the finger occurs frequently in social interaction to indicate direction of attention and one's intentions. Research with a voluntary saccade task (where saccade direction is instructed by the colour of a fixation point) suggested that gaze cues automatically activate the oculomotor system, but non-biological cues, like arrows, do not. However, other work has failed to support the claim that gaze cues are special. In the current research we introduced biological and non-biological cues into the anti-saccade task, using a range of stimulus onset asynchronies (SOAs). The anti-saccade task recruits both top-down and bottom-up attentional mechanisms, as occurs in naturalistic saccadic behaviour. In experiment 1 gaze, but not arrows, facilitated saccadic reaction times (SRTs) in the opposite direction to the cues over all SOAs, whereas in experiment 2 directional word cues had no effect on saccades. In experiment 3 finger pointing cues caused reduced SRTs in the opposite direction to the cues at short SOAs. These findings suggest that biological cues automatically recruit the oculomotor system whereas non-biological cues do not. Furthermore, the anti-saccade task set appears to facilitate saccadic responses in the opposite direction to the cues.     

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.     

Bottom-up effects modulate saccadic latencies in well-known eye movement paradigm

A well-known eye movement paradigm combines saccades (fast eye movements) with a perceptual discrimination task. At a variable time after the onset of a central arrow cue indicating the target direction [the stimulus onset asynchrony (SOA)], discrimination symbols appear briefly at saccade target and non-target locations. A previous study revealed an unexpected effect of SOA on saccadic latencies: latencies were longer in trials with longer SOAs. It was suggested that this effect reflects a top-down process as observers may wait for the discrimination symbol to appear before executing saccades. However, symbol onsets may also modulate saccade latencies from the bottom-up. To clarify the origin of the SOA effect on latencies in this paradigm, we used a simplified version of the original task plus two new symbol onset conditions for comparison. The results indicate that the modulation of saccadic latencies was not due to a top-down strategy, but to a combination of two opposing bottom-up effects: the symbol onsets at the target location shortened saccade latencies, while symbol onsets at non-target locations lengthened saccade latencies.     

Facial expressions modulate the gaze orienting effect on sound localization judgement

Recent studies have shown that cueing eye gaze can affect the processing of visual information, and this phenomenon is called the gaze-orienting effect (visual-GOE). Emerging evidence has shown that the cueing eye gaze also affects the processing of auditory information (auditory-GOE). However, it is unclear whether the auditory-GOE is modulated by emotion. We conducted three behavioural experiments to investigate whether cueing eye gaze influenced the orientation judgement to a sound, and whether the effect was modulated by facial expressions. The current study set four facial expressions (angry, fearful, happy, and neutral), manipulated the display type of facial expressions, and changed the sequence of gaze and emotional expressions. Participants were required to judge the sound orientation after facial expressions and gaze cues. The results showed that the orientation judgement of sound was influenced by gaze direction in all three experiments, and the orientation judgement of sound was faster when the face was oriented to the target location (congruent trials) than when the face was oriented away from the target location (incongruent trials). The modulation of emotion on auditory-GOE was observed only when gaze shifted followed by facial expression (Exp3); the auditory-GOE was significantly greater for angry faces than for neutral faces. These findings indicate that auditory-GOE as a social phenomenon exists widely, and the effect was modulated by facial expression. Gaze shift before the presentation of emotion was the key influencing factor for the emotional modulation in an auditory target gaze-orienting task. Our findings suggest that the integration of facial expressions and eye gaze was context-dependent.     

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 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.     

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。     

Conflict-induced perceptual filtering

In a variety of conflict paradigms, target and distractor stimuli are defined in terms of perceptual features. Interference evoked by distractor stimuli tends to be reduced when the ratio of congruent to incongruent trials is decreased, suggesting conflict-induced perceptual filtering (i.e., adjusting the processing weights assigned to stimuli associated with the target and with the distractor features). In search of evidence for such a mechanism, we administered a flanker task, in which targets and distractors were defined in terms of stimulus location (Experiment 1) or color (Experiment 2). The efficiency of processing stimuli associated with target and distractor features was assessed in intermixed trials of a visual search task, in which a target had to be detected irrespective of these features. In both experiments search times were shorter for stimuli associated with the target feature than with the distractor feature of the flanker task. This effect was increased under conditions of a reduced congruent/incongruent ratio, thereby providing evidence for conflict-dependent perceptual filtering.     

线索类型对阈下注视线索效应的影响

实验结合连续闪烁抑制范式和线索化范式, 通过操纵直视面孔和斜视面孔的呈现方式, 考察了动静线索类型对注视线索效应的影响。结果表明：两种线索在阈上条件都能产生注视线索效应, 且动态线索诱发的效应更大; 无意识条件下有且仅有动态注视线索能诱发注视线索效应。这说明眼睛运动是产生阈下注视线索效应的必要条件; 眼睛运动会增强阈上注视线索效应, 静态注视线索效应依赖于意识。研究结果支持了社会知觉与心理理论交互模型。     

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.