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.     

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.     

A biased-competition approach to spatial cueing: Combining empirical studies and computational modelling

We examined the effects of cue luminance on visual orienting. Experiment 1 established that the commonly-found early facilitation and late inhibition of return (IOR) effects were independent of cue luminance with single cues in terms of their amplitude, although IOR was delayed in the low compared to the high luminance cue condition. In contrast, Experiment 2 revealed that, with dual cues of mixed luminance, both facilitation and IOR effects were found only with bright cues. When cues had equal luminance, however, there were cueing effects for two cued locations but only when the cues were bright. The data were accommodated in a neural network model of biased competition in which cueing effects emerge at more than one location provided input activation is sufficient to overcome competitive damping of the selection system.     

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.     

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.     

返回抑制时程的三因素理论及其发展

综述了返回抑制(Inhibition of return,IOR)出现时程机制的三因素理论内容,支持该理论的实验证据,以及对理论的质疑和发展。该理论认为空间定向收益、出现检测缺失和空间选择收益三个因素共同决定了IOR出现的时程及机制。研究者通过操控任务加工水平或将实验范式相结合的方式对三因素理论提出了质疑和发展。许多关键问题如三个因素存在的认知神经科学证据、出现检测缺失和空间选择收益发挥作用的方式等是未来研究的重点和方向。     

The role of the oculomotor system in covert social attention

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

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

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

Spatiotemporal distribution of facilitation and inhibition of return arising from the reflexive orienting of covert attention

Currently, there is debate regarding both the spatial and temporal relationship between facilitation and inhibition of return (IOR) components of attention, as observed on the covert orienting of visual attention task (COVAT). These issues were addressed in a series of experiments where the spatial and temporal relationships between cue and target were manipulated. Facilitation occurred only when the stimulus onset asynchrony (SOA) was short and there was temporal overlap between cue and target. IOR occurred only when SOA was long and there was no temporal overlap between cue and target. Facilitation encompassed the cued location and all locations between the cue and fixation, whereas IOR arose for the entire cued hemifield. These findings suggest that the facilitation and IOR found on COVATs that use noninformative peripheral cues are separable and stimulus-driven processes.     

Inhibition of return in subliminal letter priming

The present study combined exogenous spatial cueing with masked repetition priming to study attentional influences on the processing of subliminal stimuli. Participants performed an alphabetic decision task (letter versus pseudo-letter classification) with central targets and briefly presented peripherally located primes that were either cued or not cued by an abrupt onset. A relatively long delay between cue and prime was used to investigate the effect of inhibition of return (IOR) on the processing of subliminal masked primes. Primes presented to the left visual field showed standard effects of Cue Validity and no IOR (significant priming with valid cues only). Primes presented to the right visual field showed no priming from valid cues (an IOR effect), and priming with invalid cues that depended on hand of response to letter targets (right-hand in Experiment 1, left-hand in Experiment 2). The results are interpreted in terms of a differential speed of engagement and disengagement of attention to the right and left visual fields for alphabetic stimuli, coupled with a complex interaction that arises between Prime Relatedness and response-hand.     

Inhibition of return exaggerates change blindness

Peripheral cues trigger attention shifts, which facilitate perceptual processing and enhance visual awareness. However, this facilitation is superseded by an inhibition of return (IOR) effect, which biases attention away from the cued location. While the link between facilitatory effects of visual attention and awareness is well established, no study has reported negative effects of spatial cueing on visual awareness. This failure is puzzling, given the claim that attention is a necessary precondition for awareness. If attention is necessary for awareness, inhibiting attention should also inhibit awareness. This leads to a slightly counterintuitive prediction: Spatial cueing will inhibit awareness at long cue–target latencies. This study shows that subliminal peripheral cues exaggerate change blindness at long cue–change latencies, demonstrating that IOR can suppress visual awareness of changes and suggesting that IOR can directly affect the contents of consciousness.     

Inhibition of return and object-based attentional selection

Visual attention research has revealed that attentional allocation can occur in space- and/or object-based coordinates. Using the direct and elegant design of R. Egly, J. Driver, and R. Rafal (1994), the present experiments tested whether space- and object-based inhibition of return (IOR) emerge under similar time courses. The experiments were capable of isolating both space- and object-based effects induced by peripheral and back-to-center cues. The results generally support the contention that spatially nonpredictive cues are effective in producing space-based IOR at a variety of stimulus onset asynchronies (SOAs) and under a variety of stimulus conditions. Whether facilitatory or inhibitory in direction, the object-based effects occurred over a very different time course than did the space-based effects. Reliable object-based IOR was only found under limited conditions and was tied to the time since the most recent cue (peripheral or central). The finding that object-based effects are generally determined by SOA from the most recent cue may help to resolve discrepancies in the IOR literature. These findings also have implications for the search facilitator role that IOR is purported to play in the guidance of visual attention.     

The effects of onsets and offsets on visual attention

 Two experiments are presented which examine the effect of onset and offset cues on early occurring attentional cueing effects and later occurring inhibition of return (IOR). The first experiment compared the effects of single onset cues, single offset cues, and simultaneous onset and offset cues (at opposite locations) at a 100-ms stimulus-onset-asynchrony (SOA) and IOR at a 900-ms SOA. Whereas the first experiment examined these conditions with choice localization keypress responses, the second experiment used simple detection keypress responses. Both experiments found that onset and offset cues presented in isolation produce early facilitation and late IOR. When onset and offset cues were simultaneously presented, facilitation but not IOR was found with localization responses, while neither facilitation or IOR was found with detection responses. Overall, these findings suggest that offset cues can be treated in the same manner as onset cues by the attentional system, although the onset cues may have priority in orienting attention when targets must be localized in space. Received: 26 May 2000 / Accepted: 31 January 2001     

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.     

内源性注意与外源性注意的跨通道比较

该研究利用空间线索技术的实验模式,考察跨视觉和听觉通道的内源性选择注意与外源性选择性注意的相互关系。实验结果表明：(1)听觉中央线索在较长的SOA(至少500毫秒)条件下,可以引导内源性空间选择性注意;同时外周线索突现也能自动化地吸引部分注意资源。(2)听觉和视觉选择注意是分离的加工通道,但二者之间存在相互联系。     

Unconscious attentional orienting to exogenous cues: A review of the literature

The present paper reviews research that focuses on the dissociation between bottom-up attention and consciousness. In particular, we focus on studies investigating spatial exogenous orienting in the absence of awareness. We discuss studies that use peripheral masked onset cues and studies that use gaze cueing. The results from these studies show that the classic biphasic pattern of facilitation and inhibition, which is characteristic of conscious exogenous cueing can also be obtained with subliminal spatial cues. It is hypothesized that unconscious attentional orienting is mediated by the subcortical retinotectal pathway. Moreover, a possible neural network including superior colliculus, pulvinar and amygdala is suggested as the underlying mechanism.     

Measuring effects of voluntary attention: A comparison among predictive arrow,colour, and number cues

The Posner cueing paradigm is one of the most widely used paradigms in attention research. Importantly, when employing it, it is critical to understand which type of orienting a cue triggers. It has been suggested that large effects elicited by predictive arrow cues reflect an interaction of involuntary and voluntary orienting. This conclusion is based on comparisons of cueing effects of predictive arrows, nonpredictive arrows (involuntary orienting), and predictive numbers (voluntary orienting). Experiment 1 investigated whether this conclusion is restricted to comparisons with number cues and showed similar results to those of previous studies, but now for comparisons to predictive colour cues, indicating that the earlier conclusion can be generalized. Experiment 2 assessed whether the size of a cueing effect is related to the ease of deriving direction information from a cue, based on the rationale that effects for arrows may be larger, because it may be easier to process direction information given by symbols such as arrows than that given by other cues. Indeed, direction information is derived faster and more accurately from arrows than from colour and number cues in a direction judgement task, and cueing effects are larger for arrows than for the other cues. Importantly though, performance in the two tasks is not correlated. Hence, the large cueing effects of arrows are not a result of the ease of information processing, but of the types of orienting that the arrows elicit.     

Sex differences in eye gaze and symbolic cueing of attention.

Observing a face with averted eyes results in a reflexive shift of attention to the gazed-at location. Here we present results that show that this effect is weaker in males than in females (Experiment 1). This result is predicted by the 'extreme male brain' theory of autism (Baron-Cohen, 2003), which suggests that males in the normal population should display more autism-like traits than females (e.g., poor joint attention). Indeed, participants' scores on the Autism-Spectrum Quotient (Baron-Cohen, Wheelwright, Stott, Bolton, & Goodyear, 2001) negatively correlated with cueing magnitude. Furthermore, exogenous orienting did not differ between the sexes in two peripheral cueing experiments (Experiments 2a and 2b). However, a final experiment showed that using nonpredictive arrows instead of eyes as a central cue also revealed a large gender difference. This demonstrates that reduced orienting from central cues in males generalizes beyond gaze cues. These results show that while peripheral cueing is equivalent in the male and female brains, the attention systems of the two sexes treat noninformative symbolic cues very differently.     

The effect of reward on orienting and reorienting in exogenous cuing

It is thought that reward-induced motivation influences perceptual, attentional, and cognitive control processes to facilitate behavioral performance. In this study, we investigated the effect of reward-induced motivation on exogenous attention orienting and inhibition of return (IOR). Attention was captured by peripheral onset cues that were nonpredictive for the target location. Participants performed a target discrimination task at short (170 ms) and long (960 ms) cue–target stimulus onset asynchronies. Reward-induced motivation was manipulated by exposing participants to low- and high-reward blocks. Typical cue facilitation effects on initial orienting were observed for both the low- and high-reward conditions. However, IOR was found only for the high-reward condition. This indicates that reward-induced motivation has a clear effect on reorienting and inhibitory processes following the initial capture of attention, but not on initial exogenous orienting that is considered to be exclusively automatic and stimulus-driven. We suggest that initial orienting is completely data-driven, not affected by top-down motivational processes, while reorienting and the accompanying IOR effect involve motivational top-down processes. To support this, we showed that reward-induced motivational processes and top-down control processes co-act in order to improve behavioral performance: High-reward-induced motivation caused an increase in top-down cognitive control, as signified by posterror slowing. Moreover, we show that personality trait propensity to reward-driven behavior (BAS-Drive scale) was related to reward-triggered behavioral changes in top-down reorienting, but not to changes in automatic orienting.     

Examining the time course of facilitation and inhibition with simultaneous onset and offset cues

The experiment conducted examined the effect of simultaneously presented onset and offset cues on the orienting of attention in the visual field. Subjects were presented with a display that consisted of four placeholder boxes around a central fixation point. An onset and an offset cue appeared simultaneously in two of the locations, and the other two locations provided a neutral baseline condition. Reaction times were measured in a simple target detection task with stimulus-onset asynchronies (SOAs) that ranged from 100 ms to 1,000 ms. As expected, the onset cue produced early facilitation and later occurring inhibition of return (IOR). The offset cue produced significant inhibition at all but the earliest SOA. These results suggest that simultaneously presented onset and offset cues both capture attention, but that attention is rapidly disengaged from the location of the offset cue, resulting in earlier occurring IOR. For the onset cues, attention is allocated for a longer period of time, producing the typical pattern of early facilitation and later occurring IOR. The differing time course of attention at each location may reflect separate facilitatory and inhibitory processes, and the priority given to the onset of a stimulus by the attentional system.