Attention and ageing: Measuring effects of involuntary and voluntary orienting in isolation and in combination

The cueing paradigm provides an established method for eliciting involuntary and voluntary attention shifts. Involuntary orienting is traditionally measured with non‐predictive peripheral cues and voluntary orienting with predictive central arrows. Recent studies with young adults have established that predictive central arrows trigger a combination of involuntary and voluntary orienting, raising the possibility that previous studies – including those with older adults – misinterpreted their findings with central arrow cues as isolating the effects of voluntary attention. The present experiment applied different cueing conditions that measured involuntary orienting, voluntary orienting, and involuntary and voluntary orienting in combination in older adults. The results show that past studies of voluntary orienting in older adults confound involuntary and voluntary orienting. Cueing effects in a condition that for the first time isolated voluntary orienting (predictive number cues) with older adults were significant, and comparable to effects for younger adults, demonstrating that older adults successfully utilize cues to direct their spatial attention strategically. A similar normal pattern of orienting was observed for involuntary orienting. Our study provides a methodology that can be applied effectively to isolate and investigate the effects of age on voluntary and involuntary attention.     

Enhanced orienting effects: Evidence for an interaction principle

Predictive arrow cues, as used in the classic “Posner paradigm”, that were long thought to engage and isolate voluntary attention, may in fact trigger a strong interaction between voluntary and involuntary attention (Ristic & Kingstone, 2006). This interaction produces an orienting effect that exceeds both the effects of involuntary and voluntary attention alone, and the additive combination of involuntary and voluntary orienting. The present study shows that nonpredictive peripheral cues—understood to engage and isolate involuntary attention—if made predictive, result in enhanced orienting effects similar to predictive arrows. The important contribution of these data is that they suggest an “interaction principle”: If attention cues can elicit reliable involuntary orienting, then when they are made spatially predictive, the resulting attention effect will be greater than the sum of involuntary and voluntary orienting alone.     

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.     

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

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

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.     

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.     

Gaze and arrow cueing of attention reveals individual differences along the autism spectrum as a function of target context

Observing averted gaze results in a reflexive shift of attention to the gazed‐at location. In two experiments, participants scoring high and low on the Autism‐Spectrum Quotient questionnaire (AQ; Baron‐Cohen, Wheelwright, Skinner, Martin, & Clubley, 2001 ) observed arrow and gaze cues to investigate cueing effect magnitude as a function of the context in which peripheral targets could appear. While identical cueing effects were found with gaze and arrow cues, the more striking results concerned target stimuli. In Experiment 1, targets could appear on a peripheral face, or on scrambled face parts. Overall, greater cueing effects were found when the target appeared on a face. However, this face bias was only observed in participants with low AQ scores, whereas high AQ scorers oriented more to scrambled features. Experiment 2 found equal cueing to targets appearing on tools, as compared with tool parts. However, individual differences were again observed, where low AQ scorers showed larger cueing towards tools, while high scorers oriented more to scrambled parts, as in Experiment 1. These results support the idea that low AQ individuals orient strongly to objects attended by others. However, since the same results were found for arrow cues, this effect may generalize to all central cues to attention. High AQ scorers possessing many more autistic‐like traits tended to orient more to scrambled shapes, perhaps reflecting a bias for orienting to local details.     

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.     

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.     

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.     

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.     

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.     

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.     

The influence of social and symbolic cues on observers' gaze behaviour

Research has shown that social and symbolic cues presented in isolation and at fixation have strong effects on observers, but it is unclear how cues compare when they are presented away from fixation and embedded in natural scenes. We here compare the effects of two types of social cue (gaze and pointing gestures) and one type of symbolic cue (arrow signs) on eye movements of observers under two viewing conditions (free viewing vs. a memory task). The results suggest that social cues are looked at more quickly, for longer and more frequently than the symbolic arrow cues. An analysis of saccades initiated from the cue suggests that the pointing cue leads to stronger cueing than the gaze and the arrow cue. While the task had only a weak influence on gaze orienting to the cues, stronger cue following was found for free viewing compared to the memory task.     

Voluntary and involuntary attention vary as a function of impulsivity

In the present study we examined, first, whether voluntary and involuntary attention manifest differently in people who differ in impulsivity (measured with the Barratt Impulsivity Scale). For Experiment 1, we used the spatial cueing task with informative and noninformative spatial cues to probe voluntary and involuntary attention, respectively. We found that participants with high impulsivity scores exhibited larger involuntary attention effects, whereas participants with low impulsivity scores exhibited larger voluntary attention effects. For Experiment 2, we used the correlated-flanker task to determine whether the differences between groups in Experiment 1 were due to high-impulsive participants being less sensitive to the display contingencies or to high-impulsive participants having a greater spread of spatial attention. Surprisingly, high-impulsive participants showed a greater sensitivity to contingencies in the environment (correlated-flanker effect). Our results illustrate one situation in which involuntary attention associated with high impulsivity can play a useful role.     

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.     

Voluntary allocation versus automatic capture of visual attention

Is there a difference in the kind of attention elicited by an abrupt-onset peripheral cue and that elicited by an instruction (e.g., a central arrow cue) to move attention to a peripheral location? In Experiment 1, we found that peripheral cues are no more effective in orienting attention than are central cues. No evidence was found for separable attentional systems consisting of a volitional response to central cues and an automatic response triggered only by peripheral cues. Rather, an identical or similar attentional process seems to be activated by either type of cue, although perhaps in different ways. Peripheral cues seem to have an automatic component, however, in that once attention is engaged by a peripheral cue, it cannot easily be disengaged for refocus elsewhere. In Experiment 2, after several sessions of practice, subjects were able to circumvent automatic attentional capture by an abrupt-onset peripheral cue and to volitionally redirect the focus of attention. Thus, attentional capture by abrupt-onset stimuli is not strongly automatic.     

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.     

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.     

Investigating the role of exogenous cueing on selection history formation

An abundance of recent empirical data suggest that repeatedly allocating visual attention to task-relevant and/or reward-predicting features in the visual world engenders an attentional bias for these frequently attended stimuli, even when they become task irrelevant and no longer predict reward. In short, attentional selection in the past hinders voluntary control of attention in the present. But do such enduring attentional biases rely on a history of voluntary, goal-directed attentional selection, or can they be generated through involuntary, effortless attentional allocation? An abrupt visual onset triggers such a reflexive allocation of covert spatial attention to its location in the visual field, automatically modulating numerous aspects of visual perception. In this Registered Report, we asked whether a selection history that has been reflexively and involuntarily derived (i.e., through abrupt-onset cueing) also interferes with goal-directed attentional control, even in the complete absence of exogenous cues. To build spatially distinct histories of exogenous selection, we presented abrupt-onset cues twice as often at one of two task locations, and as expected, these cues reflexively modulated visual processing: task accuracy increased, and response times (RTs) decreased, when the cue appeared near the target’s location, relative to that of the distractor. Upon removal of these cues, however, we found no evidence that exogenous selection history modulated task performance: task accuracy and RTs at the previously most-cued and previously least-cued sides were statistically indistinguishable. Thus, unlike voluntarily directed attention, involuntary attentional allocation may not be sufficient to engender historically contingent selection biases.