Distractor Evoked Deviations of Saccade Trajectory Are Modulated by Fixation Activity in the Superior Colliculus: Computational and Behavioral Evidence

Previous studies have shown that saccades may deviate towards or away from task irrelevant visual distractors. This observation has been attributed to active suppression (inhibition) of the distractor location unfolding over time: early in time inhibition at the distractor location is incomplete causing deviation towards the distractor, while later in time when inhibition is complete the eyes deviate away from the distractor. In a recent computational study, Wang, Kruijne and Theeuwes proposed an alternative theory that the lateral interactions in the superior colliculus (SC), which are characterized by short-distance excitation and long-distance inhibition, are sufficient for generating both deviations towards and away from distractors. In the present study, we performed a meta-analysis of the literature, ran model simulations and conducted two behavioral experiments to further explore this unconventional theory. Confirming predictions generated by the model simulations, the behavioral experiments show that a) saccades deviate towards close distractors and away from remote distractors, and b) the amount of deviation depends on the strength of fixation activity in the SC, which can be manipulated by turning off the fixation stimulus before or after target onset (Experiment 1), or by varying the eccentricity of the target and distractor (Experiment 2).     

Eye Tracking the Face in the Crowd Task: Why Are Angry Faces Found More Quickly?

Among a crowd of distractor faces, threatening or angry target faces are identified more quickly and accurately than are nonthreatening or happy target faces, a finding known as the “face in the crowd effect.” Two perceptual explanations of the effect have been proposed: (1) the “target orienting” hypothesis (i.e., threatening targets orient attention more quickly than do nonthreatening targets and (2) the “distractor processing” hypothesis (i.e., nonthreatening distractors paired with a threatening target are processed more efficiently than vice versa, leading to quicker detection of threatening targets). Using a task, with real faces and multiple identities, the current study replicated the face in the crowd effect and then, via eye tracking, found greater support for the target orienting hypothesis. Across both the classical search asymmetry paradigm (i.e., one happy target in a crowd of angry distractors vs. one angry target in a crowd of happy distractors) and the constant distractor paradigm (i.e., one happy target in a crowd of neutral distractors vs. one angry target in a crowd of neutral distractors), fewer distractors were fixated before first fixating angry targets relative to happy targets, with no difference in the processing efficiency of distractors. These results suggest that the face in the crowd effect on this task is supported to a greater degree by attentional patterns associated with properties of target rather those of the crowd.     

Distractor Detection and Suppression Have a Beneficial Effect on Attentional Blink

Background

Attentional blink (AB) is a phenomenon that describes the difficulty individuals have in reporting the second of two masked targets if the second target (T2) arrives 200–500 ms after the first target (T1). Recent studies explain the AB from cognitive resources limitation to distractors interference. For example, the temporary loss of control (TLC) hypothesis suggests that the AB is conduced by distractors disrupting the input filter for target processing. The inhibition models suggest that the T1+1 distractor triggers a suppression mechanism which could be beneficial for T1 processing but would suppress T2 at short T1–T2 lags. These models consider that the AB is caused by the appearance of distractors. However, in the present study, two methods were taken to help individuals to detect the distractors more effectively. An attenuated AB deficit was found when the distractors could be excluded or suppressed in time. We consider that under an appropriate condition the distractors detection and suppression have a beneficial effect on attentional blink.

Methodology/Principal Findings

Two methods were employed to help individuals to detect the distractors more effectively: enlarging the low-level-physical characteristic difference between targets and distractors (Experiment 1) and restricting the sets of distractors (Experiment 2). Attenuated AB deficits were found as using the above manipulations.

Conclusions/Significance

The present study found when the distractors are detected or identified quickly, they could be effectively suppressed, in order to reduce the interference from the targets and result in a smaller AB deficit. We suggest that the suppression mechanism for distractors have a beneficial effect on AB.     

Attentional capture in rapid serial visual presentation

We examined whether attentional capture can occur during an attentional blink (AB). If attention were 'locked up' during an AB, capture should not occur. To test for capture, we varied the salience of the two targets (T1 and T2) or of a distractor. Salience was controlled by adjusting chromaticity at equiluminance to equate simple reaction times. Experiment 1 demonstrated that the extent of AB varied almost entirely with T2 salience, not with T1 salience. In Experiment 2, a salient distractor between T1 and T2 reduced the AB without affecting its temporal profile; a salient distractor after T2 had no effect on AB. We conclude that attentional capture can occur during the AB, and stimulus salience modulates, rather than overriding, the AB. Independent of the post-attentional (consolidation) mechanism primarily responsible for the AB, stimulus salience affects how an attention gate is triggered (Shih, 2000).     

Interference with bottom-up feature detection by higher-level object recognition

Drawing portraits upside down is a trick that allows novice artists to reproduce lower-level image features, e.g., contours, while reducing interference from higher-level face cognition. Limiting the available processing time to suffice for lower- but not higher-level operations is a more general way of reducing interference. We elucidate this interference in a novel visual-search task to find a target among distractors. The target had a unique lower-level orientation feature but was identical to distractors in its higher-level object shape. Through bottom-up processes, the unique feature attracted gaze to the target. Subsequently, recognizing the attended object as identically shaped as the distractors, viewpoint invariant object recognition interfered. Consequently, gaze often abandoned the target to search elsewhere. If the search stimulus was extinguished at time T after the gaze arrived at the target, reports of target location were more accurate for shorter (T<500 ms) presentations. This object-to-feature interference, though perhaps unexpected, could underlie common phenomena such as the visual-search asymmetry that finding a familiar letter N among its mirror images is more difficult than the converse. Our results should enable additional examination of known phenomena and interactions between different levels of visual processes.     

Distractor effects upon habituation of complex stimuli

In two experiments, rats were given serial forward (the target followed by the distractor) or backward (the distractor followed by the target) exposure to two compound flavor stimuli that could be either similar (Salt-X/AX) or dissimilar (Salt-X/AY, Experiment 1; Salt/AX, Experiment 2). Following pre-exposure, the Salt element was presented in a compound with a novel flavor, N. The salience or effectiveness of the Salt element was then assessed by presenting the new flavor, N, under a state of salt appetite. Experiments 1 and 2 revealed that the order of presentation modulated the habituation of the Salt element only when the distractor was similar to the target: the Salt element was more salient after forward than backward pre-exposure. In the groups Dissimilar the order of pre-exposure was irrelevant; however, when the Salt element was presented in compound with a second element (Salt-X, Experiment 1), its salience was preserved, whereas when it was presented alone (Salt, Experiment 2) its salience was significantly reduced. These results, which are discussed in terms of Wagner (1981) theory of habituation, inform about the way in which stimuli presented closely in time are processed.     

Location constancy and its effect on visual selection.

The present study investigated how location constancy influences selective attention to a cued location. The relative effectiveness of target/distractor distance and target/distractor compatibility were studied under covert and overt attention conditions. Experiment 1 measured reaction time and error rates to a scaled target letter that appeared at varied locations from 0.62 to 20 deg. Experiments 2 and 3 looked at covert/overt attention when the target location was fixed rather than varied within a block of trials. To provide a comprehensive assessment of the two primary variables across location constancy conditions, effect sizes for these results as well as for related past research (Goolkasian, 1999; Goolkasian and Tarantino, 1999) are presented. The findings suggest that the location of the target (foveal vs peripheral) does not influence attentional patterns as much as the consistency of its location. When a target appears at varied locations from trial to trial, distractor compatibility effects are in general stronger than the effect of target/distractor distance. However, the relative importance of these two variables reverses when the presentation location of the target is fixed at a constant location.     

Distractor Interference during a Choice Limb Reaching Task

According to action-centered models of attention, the patterns of distractor interference that emerge in selective reaching tasks are related to the time and effort required to resolve a race for activation between competing target and non-target response producing processes. Previous studies have only used unimanual aiming tasks and, as such, only examined the effects of competition that occurs within a limb. The results of studies using unimanual aiming movements often reveal an “ipsilateral effect” - distractors on the same side of space as the effector cause greater interference than distractors on the opposite side of space. The cost of the competition when response selection is between the limbs has yet to be addressed. Participants in the present study executed reaching movements to 1 of 4 (2 left, 2 right) possible target locations with and without a distractor. Participants made ipsilateral reaches (left hand to left targets, right hand to right targets). In contrast to studies using unimanual aiming movements, a “contralateral effect” was observed; distractors affording responses for the other hand (in contralateral space) caused more interference than distractors affording responses for the same hand. The findings from the present research demonstrate that when certain portions of response planning must be resolved prior to response initiation, distractors that code for that dimension cause the greatest interference.     

Famous faces demand attention due to reduced inhibitory processing

People have particular difficulty ignoring distractors that depict faces. This phenomenon has been attributed to the high level of biological significance that faces carry. The current study aimed to elucidate the mechanism by which faces gain processing priority. We used a focused attention paradigm that tracks the influence of a distractor over time and provides a measure of inhibitory processing. Upright famous faces served as test stimuli and inverted versions of the faces as well as upright non-face objects served as control stimuli. The results revealed that although all of the stimuli elicited similar levels of distraction, only inverted distractor faces and non-face objects elicited inhibitory effects. The lack of inhibitory effects for upright famous faces provides novel evidence that reduced inhibitory processing underlies the mandatory nature of face processing.     

Priming the Semantic Neighbourhood during the Attentional Blink

Background

When two targets are presented in close temporal proximity amongst a rapid serial visual stream of distractors, a period of disrupted attention and attenuated awareness lasting 200–500 ms follows identification of the first target (T1). This phenomenon is known as the “attentional blink” (AB) and is generally attributed to a failure to consolidate information in visual short-term memory due to depleted or disrupted attentional resources. Previous research has shown that items presented during the AB that fail to reach conscious awareness are still processed to relatively high levels, including the level of meaning. For example, missed word stimuli have been shown to prime later targets that are closely associated words. Although these findings have been interpreted as evidence for semantic processing during the AB, closely associated words (e.g., day-night) may also rely on specific, well-worn, lexical associative links which enhance attention to the relevant target.

Methodology/Principal Findings

We used a measure of semantic distance to create prime-target pairs that are conceptually close, but have low word associations (e.g., wagon and van) and investigated priming from a distractor stimulus presented during the AB to a subsequent target (T2). The stimuli were words (concrete nouns) in Experiment 1 and the corresponding pictures of objects in Experiment 2. In both experiments, report of T2 was facilitated when this item was preceded by a semantically-related distractor.

Conclusions/Significance

This study is the first to show conclusively that conceptual information is extracted from distractor stimuli presented during a period of attenuated awareness and that this information spreads to neighbouring concepts within a semantic network.     

Top-Down but Not Bottom-Up Visual Scanning is Affected in Hereditary Pure Cerebellar Ataxia

The aim of this study was to clarify the nature of visual processing deficits caused by cerebellar disorders. We studied the performance of two types of visual search (top-down visual scanning and bottom-up visual scanning) in 18 patients with pure cerebellar types of spinocerebellar degeneration (SCA6: 11; SCA31: 7). The gaze fixation position was recorded with an eye-tracking device while the subjects performed two visual search tasks in which they looked for a target Landolt figure among distractors. In the serial search task, the target was similar to the distractors and the subject had to search for the target by processing each item with top-down visual scanning. In the pop-out search task, the target and distractor were clearly discernible and the visual salience of the target allowed the subjects to detect it by bottom-up visual scanning. The saliency maps clearly showed that the serial search task required top-down visual attention and the pop-out search task required bottom-up visual attention. In the serial search task, the search time to detect the target was significantly longer in SCA patients than in normal subjects, whereas the search time in the pop-out search task was comparable between the two groups. These findings suggested that SCA patients cannot efficiently scan a target using a top-down attentional process, whereas scanning with a bottom-up attentional process is not affected. In the serial search task, the amplitude of saccades was significantly smaller in SCA patients than in normal subjects. The variability of saccade amplitude (saccadic dysmetria), number of re-fixations, and unstable fixation (nystagmus) were larger in SCA patients than in normal subjects, accounting for a substantial proportion of scattered fixations around the items. Saccadic dysmetria, re-fixation, and nystagmus may play important roles in the impaired top-down visual scanning in SCA, hampering precise visual processing of individual items.     

Emotional Modulation of Attention: Fear Increases but Disgust Reduces the Attentional Blink

Background

It is well known that facial expressions represent important social cues. In humans expressing facial emotion, fear may be configured to maximize sensory exposure (e.g., increases visual input) whereas disgust can reduce sensory exposure (e.g., decreases visual input). To investigate whether such effects also extend to the attentional system, we used the “attentional blink” (AB) paradigm. Many studies have documented that the second target (T2) of a pair is typically missed when presented within a time window of about 200–500 ms from the first to-be-detected target (T1; i.e., the AB effect). It has recently been proposed that the AB effect depends on the efficiency of a gating system which facilitates the entrance of relevant input into working memory, while inhibiting irrelevant input. Following the inhibitory response on post T1 distractors, prolonged inhibition of the subsequent T2 is observed. In the present study, we hypothesized that processing facial expressions of emotion would influence this attentional gating. Fearful faces would increase but disgust faces would decrease inhibition of the second target.

Methodology/Principal Findings

We showed that processing fearful versus disgust faces has different effects on these attentional processes. We found that processing fear faces impaired the detection of T2 to a greater extent than did the processing disgust faces. This finding implies emotion-specific modulation of attention.

Conclusions/Significance

Based on the recent literature on attention, our finding suggests that processing fear-related stimuli exerts greater inhibitory responses on distractors relative to processing disgust-related stimuli. This finding is of particular interest for researchers examining the influence of emotional processing on attention and memory in both clinical and normal populations. For example, future research could extend upon the current study to examine whether inhibitory processes invoked by fear-related stimuli may be the mechanism underlying the enhanced learning of fear-related stimuli.     

Distractor inhibition predicts individual differences in the attentional blink

Background

The attentional blink (AB) refers to humans'' impaired ability to detect the second of two targets (T2) in a rapid serial visual presentation (RSVP) stream of distractors if it appears within 200–600 ms of the first target (T1). Here we examined whether humans'' ability to inhibit distractors in the RSVP stream is a key determinant of individual differences in T1 performance and AB magnitude.

Methodology/Principal Findings

We presented subjects with RSVP streams (93.3 ms/item) of letters containing white distractors, a red T1 and a green T2. Subjects'' ability to suppress distractors was assessed by determining the extent to which their second target performance was primed by a preceding distractor that shared the same identity as T2. Individual subjects'' magnitude of T2 priming from this distractor was found to be negatively correlated with their T1 accuracy and positively related to their AB magnitude. In particular, subjects with attenuated ABs showed negative priming (i.e., worse T2 performance when the priming distractor appeared in the RSVP stream compared to when it was absent), whereas those with large ABs displayed positive priming (i.e., better T2 performance when the priming distractor appeared in the RSVP stream compared to when it was absent). Thus, a subject''s ability to suppress distractors, as assessed by T2 priming magnitude, predicted both their T1 performance and AB magnitude.

Conclusions/Significance

These results confirm that distractor suppression plays a key role in RSVP target selection and support the hypothesis that the AB results, at least in part, from a failure of distractor inhibition.     

Neuronal correlates of the set-size effect in monkey lateral intraparietal area

It has long been known that the brain is limited in the amount of sensory information that it can process at any given time. A well-known form of capacity limitation in vision is the set-size effect, whereby the time needed to find a target increases in the presence of distractors. The set-size effect implies that inputs from multiple objects interfere with each other, but the loci and mechanisms of this interference are unknown. Here we show that the set-size effect has a neural correlate in competitive visuo-visual interactions in the lateral intraparietal area, an area related to spatial attention and eye movements. Monkeys performed a covert visual search task in which they discriminated the orientation of a visual target surrounded by distractors. Neurons encoded target location, but responses associated with both target and distractors declined as a function of distractor number (set size). Firing rates associated with the target in the receptive field correlated with reaction time both within and across set sizes. The findings suggest that competitive visuo-visual interactions in areas related to spatial attention contribute to capacity limitations in visual searches.     

A Salient and Task-Irrelevant Collinear Structure Hurts Visual Search

Salient distractors draw our attention spontaneously, even when we intentionally want to ignore them. When this occurs, the real targets close to or overlapping with the distractors benefit from attention capture and thus are detected and discriminated more quickly. However, a puzzling opposite effect was observed in a search display with a column of vertical collinear bars presented as a task-irrelevant distractor [6]. In this case, it was harder to discriminate the targets overlapping with the salient distractor. Here we examined whether this effect originated from factors known to modulate attentional capture: (a) low probability—the probability occurrence of target location at the collinear column was much less (14%) than the rest of the display (86%), and observers might strategically direct their attention away from the collinear distractor; (b) attentional control setting—the distractor and target task interfered with each other because they shared the same continuity set in attentional task; and/or (c) lack of time to establish the optional strategy. We tested these hypotheses by (a) increasing to 60% the trials in which targets overlapped with the same collinear distractor columns, (b) replacing the target task to be connectivity-irrelevant (i.e., luminance discrimination), and (c) having our observers practice the same search task for 10 days. Our results speak against all these hypotheses and lead us to conclude that a collinear distractor impairs search at a level that is unaffected by probabilistic information, attentional setting, and learning.     

The Rapid Perceptual Impact of Emotional Distractors

The brief presentation of an emotional distractor can temporarily impair perception of a subsequent, rapidly presented target, an effect known as emotion-induced blindness (EIB). How rapidly does this impairment unfold? To probe this question, we examined EIB for targets that immediately succeeded (“lag-1”) emotional distractors in a rapid stream of items relative to EIB for targets at later serial positions. Experiments 1 and 2 suggested that emotional distractors interfere with items presented very soon after them, with impaired target perception emerging as early as lag-1. Experiment 3 included an exploratory examination of individual differences, which suggested that EIB onsets more rapidly among participants scoring high in measures linked to negative affect.     

Negative priming under rapid serial visual presentation

Negative priming (NP) was examined under a new paradigm wherein a target and distractors were temporally separated using rapid serial visual presentation (RSVP). The results from the two experiments revealed that (a) NP was robust under RSVP, such that the responses to a target were slower when the target served as a distractor in a previous trial than when it did not; (b) NP was found regardless of whether the distractors appeared before or after the targets; and (c) NP was stronger when the distractor was more distinctive. These findings are generally similar to those on NP in the spatial search task. The implications for the processes causing NP under RSVP are discussed in the current paper.     

Reward-Priming of Location in Visual Search

Existing visual search research has demonstrated that the receipt of reward will be beneficial for subsequent perceptual and attentional processing of features that have characterized targets, but detrimental for processing of features that have characterized irrelevant distractors. Here we report a similar effect of reward on location. Observers completed a visual search task in which they selected a target, ignored a salient distractor, and received random-magnitude reward for correct performance. Results show that when target selection garnered rewarding outcome attention is subsequently a.) primed to return to the target location, and b.) biased away from the location that was occupied by the salient, task-irrelevant distractor. These results suggest that in addition to priming features, reward acts to guide visual search by priming contextual locations of visual stimuli.     

What Determines Auditory Distraction? On the Roles of Local Auditory Changes and Expectation Violations

Both the acoustic variability of a distractor sequence and the degree to which it violates expectations are important determinants of auditory distraction. In four experiments we examined the relative contribution of local auditory changes on the one hand and expectation violations on the other hand in the disruption of serial recall by irrelevant sound. We present evidence for a greater disruption by auditory sequences ending in unexpected steady state distractor repetitions compared to auditory sequences with expected changing state endings even though the former contained fewer local changes. This effect was demonstrated with piano melodies (Experiment 1) and speech distractors (Experiment 2). Furthermore, it was replicated when the expectation violation occurred after the encoding of the target items (Experiment 3), indicating that the items'' maintenance in short-term memory was disrupted by attentional capture and not their encoding. This seems to be primarily due to the violation of a model of the specific auditory distractor sequences because the effect vanishes and even reverses when the experiment provides no opportunity to build up a specific neural model about the distractor sequence (Experiment 4). Nevertheless, the violation of abstract long-term knowledge about auditory regularities seems to cause a small and transient capture effect: Disruption decreased markedly over the course of the experiments indicating that participants habituated to the unexpected distractor repetitions across trials. The overall pattern of results adds to the growing literature that the degree to which auditory distractors violate situation-specific expectations is a more important determinant of auditory distraction than the degree to which a distractor sequence contains local auditory changes.     

The oculomotor distractor effect in normal and hemianopic vision

The present study investigated the inhibitory effect of visual distractors on the latency of saccades made by hemianopic and normal human subjects. The latency of saccades made by hemianopic subjects to stimuli in their intact visual field was not affected by visual distractors presented within their hemianopic field. In contrast, the latency of saccades made by normal subjects was increased significantly under distractor conditions. The latency increase was larger for temporal than nasal distractors. The results are inconsistent with previous proposals that the crossed retinotectal pathway from the nasal hemiretina to the superior colliculus may mediate a blindsight inhibitory effect when distractors appear within a hemianopic temporal visual field. Instead, the distractor effect appears to reflect the normal processes involved in saccade target selection which may be mediated by a circuit involving both cortical and subcortical structures.