The Competitive Influences of Perceptual Load and Working Memory Guidance on Selective Attention

The perceptual load theory in selective attention literature proposes that the interference from task-irrelevant distractor is eliminated when perceptual capacity is fully consumed by task-relevant information. However, the biased competition model suggests that the contents of working memory (WM) can guide attentional selection automatically, even when this guidance is detrimental to visual search. An intriguing but unsolved question is what will happen when selective attention is influenced by both perceptual load and WM guidance. To study this issue, behavioral performances and event-related potentials (ERPs) were recorded when participants were presented with a cue to either identify or hold in memory and had to perform a visual search task subsequently, under conditions of low or high perceptual load. Behavioural data showed that high perceptual load eliminated the attentional capture by WM. The ERP results revealed an obvious WM guidance effect in P1 component with invalid trials eliciting larger P1 than neutral trials, regardless of the level of perceptual load. The interaction between perceptual load and WM guidance was significant for the posterior N1 component. The memory guidance effect on N1 was eliminated by high perceptual load. Standardized Low Resolution Electrical Tomography Analysis (sLORETA) showed that the WM guidance effect and the perceptual load effect on attention can be localized into the occipital area and parietal lobe, respectively. Merely identifying the cue produced no effect on the P1 or N1 component. These results suggest that in selective attention, the information held in WM could capture attention at the early stage of visual processing in the occipital cortex. Interestingly, this initial capture of attention by WM could be modulated by the level of perceptual load and the parietal lobe mediates target selection at the discrimination stage.     

Complex backgrounds delay low-load visual search

Past research has shown, separately, that endogenous location cues and high perceptual load search tasks increase the specificity of attentional deployment to task-relevant regions of the visual field, while complex task-irrelevant backgrounds greatly resembling task-relevant stimuli reduce it. Here, we investigated in the same study whether the perceptual load created by an endogenously cued set of task-relevant stimuli determines whether a surrounding complex background of similar task-irrelevant stimuli would interfere with search. Our results show that high perceptual load protects against interference from a complex background of similar but task-irrelevant stimuli, situated just beyond the boundaries of the task-relevant set. Furthermore, our findings demonstrate that search characteristics do not change when the relevant set is restricted attentionally to a smaller delineated area, even in the presence of a background. Finally, we found that the efficacy of endogenous location cueing is not dependent on the type of search task that occurs in the cued area. Our findings also reveal that alternative attention-directing strategies, such as guided search and signal detection, may be employed in such tasks in the absence of endogenous location cueing.     

Attentional load modulates responses of human primary visual cortex to invisible stimuli

Visual neuroscience has long sought to determine the extent to which stimulus-evoked activity in visual cortex depends on attention and awareness. Some influential theories of consciousness maintain that the allocation of attention is restricted to conscious representations [1, 2]. However, in the load theory of attention [3], competition between task-relevant and task-irrelevant stimuli for limited-capacity attention does not depend on conscious perception of the irrelevant stimuli. The critical test is whether the level of attentional load in a relevant task would determine unconscious neural processing of invisible stimuli. Human participants were scanned with high-field fMRI while they performed a foveal task of low or high attentional load. Irrelevant, invisible monocular stimuli were simultaneously presented peripherally and were continuously suppressed by a flashing mask in the other eye [4]. Attentional load in the foveal task strongly modulated retinotopic activity evoked in primary visual cortex (V1) by the invisible stimuli. Contrary to traditional views [1, 2, 5, 6], we found that availability of attentional capacity determines neural representations related to unconscious processing of continuously suppressed stimuli in human primary visual cortex. Spillover of attention to cortical representations of invisible stimuli (under low load) cannot be a sufficient condition for their awareness.     

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.     

Temporal-Spatial Neural Activation Patterns Linked to Perceptual Encoding of Emotional Salience

It is well known that we continuously filter incoming sensory information, selectively allocating attention to what is important while suppressing distracting or irrelevant information. Yet questions remain about spatiotemporal patterns of neural processes underlying attentional biases toward emotionally significant aspects of the world. One index of affectively biased attention is an emotional variant of an attentional blink (AB) paradigm, which reveals enhanced perceptual encoding for emotionally salient over neutral stimuli under conditions of limited executive attention. The present study took advantage of the high spatial and temporal resolution of magnetoencephalography (MEG) to investigate neural activation related to emotional and neutral targets in an AB task. MEG data were collected while participants performed a rapid stimulus visual presentation task in which two target stimuli were embedded in a stream of distractor words. The first target (T1) was a number and the second (T2) either an emotionally salient or neutral word. Behavioural results replicated previous findings of greater accuracy for emotionally salient than neutral T2 words. MEG source analyses showed that activation in orbitofrontal cortex, characterized by greater power in the theta and alpha bands, and dorsolateral prefrontal activation were associated with successful perceptual encoding of emotionally salient relative to neutral words. These effects were observed between 250 and 550 ms, latencies associated with discrimination of perceived from unperceived stimuli. These data suggest that important nodes of both emotional salience and frontoparietal executive systems are associated with the emotional modulation of the attentional blink.     

Expectation Suppression in Early Visual Cortex Depends on Task Set

Stimulus expectation can modulate neural responses in early sensory cortical regions, with expected stimuli often leading to a reduced neural response. However, it is unclear whether this expectation suppression is an automatic phenomenon or is instead dependent on the type of task a subject is engaged in. To investigate this, human subjects were presented with visual grating stimuli in the periphery that were either predictable or non-predictable while they performed three tasks that differently engaged cognitive resources. In two of the tasks, the predictable stimulus was task-irrelevant and spatial attention was engaged at fixation, with a high load on either perceptual or working memory resources. In the third task, the predictable stimulus was task-relevant, and therefore spatially attended. We observed that expectation suppression is dependent on the cognitive resources engaged by a subjects’ current task. When the grating was task-irrelevant, expectation suppression for predictable items was visible in retinotopically specific areas of early visual cortex (V1-V3) during the perceptual task, but it was abolished when working memory was loaded. When the grating was task-relevant and spatially attended, there was no significant effect of expectation in early visual cortex. These results suggest that expectation suppression is not an automatic phenomenon, but dependent on attentional state and type of available cognitive resources.     

Task attention facilitates learning of task-irrelevant stimuli

Attention plays a fundamental role in visual learning and memory. One highly established principle of visual attention is that the harder a central task is, the more attentional resources are used to perform the task and the smaller amount of attention is allocated to peripheral processing because of limited attention capacity. Here we show that this principle holds true in a dual-task setting but not in a paradigm of task-irrelevant perceptual learning. In Experiment 1, eight participants were asked to identify either bright or dim number targets at the screen center and to remember concurrently presented scene backgrounds. Their recognition performances for scenes paired with dim/hard targets were worse than those for scenes paired with bright/easy targets. In Experiment 2, eight participants were asked to identify either bright or dim letter targets at the screen center while a task-irrelevant coherent motion was concurrently presented in the background. After five days of training on letter identification, participants improved their motion sensitivity to the direction paired with hard/dim targets improved but not to the direction paired with easy/bright targets. Taken together, these results suggest that task-irrelevant stimuli are not subject to the attentional control mechanisms that task-relevant stimuli abide.     

Perceptual load-dependent neural correlates of distractor interference inhibition

Background

The load theory of selective attention hypothesizes that distractor interference is suppressed after perceptual processing (i.e., in the later stage of central processing) at low perceptual load of the central task, but in the early stage of perceptual processing at high perceptual load. Consistently, studies on the neural correlates of attention have found a smaller distractor-related activation in the sensory cortex at high relative to low perceptual load. However, it is not clear whether the distractor-related activation in brain regions linked to later stages of central processing (e.g., in the frontostriatal circuits) is also smaller at high rather than low perceptual load, as might be predicted based on the load theory.

Methodology/Principal Findings

We studied 24 healthy participants using functional magnetic resonance imaging (fMRI) during a visual target identification task with two perceptual loads (low vs. high). Participants showed distractor-related increases in activation in the midbrain, striatum, occipital and medial and lateral prefrontal cortices at low load, but distractor-related decreases in activation in the midbrain ventral tegmental area and substantia nigra (VTA/SN), striatum, thalamus, and extensive sensory cortices at high load.

Conclusions

Multiple levels of central processing involving midbrain and frontostriatal circuits participate in suppressing distractor interference at either low or high perceptual load. For suppressing distractor interference, the processing of sensory inputs in both early and late stages of central processing are enhanced at low load but inhibited at high load.     

Impaired Attentional Disengagement from Stimuli Matching the Contents of Working Memory in Social Anxiety

Although many cognitive models in anxiety propose that an impaired top-down control enhances the processing of task-irrelevant stimuli, few studies have paid attention to task-irrelevant stimuli under a cognitive load task. In the present study, we investigated the effects of the working memory load on attention to task-irrelevant stimuli in trait social anxiety. The results showed that as trait social anxiety increased, participants were unable to disengage from task-irrelevant stimuli identical to the memory cue under low and high working memory loads. Impaired attentional disengagement was positively correlated with trait social anxiety. This impaired attentional disengagement was related to trait social anxiety, but not state anxiety. Our findings suggest that socially anxious people have difficulty in disengaging attention from a task-irrelevant memory cue owing to an impaired top-down control under a working memory load.     

Learned value magnifies salience-based attentional capture

Visual attention is captured by physically salient stimuli (termed salience-based attentional capture), and by otherwise task-irrelevant stimuli that contain goal-related features (termed contingent attentional capture). Recently, we reported that physically nonsalient stimuli associated with value through reward learning also capture attention involuntarily (Anderson, Laurent, & Yantis, PNAS, 2011). Although it is known that physical salience and goal-relatedness both influence attentional priority, it is unknown whether or how attentional capture by a salient stimulus is modulated by its associated value. Here we show that a physically salient, task-irrelevant distractor previously associated with a large reward slows visual search more than an equally salient distractor previously associated with a smaller reward. This magnification of salience-based attentional capture by learned value extinguishes over several hundred trials. These findings reveal a broad influence of learned value on involuntary attentional capture.     

Increased Early Processing of Task-Irrelevant Auditory Stimuli in Older Adults

The inhibitory deficit hypothesis of cognitive aging posits that older adults’ inability to adequately suppress processing of irrelevant information is a major source of cognitive decline. Prior research has demonstrated that in response to task-irrelevant auditory stimuli there is an age-associated increase in the amplitude of the N1 wave, an ERP marker of early perceptual processing. Here, we tested predictions derived from the inhibitory deficit hypothesis that the age-related increase in N1 would be 1) observed under an auditory-ignore, but not auditory-attend condition, 2) attenuated in individuals with high executive capacity (EC), and 3) augmented by increasing cognitive load of the primary visual task. ERPs were measured in 114 well-matched young, middle-aged, young-old, and old-old adults, designated as having high or average EC based on neuropsychological testing. Under the auditory-ignore (visual-attend) task, participants ignored auditory stimuli and responded to rare target letters under low and high load. Under the auditory-attend task, participants ignored visual stimuli and responded to rare target tones. Results confirmed an age-associated increase in N1 amplitude to auditory stimuli under the auditory-ignore but not auditory-attend task. Contrary to predictions, EC did not modulate the N1 response. The load effect was the opposite of expectation: the N1 to task-irrelevant auditory events was smaller under high load. Finally, older adults did not simply fail to suppress the N1 to auditory stimuli in the task-irrelevant modality; they generated a larger response than to identical stimuli in the task-relevant modality. In summary, several of the study’s findings do not fit the inhibitory-deficit hypothesis of cognitive aging, which may need to be refined or supplemented by alternative accounts.     

Valence-specific modulation in the accumulation of perceptual evidence prior to visual scene recognition

Visual scene recognition is a dynamic process through which incoming sensory information is iteratively compared with predictions regarding the most likely identity of the input stimulus. In this study, we used a novel progressive unfolding task to characterize the accumulation of perceptual evidence prior to scene recognition, and its potential modulation by the emotional valence of these scenes. Our results show that emotional (pleasant and unpleasant) scenes led to slower accumulation of evidence compared to neutral scenes. In addition, when controlling for the potential contribution of non-emotional factors (i.e., familiarity and complexity of the pictures), our results confirm a reliable shift in the accumulation of evidence for pleasant relative to neutral and unpleasant scenes, suggesting a valence-specific effect. These findings indicate that proactive iterations between sensory processing and top-down predictions during scene recognition are reliably influenced by the rapidly extracted (positive) emotional valence of the visual stimuli. We interpret these findings in accordance with the notion of a genuine positivity offset during emotional scene recognition.     

Perceptual Grouping Enhances Visual Plasticity

Visual perceptual learning, a manifestation of neural plasticity, refers to improvements in performance on a visual task achieved by training. Attention is known to play an important role in perceptual learning, given that the observer''s discriminative ability improves only for those stimulus feature that are attended. However, the distribution of attention can be severely constrained by perceptual grouping, a process whereby the visual system organizes the initial retinal input into candidate objects. Taken together, these two pieces of evidence suggest the interesting possibility that perceptual grouping might also affect perceptual learning, either directly or via attentional mechanisms. To address this issue, we conducted two experiments. During the training phase, participants attended to the contrast of the task-relevant stimulus (oriented grating), while two similar task-irrelevant stimuli were presented in the adjacent positions. One of the two flanking stimuli was perceptually grouped with the attended stimulus as a consequence of its similar orientation (Experiment 1) or because it was part of the same perceptual object (Experiment 2). A test phase followed the training phase at each location. Compared to the task-irrelevant no-grouping stimulus, orientation discrimination improved at the attended location. Critically, a perceptual learning effect equivalent to the one observed for the attended location also emerged for the task-irrelevant grouping stimulus, indicating that perceptual grouping induced a transfer of learning to the stimulus (or feature) being perceptually grouped with the task-relevant one. Our findings indicate that no voluntary effort to direct attention to the grouping stimulus or feature is necessary to enhance visual plasticity.     

How do we select perceptions and actions? Human brain imaging studies.

The selective nature of human perception and action implies a modulatory interaction between sensorimotor processes and attentional processes. This paper explores the use of functional imaging in humans to explore the mechanisms of perceptual selection and the fate of irrelevant stimuli that are not selected. Experiments with positron emission tomography show that two qualitatively different patterns of modulation of cerebral blood flow can be observed in experiments where non-spatial visual attention and auditory attention are manipulated. These patterns of modulation of cerebral blood flow modulation can be described as gain control and bias signal mechanisms. In visual and auditory cortex, the dominant change in cerebral blood flow associated with attention to either modality is related to a bias signal. The relation of these patterns of modulation to attentional effects that have been observed in single neurons is discussed. The existence of mechanisms for selective perception raises the more general question of whether irrelevant ignored stimuli are nevertheless perceived. Lavie''s theory of attention proposes that the degree to which ignored stimuli are processed varies depending on the perceptual load of the current task. Evidence from behavioural and functional magnetic resonance imaging studies of ignored visual motion processing is presented in support of this proposal.     

The Influence of a Working Memory Task on Affective Perception of Facial Expressions

In a dual-task paradigm, participants performed a spatial location working memory task and a forced two-choice perceptual decision task (neutral vs. fearful) with gradually morphed emotional faces (neutral ∼ fearful). Task-irrelevant word distractors (negative, neutral, and control) were experimentally manipulated during spatial working memory encoding. We hypothesized that, if affective perception is influenced by concurrent cognitive load using a working memory task, task-irrelevant emotional distractors would bias subsequent perceptual decision-making on ambiguous facial expression. We found that when either neutral or negative emotional words were presented as task-irrelevant working-memory distractors, participants more frequently reported fearful face perception - but only at the higher emotional intensity levels of morphed faces. Also, the affective perception bias due to negative emotional distractors correlated with a decrease in working memory performance. Taken together, our findings suggest that concurrent working memory load by task-irrelevant distractors has an impact on affective perception of facial expressions.     

Neural correlates of individual performance differences in resolving perceptual conflict

Attentional mechanisms are a crucial prerequisite to organize behavior. Most situations may be characterized by a 'competition' between salient, but irrelevant stimuli and less salient, relevant stimuli. In such situations top-down and bottom-up mechanisms interact with each other. In the present fMRI study, we examined how interindividual differences in resolving situations of perceptual conflict are reflected in brain networks mediating attentional selection. Doing so, we employed a change detection task in which subjects had to detect luminance changes in the presence and absence of competing distractors. The results show that good performers presented increased activation in the orbitofrontal cortex (BA 11), anterior cingulate (BA 25), inferior parietal lobule (BA 40) and visual areas V2 and V3 but decreased activation in BA 39. This suggests that areas mediating top-down attentional control are stronger activated in this group. Increased activity in visual areas reflects distinct neuronal enhancement relating to selective attentional mechanisms in order to solve the perceptual conflict. Opposed to good performers, brain areas activated by poor performers comprised the left inferior parietal lobule (BA 39) and fronto-parietal and visual regions were continuously deactivated, suggesting that poor performers perceive stronger conflict than good performers. Moreover, the suppression of neural activation in visual areas might indicate a strategy of poor performers to inhibit the processing of the irrelevant non-target feature. These results indicate that high sensitivity in perceptual areas and increased attentional control led to less conflict in stimulus processing and consequently to higher performance in competitive attentional selection.     

Reduced distractibility in a remote culture

Background

In visual processing, there are marked cultural differences in the tendency to adopt either a global or local processing style. A remote culture (the Himba) has recently been reported to have a greater local bias in visual processing than Westerners. Here we give the first evidence that a greater, and remarkable, attentional selectivity provides the basis for this local bias.

Methodology/Principal Findings

In Experiment 1, Eriksen-type flanker interference was measured in the Himba and in Western controls. In both groups, responses to the direction of a task-relevant target arrow were affected by the compatibility of task-irrelevant distractor arrows. However, the Himba showed a marked reduction in overall flanker interference compared to Westerners. The smaller interference effect in the Himba occurred despite their overall slower performance than Westerners, and was evident even at a low level of perceptual load of the displays. In Experiment 2, the attentional selectivity of the Himba was further demonstrated by showing that their attention was not even captured by a moving singleton distractor.

Conclusions/Significance

We argue that the reduced distractibility in the Himba is clearly consistent with their tendency to prioritize the analysis of local details in visual processing.     

Abnormal attentional modulation of retinotopic cortex in parietal patients with spatial neglect

Brain regions beyond visual cortex are thought to be responsible for attention-related modulation of visual processing [1, 2], but most evidence is indirect. Here, we applied functional magnetic resonance imaging (fMRI), including retinotopic mapping of visual areas, to patients with focal right-parietal lesions and left spatial neglect [3, 4]. When attentional load at fixation was minimal, retinotopic areas in right visual cortex showed preserved responses to task-irrelevant checkerboards in the contralateral left hemifield, analogously to left visual cortex for right-hemifield checkerboards, indicating a "symmetric" pattern in both hemispheres with respect to contralateral stimulation under these conditions. But when attentional load at fixation was increased, a functional asymmetry emerged for visual cortex, with contralateral responses in right visual areas being pathologically reduced (even eliminated for right V4/TEO), whereas left visual areas showed no such reduction in their contralateral response. These results reveal attention-dependent abnormalities in visual cortex after lesions in distant (parietal) regions. This may explain otherwise puzzling aspects of neglect [5, 6], as confirmed here by additional behavioral testing.     

Multiple spotlights of attentional selection in human visual cortex

Spatially directed attention strongly enhances visual perceptual processing. The metaphor of the "spotlight" has long been used to describe spatial attention; however, there has been considerable debate as to whether spatial attention must be unitary or may be split between discrete regions of space. This question was addressed here through functional MR imaging of human subjects as they performed a task that required simultaneous attention to two briefly displayed and masked targets at locations separated by distractor stimuli. These data reveal retinotopically specific enhanced activation in striate and extrastriate visual cortical representations of the two attended stimuli and no enhancement at the intervening representation of distractor stimuli. This finding of two spotlights was obtained within a single cortical hemisphere and across the two hemispheres. This provides direct evidence that spatial attention can select, in parallel, multiple low-level perceptual representations.     

Hemispheric Asymmetry in the Auditory Facilitation Effect in Dual-Stream Rapid Serial Visual Presentation Tasks

Even though auditory stimuli do not directly convey information related to visual stimuli, they often improve visual detection and identification performance. Auditory stimuli often alter visual perception depending on the reliability of the sensory input, with visual and auditory information reciprocally compensating for ambiguity in the other sensory domain. Perceptual processing is characterized by hemispheric asymmetry. While the left hemisphere is more involved in linguistic processing, the right hemisphere dominates spatial processing. In this context, we hypothesized that an auditory facilitation effect in the right visual field for the target identification task, and a similar effect would be observed in the left visual field for the target localization task. In the present study, we conducted target identification and localization tasks using a dual-stream rapid serial visual presentation. When two targets are embedded in a rapid serial visual presentation stream, the target detection or discrimination performance for the second target is generally lower than for the first target; this deficit is well known as attentional blink. Our results indicate that auditory stimuli improved target identification performance for the second target within the stream when visual stimuli were presented in the right, but not the left visual field. In contrast, auditory stimuli improved second target localization performance when visual stimuli were presented in the left visual field. An auditory facilitation effect was observed in perceptual processing, depending on the hemispheric specialization. Our results demonstrate a dissociation between the lateral visual hemifield in which a stimulus is projected and the kind of visual judgment that may benefit from the presentation of an auditory cue.