Controlling attention to nociceptive stimuli with working memory

Background

Because pain often signals the occurrence of potential tissue damage, a nociceptive stimulus has the capacity to involuntarily capture attention and take priority over other sensory inputs. Whether distraction by nociception actually occurs may depend upon the cognitive characteristics of the ongoing activities. The present study tested the role of working memory in controlling the attentional capture by nociception.

Methodology and Principal Findings

Participants performed visual discrimination and matching tasks in which visual targets were shortly preceded by a tactile distracter. The two tasks were chosen because of the different effects the involvement of working memory produces on performance, in order to dissociate the specific role of working memory in the control of attention from the effect of general resource demands. Occasionally (i.e. 17% of the trials), tactile distracters were replaced by a novel nociceptive stimulus in order to distract participants from the visual tasks. Indeed, in the control conditions (no working memory), reaction times to visual targets were increased when the target was preceded by a novel nociceptive distracter as compared to the target preceded by a frequent tactile distracter, suggesting attentional capture by the novel nociceptive stimulus. However, when the task required an active rehearsal of the visual target in working memory, the novel nociceptive stimulus no longer induced a lengthening of reaction times to visual targets, indicating a reduction of the distraction produced by the novel nociceptive stimulus. This effect was independent of the overall task demands.

Conclusion and Significance

Loading working memory with pain-unrelated information may reduce the ability of nociceptive input to involuntarily capture attention, and shields cognitive processing from nociceptive distraction. An efficient control of attention over pain is best guaranteed by the ability to maintain active goal priorities during achievement of cognitive activities and to keep pain-related information out of task settings.     

The attentional window modulates capture by audiovisual events

Visual search is markedly improved when a target color change is synchronized with a spatially non-informative auditory signal. This "pip and pop" effect is an automatic process as even a distractor captures attention when accompanied by a tone. Previous studies investigating visual attention have indicated that automatic capture is susceptible to the size of the attentional window. The present study investigated whether the pip and pop effect is modulated by the extent to which participants divide their attention across the visual field We show that participants were better in detecting a synchronized audiovisual event when they divided their attention across the visual field relative to a condition in which they focused their attention. We argue that audiovisual capture is reduced under focused conditions relative to distributed settings.     

High visual working memory capacity in trait social anxiety

Working memory capacity is one of the most important cognitive functions influencing individual traits, such as attentional control, fluid intelligence, and also psychopathological traits. Previous research suggests that anxiety is associated with impaired cognitive function, and studies have shown low verbal working memory capacity in individuals with high trait anxiety. However, the relationship between trait anxiety and visual working memory capacity is still unclear. Considering that people allocate visual attention more widely to detect danger under threat, visual working memory capacity might be higher in anxious people. In the present study, we show that visual working memory capacity increases as trait social anxiety increases by using a change detection task. When the demand to inhibit distractors increased, however, high visual working memory capacity diminished in individuals with social anxiety, and instead, impaired filtering of distractors was predicted by trait social anxiety. State anxiety was not correlated with visual working memory capacity. These results indicate that socially anxious people could potentially hold a large amount of information in working memory. However, because of an impaired cognitive function, they could not inhibit goal-irrelevant distractors and their performance decreased under highly demanding conditions.     

Content-specific working memory modulation of the attentional blink

Three experiments were conducted to investigate the effects of working memory content on temporal attention in a rapid serial visual presentation attentional blink paradigm. It was shown that categorical similarity between working memory content and the target stimuli pertaining to the attentional task (both digits) increased attentional blink magnitude compared to a condition in which this similarity was absent (colors and digits, respectively). This effect was only observed when the items in working memory were not presented as conjunctions of the involved categories (i.e., colored digits). This suggested that storage and retrieval from working memory was at least preferentially conjunctive in this case. It was furthermore shown that the content of working memory enhanced the identification rate of the second target, by means of repetition priming, when inter-target lag was short and the attentional blink was in effect. The results are incompatible with theories of temporal attention that assume working memory has no causal role in the attentional blink and support theories that do.     

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.     

Fine-Grained,Local Maps and Coarse,Global Representations Support Human Spatial Working Memory

While sensory processes are tuned to particular features, such as an object''s specific location, color or orientation, visual working memory (vWM) is assumed to store information using representations, which generalize over a feature dimension. Additionally, current vWM models presume that different features or objects are stored independently. On the other hand, configurational effects, when observed, are supposed to mainly reflect encoding strategies. We show that the location of the target, relative to the display center and boundaries, and overall memory load influenced recall precision, indicating that, like sensory processes, capacity limited vWM resources are spatially tuned. When recalling one of three memory items the target distance from the display center was overestimated, similar to the error when only one item was memorized, but its distance from the memory items'' average position was underestimated, showing that not only individual memory items'' position, but also the global configuration of the memory array may be stored. Finally, presenting the non-target items at recall, consequently providing landmarks and configurational information, improved precision and accuracy of target recall. Similarly, when the non-target items were translated at recall, relative to their position in the initial display, a parallel displacement of the recalled target was observed. These findings suggest that fine-grained spatial information in vWM is represented in local maps whose resolution varies with distance from landmarks, such as the display center, while coarse representations are used to store the memory array configuration. Both these representations are updated at the time of recall.     

Individual differences and metacognitive knowledge of visual search strategy

A crucial ability for an organism is to orient toward important objects and to ignore temporarily irrelevant objects. Attention provides the perceptual selectivity necessary to filter an overwhelming input of sensory information to allow for efficient object detection. Although much research has examined visual search and the 'template' of attentional set that allows for target detection, the behavior of individual subjects often reveals the limits of experimental control of attention. Few studies have examined important aspects such as individual differences and metacognitive strategies. The present study analyzes the data from two visual search experiments for a conjunctively defined target (Proulx, 2007). The data revealed attentional capture blindness, individual differences in search strategies, and a significant rate of metacognitive errors for the assessment of the strategies employed. These results highlight a challenge for visual attention studies to account for individual differences in search behavior and distractibility, and participants that do not (or are unable to) follow instructions.     

Feature-based attention in the frontal eye field and area V4 during visual search

When we search for a target in a crowded visual scene, we often use the distinguishing features of the target, such as color or shape, to guide our attention and eye movements. To investigate the neural mechanisms of feature-based attention, we simultaneously recorded neural responses in the frontal eye field (FEF) and area V4 while monkeys performed a visual search task. The responses of cells in both areas were modulated by feature attention, independent of spatial attention, and the magnitude of response enhancement was inversely correlated with the number of saccades needed to find the target. However, an analysis of the latency of sensory and attentional influences on responses suggested that V4 provides bottom-up sensory information about stimulus features, whereas the FEF provides a top-down attentional bias toward target features that modulates sensory processing in V4 and that could be used to guide the eyes to a searched-for target.     

Top-down modulation of lateral interactions in early vision: does attention affect integration of the whole or just perception of the parts?

Attention can modulate sensitivity to local stimuli in early vision. But, can attention also modulate integration of local stimuli into global visual patterns? We recently measured effects of attention on the phenomenon of lateral interactions between collinear elements, commonly thought to reflect long-range mechanisms in early visual cortex underlying contour integration. We showed improved detection of low-contrast central Gabor targets in the context of collinear flankers, but only when the collinear flankers were attended for a secondary task rather than ignored in favor of an orthogonal flanker pair. Here, we contrast two hypotheses for how attention might modulate flanker influences on the target: by changing just local sensitivity to the flankers themselves (flanker-modulation-only hypothesis), or by weighting integrative connections between flanker and target (connection-weighting hypothesis). Modeled on the known nonlinear dependence of target visibility on collinear flanker contrast, the first hypothesis predicts that an increase in physical flanker contrast should readily offset any reduction in their effective contrast when ignored, thus eliminating attentional modulation. Conversely, the second hypothesis predicts that attentional modulation should persist even for the highest flanker contrasts. Our results showed the latter outcome and indicated that attention modulates flanker-target integration, rather than just processing of local flanker elements.     

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.     

Alpha ERD and human visual selective attention

We compared the alpha band EEG depression (event-related desynchnization, ERD) level in two tasks, involving activation of different attentional processes: visual search for a deviant relevant stimulus among many similar ones and visual oddball. Control data for the visual search task consisted of simple viewing of several stimuli being of the same shape as the relevant stimulus in the search trials. Gaze position was verified by eye tracking method. We interpreted alpha band ERD as a correlate of activation of attentional processes. Fixating the target in visual search task caused a significantly larger ERD than fixating the same stimuli in control trials over all leads. We suppose this to be related with task and visual environment complexities. The frontal ERD domination may indicate attentional control over voluntary movements execution (top-down attention). The caudal ERD may be related with updating of visual information as a result of search process (bottom-up attention). Both relevant and irrelevant stimuli in the oddball task also induced alpha band ERD, but it was larger in response to relevant one and reached maximum level over occipital leads. Domination of caudal ERD in oddball task is supposed to indicate bottom-up attention processes.     

Selective visual processing across competition episodes: a theory of task-driven visual attention and working memory

The goal of this review is to introduce a theory of task-driven visual attention and working memory (TRAM). Based on a specific biased competition model, the ‘theory of visual attention’ (TVA) and its neural interpretation (NTVA), TRAM introduces the following assumption. First, selective visual processing over time is structured in competition episodes. Within an episode, that is, during its first two phases, a limited number of proto-objects are competitively encoded—modulated by the current task—in activation-based visual working memory (VWM). In processing phase 3, relevant VWM objects are transferred via a short-term consolidation into passive VWM. Second, each time attentional priorities change (e.g. after an eye movement), a new competition episode is initiated. Third, if a phase 3 VWM process (e.g. short-term consolidation) is not finished, whereas a new episode is called, a protective maintenance process allows its completion. After a VWM object change, its protective maintenance process is followed by an encapsulation of the VWM object causing attentional resource costs in trailing competition episodes. Viewed from this perspective, a new explanation of key findings of the attentional blink will be offered. Finally, a new suggestion will be made as to how VWM items might interact with visual search processes.     

Errors Disrupt Subsequent Early Attentional Processes

It has been demonstrated that target detection is impaired following an error in an unrelated flanker task. These findings support the idea that the occurrence or processing of unexpected error-like events interfere with subsequent information processing. In the present study, we investigated the effect of errors on early visual ERP components. We therefore combined a flanker task and a visual discrimination task. Additionally, the intertrial interval between both tasks was manipulated in order to investigate the duration of these negative after-effects. The results of the visual discrimination task indicated that the amplitude of the N1 component, which is related to endogenous attention, was significantly decreased following an error, irrespective of the intertrial interval. Additionally, P3 amplitude was attenuated after an erroneous trial, but only in the long-interval condition. These results indicate that low-level attentional processes are impaired after errors.     

Domain-Specific Control of Selective Attention

Previous research has shown that loading information on working memory affects selective attention. However, whether the load effect on selective attention is domain-general or domain-specific remains unresolved. The domain-general effect refers to the findings that load in one content (e.g. phonological) domain in working memory influences processing in another content (e.g., visuospatial) domain. Attentional control supervises selection regardless of information domain. The domain-specific effect refers to the constraint of influence only when maintenance and processing operate in the same domain. Selective attention operates in a specific content domain. This study is designed to resolve this controversy. Across three experiments, we manipulated the type of representation maintained in working memory and the type of representation upon which the participants must exert control to resolve conflict and select a target into the focus of attention. In Experiments 1a and 1b, participants maintained digits and nonverbalized objects, respectively, in working memory while selecting a target in a letter array. In Experiment 2, we presented auditory digits with a letter flanker task to exclude the involvement of resource competition within the same input modality. In Experiments 3a and 3b, we replaced the letter flanker task with an object flanker task while manipulating the memory load on object and digit representation, respectively. The results consistently showed that memory load modulated distractibility only when the stimuli of the two tasks were represented in the same domain. The magnitude of distractor interference was larger under high load than under low load, reflecting a lower efficacy of information prioritization. When the stimuli of the two tasks were represented in different domains, memory load did not modulate distractibility. Control of processing priority in selective attention demands domain-specific resources.     

Set-size effects for spatial frequency change and discrimination in multiple targets

In visual search tasks with a near-threshold target amongst distracters, log detection thresholds rise in proportion to the log of the number of stimuli. Previous research has shown a very steep slope for this set-size effect where the target is a change in spatial frequency (SF) across an ISI, suggesting a low-level explanation for 'change blindness (Wright et al., 2000). Here, we analyse stimulus and task variables in order to determine the contributions of stimulus detection and attention processes. Stimuli consisted of two 150 ms frames each containing 1 to 4 Gabor targets, with an ISI of 250 ms. In a 2AFC detection task with uniform distracters, slopes of 0.23-0.52 were found, in line with visual search results. 2AFC SF discrimination tasks gave slopes of 0.68, 0.69 with homogeneous distracters and 0.76-0.96 with inhomogeneous distracters, consistent with averaging of stimuli within a frame. If the distracters were also made to change across ISI, averaging was impossible, and focal attention was required to solve the discrimination. This always gave set-size slopes > 1. It is concluded that, under conditions where a stimulus array can be analysed globally, change detection performance is limited by signal detection mechanisms, rather than limited capacity attention or memory mechanisms. However, where this is prevented, for example by changing more than one item, limitations due to attention or memory produce an even steeper set-size effect.     

The Frontal Eye Fields Limit the Capacity of Visual Short-Term Memory in Rhesus Monkeys

The frontal eye fields (FEF) in rhesus monkeys have been implicated in visual short-term memory (VSTM) as well as control of visual attention. Here we examined the importance of the area in the VSTM capacity and the relationship between VSTM and attention, using the chemical inactivation technique and multi-target saccade tasks with or without the need of target-location memory. During FEF inactivation, serial saccades to targets defined by color contrast were unaffected, but saccades relying on short-term memory were impaired when the target count was at the capacity limit of VSTM. The memory impairment was specific to the FEF-coded retinotopic locations, and subject to competition among targets distributed across visual fields. These results together suggest that the FEF plays a crucial role during the entry of information into VSTM, by enabling attention deployment on targets to be remembered. In this view, the memory capacity results from the limited availability of attentional resources provided by FEF: The FEF can concurrently maintain only a limited number of activations to register the targets into memory. When lesions render part of the area unavailable for activation, the number would decrease, further reducing the capacity of VSTM.     

Attentional Requirements on Feature Search Are Modulated by Stimulus Properties

We report a series of dual-task experiments, in which a rapid serial visual presentation (RSVP) task was combined with a visual search task. Orientation, motion, and color were used as the defining target features in the search task. Lag between target onsets was manipulated and interference between the two tasks was quantified by measuring detection scores for the search task as a function of lag. While simultaneous performance of an orientation detection task with an RSVP letter identification task resulted in a performance decrease for lags up to 320 ms, no such decrease was detected for highly salient motion- and color-defined targets. Subsequently, detectability of the motion and color feature was matched to that of the orientation-feature resulting in the reintroduction of a (smaller) performance decrease, but only during simultaneous performance (lag 0 ms). The results suggest that there are two causes for the impaired search performance occurring when a feature search task is combined with an RSVP task. The first is short-lasting interference probably due to attentional competition; the second, which plays a role only when targets for both tasks share features, is interference that may be attributed to a central processing bottleneck.     

The Effects of Feature-Based Priming and Visual Working Memory on Oculomotor Capture

Recently, it has been demonstrated that objects held in working memory can influence rapid oculomotor selection. This has been taken as evidence that perceptual salience can be modified by active working memory representations. The goal of the present study was to examine whether these results could also be caused by feature-based priming. In two experiments, participants were asked to saccade to a target line segment of a certain orientation that was presented together with a to-be-ignored distractor. Both objects were given a task-irrelevant color that varied per trial. In a secondary task, a color had to be memorized, and that color could either match the color of the target, match the color of the distractor, or it did not match the color of any of the objects in the search task. The memory task was completed either after the search task (Experiment 1), or before it (Experiment 2). The results showed that in both experiments the memorized color biased oculomotor selection. Eye movements were more frequently drawn towards objects that matched the memorized color, irrespective of whether the memory task was completed after (Experiment 1) or before (Experiment 2) the search task. This bias was particularly prevalent in short-latency saccades. The results show that early oculomotor selection performance is not only affected by properties that are actively maintained in working memory but also by those previously memorized. Both working memory and feature priming can cause early biases in oculomotor selection.     

Effective visual working memory capacity: an emergent effect from the neural dynamics in an attractor network

The study of working memory capacity is of outmost importance in cognitive psychology as working memory is at the basis of general cognitive function. Although the working memory capacity limit has been thoroughly studied, its origin still remains a matter of strong debate. Only recently has the role of visual saliency in modulating working memory storage capacity been assessed experimentally and proved to provide valuable insights into working memory function. In the computational arena, attractor networks have successfully accounted for psychophysical and neurophysiological data in numerous working memory tasks given their ability to produce a sustained elevated firing rate during a delay period. Here we investigate the mechanisms underlying working memory capacity by means of a biophysically-realistic attractor network with spiking neurons while accounting for two recent experimental observations: 1) the presence of a visually salient item reduces the number of items that can be held in working memory, and 2) visually salient items are commonly kept in memory at the cost of not keeping as many non-salient items.OUR MODEL SUGGESTS THAT WORKING MEMORY CAPACITY IS DETERMINED BY TWO FUNDAMENTAL PROCESSES: encoding of visual items into working memory and maintenance of the encoded items upon their removal from the visual display. While maintenance critically depends on the constraints that lateral inhibition imposes to the mnemonic activity, encoding is limited by the ability of the stimulated neural assemblies to reach a sufficiently high level of excitation, a process governed by the dynamics of competition and cooperation among neuronal pools. Encoding is therefore contingent upon the visual working memory task and has led us to introduce the concept of effective working memory capacity (eWMC) in contrast to the maximal upper capacity limit only reached under ideal conditions.     

Retinotopic mapping of categorical and coordinate spatial relation processing in early visual cortex

Spatial relations are commonly divided in two global classes. Categorical relations concern abstract relations which define areas of spatial equivalence, whereas coordinate relations are metric and concern exact distances. Categorical and coordinate relation processing are thought to rely on at least partially separate neurocognitive mechanisms, as reflected by differential lateralization patterns, in particular in the parietal cortex. In this study we address this textbook principle from a new angle. We studied retinotopic activation in early visual cortex, as a reflection of attentional distribution, in a spatial working memory task with either a categorical or a coordinate instruction. Participants were asked to memorize a dot position, with regard to a central cross, and to indicate whether a subsequent dot position matched the first dot position, either categorically (opposite quadrant of the cross) or coordinately (same distance to the centre of the cross). BOLD responses across the retinotopic maps of V1, V2, and V3 indicate that the spatial distribution of cortical activity was different for categorical and coordinate instructions throughout the retention interval; a more local focus was found during categorical processing, whereas focus was more global for coordinate processing. This effect was strongest for V3, approached significance in V2 and was absent in V1. Furthermore, during stimulus presentation the two instructions led to different levels of activation in V3 during stimulus encoding; a stronger increase in activity was found for categorical processing. Together this is the first demonstration that instructions for specific types of spatial relations may yield distinct attentional patterns which are already reflected in activity early in the visual cortex.