Filtering distractors is costly.

To find a target in visual search, it is often necessary to filter out task-irrelevant distractors. People find the process of distractor filtering effortful, exerting physical effort to reduce the number of distractors that need to be filtered on a given search trial. Working memory demands are sufficiently costly that people are sometimes willing to accept aversive heat stimulation in exchange for the ability to avoid performing a working memory task. The present study examines whether filtering distractors in visual search is similarly costly. The findings reveal that individuals are sometimes willing to accept an electric shock in exchange for the ability to skip a single trial of visual search, increasingly so as the demands of distractor filtering increase. This was true even when acceptance of shock resulted in no overall time savings, although acceptance of shock was overall infrequent and influenced by a plurality of factors, including boredom and curiosity. These findings have implications for our understanding of the mental burden of distractor filtering and why people seek to avoid cognitive effort more broadly.

Observational learning of threat-related attentional bias.

Attentional bias to threat has been almost exclusively examined after participants experienced repeated pairings between a conditioned stimulus (CS) and an aversive unconditioned stimulus (US). This study aimed to determine whether threat-related attentional capture can result from observational learning, when participants acquire knowledge of the aversive qualities of a stimulus without themselves experiencing aversive outcomes. Non-clinical young-adult participants (N = 38) first watched a video of an individual (the demonstrator) performing a Pavlovian conditioning task in which one colour was paired with shock (CS+) and another colour was neutral (CS-). They then carried out visual search for a shape-defined target. Oculomotor measures evidenced an attentional bias toward the CS+ colour, suggesting that threat-related attentional capture can ensue from observational learning. Exploratory analyses also revealed that this effect was positively correlated with empathy for the demonstrator. Our findings extend empirical and theoretical knowledge about threat-driven attention and provide valuable insights to better understand the formation of anxiety disorders.

Reward history modulates visual attention in an avian model.

Attention can be biased towards previously reward-associated stimuli even when they are task-irrelevant and physically non-salient, although studies of reward-modulated attention have been largely limited to primate (including human and nonhuman) models. Birds have been shown to have the capacity to discriminate reward and spatial cues in a manner similar to primates, but whether reward history involuntarily affects their attention in the same way remains unclear. We adapted a spatial cueing paradigm with differential rewards to investigate how reward modulates the allocation of attention in peafowl (Pavo cristatus). The birds were required to locate and peck a target on a computer screen that was preceded by a high-value or low-value color cue that was uninformative with respect to the location of the upcoming target. All birds exhibited a validity effect (performance enhanced on valid compared to invalid cue), and an interaction effect between value and validity was evident at the group level, being particularly pronounced in the birds with the greatest amount of reward training. The time course of reward learning was conspicuously incremental, phenomenologically slower compared to primates. Our findings suggest a similar influence of reward history on attention across phylogeny despite a significant difference in neuroanatomy.

Value-Biased Competition in the Auditory System of the Brain.

Attentional capture by previously reward-associated stimuli has predominantly been measured in the visual domain. Recently, behavioral studies of value-driven attention have demonstrated involuntary attentional capture by previously reward-associated sounds, emulating behavioral findings within the visual domain and suggesting a common mechanism of attentional capture by value across sensory modalities. However, the neural correlates of the modulatory role of learned value on the processing of auditory information has not been examined. Here, we conducted a neuroimaging study on human participants using a previously established behavioral paradigm that measures value-driven attention in an auditory target identification task. We replicate behavioral findings of both voluntary prioritization and involuntary attentional capture by previously reward-associated sounds. When task-relevant, the selective processing of high-value sounds is supported by reduced activation in the dorsal attention network of the visual system (FEF, intraparietal sulcus, right middle frontal gyrus), implicating cross-modal processes of biased competition. When task-irrelevant, in contrast, high-value sounds evoke elevated activation in posterior parietal cortex and are represented with greater fidelity in the auditory cortex. Our findings reveal two distinct mechanisms of prioritizing reward-related auditory signals, with voluntary and involuntary modes of orienting that are differently manifested in biased competition.

Motivational Salience Guides Attention to Valuable and Threatening Stimuli: Evidence from Behavior and Functional Magnetic Resonance Imaging.

Rewarding and aversive outcomes have opposing effects on behavior, facilitating approach and avoidance, although we need to accurately anticipate each type of outcome to behave effectively. Attention is biased toward stimuli that have been learned to predict either type of outcome, and it remains an open question whether such orienting is driven by separate systems for value- and threat-based orienting or whether there exists a common underlying mechanism of attentional control driven by motivational salience. Here, we provide a direct comparison of the neural correlates of value- and threat-based attentional capture after associative learning. Across multiple measures of behavior and brain activation, our findings overwhelmingly support a motivational salience account of the control of attention. We conclude that there exists a core mechanism of experience-dependent attentional control driven by motivational salience and that prior characterizations of attention as being value driven or supporting threat monitoring need to be revisited.

Attentional avoidance of threatening stimuli.

Aversive conditioning has been shown to influence the control of attention, such that aversively conditioned stimuli receive elevated priority. Although aversively conditioned but task-irrelevant distractors are known to capture attention during speeded search in rapid orienting tasks, it is unclear whether this bias extends to situations where orienting can be more deliberate. We demonstrate that punishment, via electric shock, does not give rise to oculomotor capture by shock-associated stimuli during a foraging task; rather, such aversively conditioned stimuli are actively avoided when searching through a display. On the other hand, even during a foraging task, we found some evidence for a covert attentional bias to threat. Our findings indicate that the previously described effects of aversive conditioning on visual search may not generalize beyond the initial glance and can be suppressed when conditions allow for more deliberate search strategies. More generally, our findings reveal that sustained attentional avoidance of aversively conditioned stimuli is possible during active search.

The influence of threat on the efficiency of goal-directed attentional control.

Anxiety has consistently been found to potentiate attentional capture by physically salient stimuli, which could be due to enhanced distractor processing, impaired goal-directed attention, or both. At the same time, a recent study demonstrated that a threat manipulation reduces attentional capture by reward-associated stimuli, suggesting that anxiety does not increase distractibility or, otherwise, interfere with the control of attention generally. Here, we experimentally induced anxiety via threat-of-shock in the adaptive choice visual search task to examine whether the experience of threat influences goal-directed attentional control. Participants chose to search through one of two task-relevant colors on each trial, where searching through the less abundant color would be optimal for maximizing performance. Performance was evaluated with and without the threat of unpredictable electric shock. Under threat, participants were more optimal in their visual search and missed fewer targets. Performance improvements were demonstrated on trials that the optimal target color switched, demonstrating that threat is beneficial in adapting to changing attentional demands. Our findings demonstrate that threat can facilitate the efficiency of goal-directed attentional control and are at odds with an antagonistic relationship between anxiety and the control of attention.

Inertia in value-driven attention.

Previously reward-associated stimuli persistently capture attention. We attempted to extinguish this attentional bias through a reversal learning procedure where the high-value color changed unexpectedly. Attentional priority shifted during training in favor of the currently high-value color, although a residual bias toward the original high-value color was still evident. Importantly, during a subsequent test phase, attention was initially more strongly biased toward the original high-value color, counter to the attentional priorities evident at the end of training. Our results show that value-based attentional biases do not quickly update with new learning and lag behind the reshaping of strategic attentional priorities by reward.

Using aversive conditioning with near-real-time feedback to shape eye movements during naturalistic viewing.

Strategically shaping patterns of eye movements through training has manifold promising applications, with the potential to improve the speed and efficiency of visual search, improve the ability of humans to extract information from complex displays, and help correct disordered eye movement patterns. However, training how a person moves their eyes when viewing an image or scene is notoriously difficult, with typical approaches relying on explicit instruction and strategy, which have notable limitations. The present study introduces a novel approach to eye movement training using aversive conditioning with near-real-time feedback. Participants viewed indoor scenes (eight scenes presented over 48 trials) with the goal of remembering those scenes for a later memory test. During viewing, saccades meeting specific amplitude and direction criteria probabilistically triggered an aversive electric shock, which was felt within 50 ms after the eliciting eye movement, allowing for a close temporal coupling between an oculomotor behavior and the feedback intended to shape it. Results demonstrate a bias against performing an initial saccade in the direction paired with shock (Experiment 1) or generally of the amplitude paired with shock (Experiment 2), an effect that operates without apparent awareness of the relationship between shocks and saccades, persists into extinction, and generalizes to the viewing of novel images. The present study serves as a proof of concept concerning the implementation of near-real-time feedback in eye movement training.

The effect of concurrent reward on aversive information processing in the brain.

Neural networks for the processing of appetitive and aversive information, in isolation, have been well characterized. However, how the brain integrates competing signals associated with simultaneous appetitive and aversive information is less clear. In particular, it is unknown how the presence of concurrent reward modulates the processing of an aversive event throughout the brain. Here, we utilized a four-armed bandit task in an fMRI study to measure the representation of an aversive electric shock with and without the simultaneous receipt of monetary reward. Using a region of interest (ROI) approach, we first identified regions activated by the experience of aversive electric shock, and then measured how this shock-related activation is modulated by concurrent reward using independent data. Informed by prior literature and our own preliminary data, analyses focused on the dorsolateral prefrontal cortex, anterior and posterior insula, anterior cingulate cortex, and the thalamus and somatosensory cortex. We hypothesized that the neural response to punishment in these ROIs would be attenuated by the presence of concurrent reward. However, we found no evidence of concurrent reward attenuating the neural response to punishment in any ROI and also no evidence of concurrent punishment attenuating the neural response to reward in exploratory analyses. Altogether, our findings are consistent with the idea that neural networks responsible for the processing of reward and punishment signals are largely independent of one another, and that representations of overall value or utility are arrived at through the integration of separate reward and punishment signals at later stages of information processing.

Measuring attention to reward as an individual trait: the value-driven attention questionnaire (VDAQ).

Reward history is a powerful determinant of what we pay attention to. This influence of reward on attention varies substantially across individuals, being related to a variety of personality variables and clinical conditions. Currently, the ability to measure and quantify attention-to-reward is restricted to the use of psychophysical laboratory tasks, which limits research into the construct in a variety of ways. In the present study, we introduce a questionnaire designed to provide a brief and accessible means of assessing attention-to-reward. Scores on the questionnaire correlate with other measures known to be related to attention-to-reward and predict performance on multiple laboratory tasks measuring the construct. In demonstrating this relationship, we also provide evidence that attention-to-reward as measured in the lab, an automatic and implicit bias in information processing, is related to overt behaviors and motivations in everyday life as assessed via the questionnaire. Variation in scores on the questionnaire is additionally associated with a distinct biomarker in brain connectivity, and the questionnaire exhibits acceptable test-retest reliability. Overall, the Value-Driven Attention Questionnaire (VDAQ) provides a useful proxy-measure of attention-to-reward that is much more accessible than typical laboratory assessments.

Semantic generalization of value-based attentional priority.

This study aimed to determine whether attentional prioritization of stimuli associated with reward transfers across conceptual knowledge independently of physical features. Participants successively performed two color-word Stroop tasks. In the learning phase, neutral words were associated with high, low, or no monetary reward. In the generalization phase (in which no reward was delivered), synonyms of words previously paired with reward served as Stroop stimuli. Results are consistent with semantic generalization of stimulus-reward associations, with synonyms of high-value words impairing color-naming performance, although this effect was particular to participants who were unaware of the reward contingencies.

Neural evidence for automatic value-modulated approach behaviour.

Reward learning has the ability to bias both attention and behaviour. The current study presents behavioural and neural evidence that irrelevant responses evoked by previously reward-associated stimuli are more robustly represented in the motor system using a combined go/no-go and flankers task. Following a colour-reward association training, participants were instructed to respond to a central target only in a response-relevant context, while ignoring flankers that appeared either in a high-value or low-value colour. The motor cortex and cerebellum exhibited reduced activation to low-value flankers in a response-irrelevant context, consistent with goal-directed response suppression. However, these same regions exhibited similar activation to high-value flankers regardless of their response relevance, indicating less effective suppression, and the resulting interaction in motor cortex activation was strongly predicted by the influence of the flankers on behaviour. These findings suggest that associative reward learning produces a general approach bias, which is particularly evident when it conflicts with task goals, extending the principle of value-driven attention to stimulus-evoked responses in the motor system.

Test-retest reliability of value-driven attentional capture.

Attention is biased toward learned predictors of reward. The degree to which attention is automatically drawn to arbitrary reward cues has been linked to a variety of psychopathologies, including drug dependence, HIV-risk behaviors, depressive symptoms, and attention deficit/hyperactivity disorder. In the context of addiction specifically, attentional biases toward drug cues have been related to drug craving and treatment outcomes. Given the potential role of value-based attention in psychopathology, the ability to quantify the magnitude of such bias before and after a treatment intervention in order to assess treatment-related changes in attention allocation would be desirable. However, the test-retest reliability of value-driven attentional capture by arbitrary reward cues has not been established. In the present study, we show that an oculomotor measure of value-driven attentional capture produces highly robust test-retest reliability for a behavioral assessment, whereas the response time (RT) measure more commonly used in the attentional bias literature does not. Our findings provide methodological support for the ability to obtain a reliable measure of susceptibility to value-driven attentional capture at multiple points in time, and they highlight a limitation of RT-based measures that should inform the use of attentional-bias tasks as an assessment tool.

On the representational nature of value-driven spatial attentional biases.

Reward learning biases attention toward both reward-associated objects and reward-associated regions of space. The relationship between objects and space in the value-based control of attention, as well as the contextual specificity of space-reward pairings, remains unclear. In the present study, using a free-viewing task, we provide evidence of overt attentional biases toward previously rewarded regions of texture scenes that lack objects. When scrutinizing a texture scene, participants look more frequently toward, and spend a longer amount of time looking at, regions that they have repeatedly oriented to in the past as a result of performance feedback. These biases were scene specific, such that different spatial contexts produced different patterns of habitual spatial orienting. Our findings indicate that reinforcement learning can modify looking behavior via a representation that is purely spatial in nature in a context-specific manner. NEW & NOTEWORTHY The representational nature of space in the value-driven control of attention remains unclear. Here, we provide evidence for scene-specific overt spatial attentional biases following reinforcement learning, even though the scenes contained no objects. Our findings indicate that reinforcement learning can modify looking behavior via a representation that is purely spatial in nature in a context-specific manner.

Linking dopaminergic reward signals to the development of attentional bias: A positron emission tomographic study.

The attention system is shaped by reward history, such that learned reward cues involuntarily draw attention. Recent research has begun to uncover the neural mechanisms by which learned reward cues compete for attention, implicating dopamine (DA) signaling within the dorsal striatum. How these elevated priority signals develop in the brain during the course of learning is less well understood, as is the relationship between value-based attention and the experience of reward during learning. We hypothesized that the magnitude of the striatal DA response to reward during learning contributes to the development of a learned attentional bias towards the cue that predicted it, and examined this hypothesis using positron emission tomography with [11C]raclopride. We measured changes in dopamine release for rewarded versus unrewarded visual search for color-defined targets as indicated by the density and distribution of the available D2/D3 receptors. We then tested for correlations of individual differences in this measure of reward-related DA release to individual differences in the degree to which previously reward-associated but currently task-irrelevant stimuli impair performance in an attention task (i.e., value-driven attentional bias), revealing a significant relationship in the right anterior caudate. The degree to which reward-related DA release was right hemisphere lateralized was also predictive of later attentional bias. Our findings provide support for the hypothesis that value-driven attentional bias can be predicted from reward-related DA release during learning.

Density of available striatal dopamine receptors predicts trait impulsiveness during performance of an attention-demanding task.

The density (measured at binding potential) of available striatal D2/D3 receptors has been shown to predict trait impulsiveness. This relationship is highly robust and well replicated. In each case, however, the availability of dopamine receptors was measured at rest. More broadly, the extent to which relationships between dopamine receptor availability and behavioral traits hold when participants perform a cognitive task is unclear. Furthermore, the performance of a cognitive task engages fundamentally different neural networks than are maximally engaged during the resting state. This complicates interpretation of previously observed correlations, which could be influenced by two distinct factors. The first is variation in available receptor density, which reflects a stable trait of the individual. The second is variation in context-specific dopamine release, which differentially displaces some dopamine radiotracers (such as raclopride) across individuals. Using an existing data set, we related trait impulsiveness, as measured using the Barratt Impulsiveness Scale (BIS-11), to the density (binding potential) of available striatal D2/D3 receptors as measured using positron emission tomography (PET) with [11C]raclopride. Importantly, the PET scan was completed while participants performed an attention-demanding visual search task. We replicate robust correlations between this measure of receptor availability and trait impulsiveness previously demonstrated during the resting state, extending this relationship to periods of active task engagement. Our results support the idea that this relationship depends on striatal D2/D3 receptor density and not on context-dependent dopamine release.NEW & NOTEWORTHY Several studies have demonstrated a relationship between the density of available striatal D2/D3 receptors and trait impulsiveness. However, in each case, the availability of dopamine receptors was measured during the resting state. This complicates interpretation of previously observed correlations, which could be influenced by either stable variation in receptor density or context-dependent dopamine release. We present evidence uniquely consistent with the former interpretation, providing clarity to the nature of this brain-behavior relationship.

Counterintuitive effects of negative social feedback on attention.

Which stimuli we pay attention to is strongly influenced by learning. Stimuli previously associated with reward outcomes, such as money and food, and stimuli previously associated with aversive outcomes, such as monetary loss and electric shock, automatically capture attention. Social reward (happy expressions) can bias attention towards associated stimuli, but the role of negative social feedback in biasing attentional selection remains unexplored. On the one hand, negative social feedback often serves to discourage particular behaviours. If attentional selection can be curbed much like any other behavioural preference, we might expect stimuli associated with negative social feedback to be more readily ignored. On the other hand, if negative social feedback influences attention in the same way that other aversive outcomes do, such feedback might ironically bias attention towards the stimuli it is intended to discourage selection of. In the present study, participants first completed a training phase in which colour targets were associated with negative social feedback. Then, in a subsequent test phase, these same colour stimuli served as task-irrelevant distractors during a visual search task. The results strongly support the latter interpretation in that stimuli previously associated with negative social feedback impaired search performance.

Reward, attention, and HIV-related risk in HIV+ individuals.

Human immunodeficiency virus (HIV) is often contracted through engaging in risky reward-motivated behaviors such as needle sharing and unprotected sex. Understanding the factors that make an individual more vulnerable to succumbing to the temptation to engage in these risky behaviors is important to limiting the spread of HIV. One potential source of this vulnerability concerns the degree to which an individual is able to resist paying attention to irrelevant reward information. In the present study, we examine this possible link by characterizing individual differences in value-based attentional bias in a sample of HIV+ individuals with varying histories of risk-taking behavior. Participants learned associations between experimental stimuli and monetary reward outcome. The degree of attentional bias for these reward-associated stimuli, reflected in their ability to capture attention when presented as task-irrelevant distractors, was then assessed both immediately and six months following reward learning. Value-driven attentional capture was related to substance abuse history and non-planning impulsiveness during the time leading up to contraction of HIV as measured via self-report. These findings suggest a link between the ability to ignore reward-associated information and prior HIV-related risk-taking behavior. Additionally, particular aspects of HIV-associated neurocognitive disorders were related to attentional bias, including motor deficits commonly associated with HIV-induced damage to the basal ganglia.

The attribution of value-based attentional priority in individuals with depressive symptoms.

The capture of attention by stimuli previously associated with reward has been demonstrated across a wide range of studies. Such value-based attentional priority appears to be robust, and cases where reward feedback fails to modulate subsequent attention have not been reported. However, individuals differ in their sensitivity to external rewards, and such sensitivity is abnormally blunted in depression. Here, we show that depressive symptomology is accompanied by insensitivity to value-based attentional bias. We replicate attentional capture by stimuli previously associated with reward in a control sample and show that these same reward-related stimuli do not capture attention in individuals experiencing symptoms of depression. This sharp contrast in performance indicates that value-based attentional biases depend on the normal functioning of the brain's reward system and suggests that a failure to preferentially attend to reward-related information may play a role in the experience of depression.