Clayton Hickey

Reward Changes Salience in Human Vision via the Anterior Cingulate

Reward-related mesolimbic dopamine steers animal behavior, creating automatic approach toward reward-associated objects and avoidance of objects unlikely to be beneficial. Theories of dopamine suggest that this reflects underlying biases in perception and attention, with reward enhancing the representation of reward-associated stimuli such that attention is more likely to be deployed to the location of these objects. Using measures of behavior and brain electricity in male and female humans, we demonstrate this to be the case. Sensory and perceptual processing of reward-associated visual features is facilitated such that attention is deployed to objects characterized by these features in subsequent experimental trials. This is the case even when participants know that a strategic decision to attend to reward-associated features will be counterproductive and result in suboptimal performance. Other results show that the magnitude of visual bias created by reward is predicted by the response to reward feedback in anterior cingulate cortex, an area with strong connections to dopaminergic structures in the midbrain. These results demonstrate that reward has an impact on vision that is independent of its role in the strategic establishment of endogenous attention. We suggest that reward acts to change visual salience and thus plays an important and undervalued role in attentional control.

Electrophysiological Evidence of the Capture of Visual Attention

We investigated the ability of salient yet task-irrelevant stimuli to capture attention in two visual search experiments. Participants were presented with circular search arrays that contained a highly salient distractor singleton defined by color and a less salient target singleton defined by form. A component of the event-related potential called the N2pc was used to track the allocation of attention to lateralized positions in the arrays. In Experiment 1, a lateralized distractor elicited an N2pc when a concurrent target was presented on the vertical meridian and thus could not elicit lateralized components such as the N2pc. A similar distractor-elicited N2pc was found in Experiment 2, which was conducted to rule out certain voluntary search strategies. Additionally, in Experiment 2 both the distractor and the target elicited the N2pc component when the two stimuli were presented on opposite sides of the search array. Critically, the distractor-elicited N2pc preceded the target-elicited N2pc on these trials. These results demonstrate that participants shifted attention to the target only after shifting attention to the more salient but task-irrelevant distractor. This pattern of results is in line with theories of attention in which stimulus-driven control plays an integral role.

Electrophysiological indices of target and distractor processing in visual search

Attentional selection of a target presented among distractors can be indexed with an event-related potential (ERP) component known as the N2pc. Theoretical interpretation of the N2pc has suggested that it reflects a fundamental mechanism of attention that shelters the cortical representation of targets by suppressing neural activity stemming from distractors. Results from fields other than human electrophysiology, however, suggest that attention does not act solely through distractor suppression; rather, it modulates the processing of both target and distractors. We conducted four ERP experiments designed to investigate whether the N2pc reflects multiple attentional mechanisms. Our goal was to reconcile ostensibly conflicting outcomes obtained in electrophysiological studies of attention with those obtained using other methodologies. Participants viewed visual search arrays containing one target and one distractor. In Experiments 1 through 3, the distractor was isoluminant with the background, and therefore, did not elicit early lateralized ERP activity. This work revealed a novel contralateral ERP component that appears to reflect direct suppression of the cortical representation of the distractor. We accordingly name this component the distractor positivity (PD). In Experiment 4, an ERP component associated with target processing was additionally isolated. We refer to this component as the target negativity (NT). We believe that the N2pc reflects the summation of the PD and NT, and that these discrete components may have been confounded in earlier electrophysiological studies. Overall, this study demonstrates that attention acts on both target and distractor representations, and that this can be indexed in the visual ERP.

REDUCED ATTENTIONAL CAPTURE IN ACTION VIDEO GAME PLAYERS

Recent studies indicate that playing action video games improves performance on a number of attention-based tasks. However, it remains unclear whether action video game experience primarily affects endogenous or exogenous forms of spatial orienting. To examine this issue, action video game players and non-action video game players performed an attentional capture task. The results show that action video game players responded quicker than non-action video game players, both when a target appeared in isolation and when a salient, task-irrelevant distractor was present in the display. Action video game players additionally showed a smaller capture effect than did non-action video game players. When coupled with the findings of previous studies, the collective evidence indicates that extensive experience with action video games may enhance players’ top-down attentional control, which, in turn, can modulate the negative effects of bottom-up attentional capture.

Reward Guides Vision when It's Your Thing: Trait Reward-Seeking in Reward-Mediated Visual Priming

Reward-related mesolimbic dopamine is thought to play an important role in guiding animal behaviour, biasing approach towards potentially beneficial environmental stimuli and away from objects unlikely to garner positive outcome. This is considered to result in part from an impact on perceptual and attentional processes: dopamine initiates a series of cognitive events that result in the priming of reward-associated perceptual features. We have provided behavioural and electrophysiological evidence that this mechanism guides human vision in search, an effect we refer to as reward priming. We have also demonstrated that there is substantial individual variability in this effect. Here we show that behavioural differences in reward priming are predicted remarkably well by a personality index that captures the degree to which a persons behaviour is driven by reward outcome. Participants with reward-seeking personalities are found to be those who allocate visual resources to objects characterized by reward-associated visual features. These results add to a rapidly developing literature demonstrating the crucial role reward plays in attentional control. They additionally illustrate the striking impact personality traits can have on low-level cognitive processes like perception and selective attention.

Reward creates oculomotor salience

Summary Theories of animal approach behaviour suggest that reward can create low-level biases in perceptual and motor systems, potentiating the processing of reward-associated environmental stimuli and causing animals to instinctively orient the head and eyes toward these objects [1]. However, the idea that reward can have this kind of direct impact on subsequent oculomotor processing has never been robustly tested, and existing research has largely confounded low-level effects with those mediated by strategy and attentional-set [2]. Here we demonstrate in humans that saccade trajectories are disrupted by a reward-associated distractor even when participants expect this object, know where it may appear, and do their best to ignore it. The reward history of a visual object thus has a direct, low-level, and non-strategic influence on how we deploy our eyes.

Early multisensory interactions affect the competition among multiple visual objects

In dynamic cluttered environments, audition and vision may benefit from each other in determining what deserves further attention and what does not. We investigated the underlying neural mechanisms responsible for attentional guidance by audiovisual stimuli in such an environment. Event-related potentials (ERPs) were measured during visual search through dynamic displays consisting of line elements that randomly changed orientation. Search accuracy improved when a target orientation change was synchronized with an auditory signal as compared to when the auditory signal was absent or synchronized with a distractor orientation change. The ERP data show that behavioral benefits were related to an early multisensory interaction over left parieto-occipital cortex (50-60 ms post-stimulus onset), which was followed by an early positive modulation (80-100 ms) over occipital and temporal areas contralateral to the audiovisual event, an enhanced N2pc (210-250 ms), and a contralateral negative slow wave (CNSW). The early multisensory interaction was correlated with behavioral search benefits, indicating that participants with a strong multisensory interaction benefited the most from the synchronized auditory signal. We suggest that an auditory signal enhances the neural response to a synchronized visual event, which increases the chances of selection in a multiple object environment.

Reward has a residual impact on target selection in visual search, but not on the suppression of distractors

In the reinforcement learning literature, good outcome following selection of a visual object is thought to bias perception and attention in favour of similar objects in later experience. This impact of reward might be instantiated in two ways: Reward could prime target features or it could act to facilitate suppression of distractors present when reward was received. Here we report results from an experiment in which reward outcome was selectively associated either with the colour defining a visual search target or with the colour defining a salient distractor in the display. Rewards impact on search was evident only when it was tied to the target; reward made it no easier to ignore a distractor when it subsequently reappeared as a distractor. This suggests that reward acts largely to prime target representations, consistent with the idea that objects associated with good outcome become visually salient.

Neural Mechanisms of Incentive Salience in Naturalistic Human Vision

What role does reward play in real-world human vision? Reward coding in the midbrain is thought to cause the rapid prioritization of reward-associated visual stimuli. However, existing evidence for this incentive salience hypothesis in vision is equivocal, particularly in naturalistic circumstances, and little is known about underlying neural systems. Here we use human fMRI to test whether reward primes perceptual encoding of naturalistic visual stimuli and to identify the neural mechanisms underlying this function. Participants detected a cued object category in briefly presented images of city- and landscapes. Using multivoxel pattern analysis in visual cortex, we found that the encoding of reward-associated targets was enhanced, whereas encoding of reward-associated distractors was suppressed, with the strength of this effect predicted by activity in the dopaminergic midbrain and a connected cortical network. These results identify a novel interaction between neural systems responsible for reward processing and visual perception in the human brain.

The time course of exogenous and endogenous control of covert attention

Studies of eye-movements and manual response have established that rapid overt selection is largely exogenously driven toward salient stimuli, whereas slower selection is largely endogenously driven to relevant objects. We use the N2pc, an event-related potential index of covert attention, to demonstrate that this time course reflects an underlying pattern in the deployment of covert attention. We find that shifts of attention that occur soon after the onset of a visual search array are directed toward salient, task-irrelevant visual stimuli and are associated with slow responses to the target. In contrast, slower shifts are target-directed and are associated with fast responses. The time course of exogenous and endogenous control provides a framework in which some inconsistent results in the capture literature might be reconciled; capture may occur when attention is rapidly deployed.