Chiara Della Libera

Visual Selective Attention and the Effects of Monetary Rewards

Outcomes of actions, in the form of rewards and punishments, are known to shape behavior. For example, an action followed by reward will be more readily elicited on subsequent encounters with the same stimuli and context—a phenomenon known as the law of effect. These consequences of rewards (and punishments) are important because they reinforce adaptive behaviors at the expense of competing ones, thus increasing fitness of the organism in its environment. However, it is unknown whether similar influences regulate covert mental processes, such as visual selective attention. Visual selective attention allows privileged processing of task-relevant information, while inhibiting distracting contextual elements. Using variable monetary rewards as arbitrary feedback on performance, we tested whether acts of attentional selection, and in particular the resulting aftereffects, can be modulated by their consequences. Results show that the efficacy of visual selective attention can be sensibly adjusted by external feedback. Specifically, although lingering inhibition of distractors is robust after highly rewarded selections, it is eliminated after poorly rewarded selections. This powerful feature of visual selective attention provides attentive processes with both flexibility and self-regulation properties.

Learning to Attend and to Ignore Is a Matter of Gains and Losses

Efficient goal-directed behavior in a crowded world is crucially mediated by visual selective attention (VSA), which regulates deployment of cognitive resources toward selected, behaviorally relevant visual objects. Acting as a filter on perceptual representations, VSA allows preferential processing of relevant objects and concurrently inhibits traces of irrelevant items, thus preventing harmful distraction. Recent evidence showed that monetary rewards for performance on VSA tasks strongly affect immediately subsequent deployment of attention; a typical aftereffect of VSA (negative priming) was found only following highly rewarded selections. Here we report a much more striking demonstration that the controlled delivery of monetary rewards also affects attentional processing several days later. Thus, the propensity to select or to ignore specific visual objects appears to be strongly biased by the more or less rewarding consequences of past attentional encounters with the same objects.

Altering Spatial Priority Maps via Reward-Based Learning

Spatial priority maps are real-time representations of the behavioral salience of locations in the visual field, resulting from the combined influence of stimulus driven activity and top-down signals related to the current goals of the individual. They arbitrate which of a number of (potential) targets in the visual scene will win the competition for attentional resources. As a result, deployment of visual attention to a specific spatial location is determined by the current peak of activation (corresponding to the highest behavioral salience) across the map. Here we report a behavioral study performed on healthy human volunteers, where we demonstrate that spatial priority maps can be shaped via reward-based learning, reflecting long-lasting alterations (biases) in the behavioral salience of specific spatial locations. These biases exert an especially strong influence on performance under conditions where multiple potential targets compete for selection, conferring competitive advantage to targets presented in spatial locations associated with greater reward during learning relative to targets presented in locations associated with lesser reward. Such acquired biases of spatial attention are persistent, are nonstrategic in nature, and generalize across stimuli and task contexts. These results suggest that reward-based attentional learning can induce plastic changes in spatial priority maps, endowing these representations with the “intelligent” capacity to learn from experience.

Dissociable Effects of Reward on Attentional Learning: From Passive Associations to Active Monitoring

Visual selective attention (VSA) is the cognitive function that regulates ongoing processing of retinal input in order for selected representations to gain privileged access to perceptual awareness and guide behavior, facilitating analysis of currently relevant information while suppressing the less relevant input. Recent findings indicate that the deployment of VSA is shaped according to past outcomes. Targets whose selection has led to rewarding outcomes become relatively easier to select in the future, and distracters that have been ignored with higher gains are more easily discarded. Although outcomes (monetary rewards) were completely predetermined in our prior studies, participants were told that higher rewards would follow more efficient responses. In a new experiment we have eliminated the illusory link between performance and outcomes by informing subjects that rewards were randomly assigned. This trivial yet crucial manipulation led to strikingly different results. Items that were associated more frequently with higher gains became more difficult to ignore, regardless of the role (target or distracter) they played when differential rewards were delivered. Therefore, VSA is shaped by two distinct reward-related learning mechanisms: one requiring active monitoring of performance and outcome, and a second one detecting the sheer association between objects in the environment (whether attended or ignored) and the more-or-less rewarding events that accompany them.

Neural basis of visual selective attention

Attentional modulation along the object-recognition pathway of the cortical visual system of primates has been shown to consist of enhanced representation of the retinal input at a specific location in space, or of objects located anywhere in the visual field which possess a critical object feature. Moreover, selective attention mechanisms allow the visual system to resolve competition among multiple objects in a crowded scene in favor of the object that is relevant for the current behavior. Finally, selective attention affects the spontaneous activity of neurons as well as their visually driven responses, and it does so not only by modulating the spiking activity of individual neurons, but also by modulating the degree of coherent firing within the critical neuronal populations. WIREs Cogni Sci 2011 2 392-407 DOI: 10.1002/wcs.117 For further resources related to this article, please visit the WIREs website.

Biases of attention in chronic smokers: Men and women are not alike

The activation of motivational systems by stimuli in the environment that are associated with rewarding experiences is able to trigger plastic changes in the brain, thereby altering the attentional priority of those stimuli. As a result, attentional deployment is often abnormal in addiction, with drug-related stimuli attracting attention automatically and gaining control over behavior. For example, smokers show attentional biases toward smoke-related cues, but the mechanisms underlying these effects and the nature of their link to addiction are still debated. Here, we investigated the influence of gender and individual factors on the temporal dynamics of attentional deployment toward smoke-related stimuli in young smokers. Crucially, we found a striking gender difference, with only males exhibiting a typical attentional bias for smoke-related items, and the bias revealed strong time dependency. Additionally, for both males and females, various personality traits and smoking habits predicted the direction and strength of the measured bias. Overall, these results unveil a crucial influence of several predictors—notably, gender—on the biases of attention toward smoke-related items in chronic smokers.

Reward-based plasticity of spatial priority maps: Exploiting inter-subject variability to probe the underlying neurobiology

ABSTRACT Recent evidence indicates that the attentional priority of objects and locations is altered by the controlled delivery of reward, reflecting reward-based attentional learning. Here, we take an approach hinging on intersubject variability to probe the neurobiological bases of the reward-driven plasticity of spatial priority maps. Specifically, we ask whether an individual’s susceptibility to the reward-based treatment can be accounted for by specific predictors, notably personality traits that are linked to reward processing (along with more general personality traits), but also gender. Using a visual search protocol, we show that when different target locations are associated with unequal reward probability, different priorities are acquired by the more rewarded relative to the less rewarded locations. However, while males exhibit the expected pattern of results, with greater priority for locations associated with higher reward, females show an opposite trend. Critically, both the extent and the direction of reward-based adjustments are further predicted by personality traits indexing reward sensitivity, indicating that not only male and female brains are differentially sensitive to reward, but also that specific personality traits further contribute to shaping their learning-dependent attentional plasticity. These results contribute to a better understanding of the neurobiology underlying reward-dependent attentional learning and cross-subject variability in this domain.

Augmenting distractor filtering via transcranial magnetic stimulation of the lateral occipital cortex.

Visual selective attention (VSA) optimizes perception and behavioral control by enabling efficient selection of relevant information and filtering of distractors. While focusing resources on task-relevant information helps counteract distraction, dedicated filtering mechanisms have recently been demonstrated, allowing neural systems to implement suitable policies for the suppression of potential interference. Limited evidence is presently available concerning the neural underpinnings of these mechanisms, and whether neural circuitry within the visual cortex might play a causal role in their instantiation, a possibility that we directly tested here. In two related experiments, transcranial magnetic stimulation (TMS) was applied over the lateral occipital cortex of healthy humans at different times during the execution of a behavioral task which entailed varying levels of distractor interference and need for attentional engagement. While earlier TMS boosted target selection, stimulation within a restricted time epoch close to (and in the course of) stimulus presentation engendered selective enhancement of distractor suppression, by affecting the ongoing, reactive instantiation of attentional filtering mechanisms required by specific task conditions. The results attest to a causal role of mid-tier ventral visual areas in distractor filtering and offer insights into the mechanisms through which TMS may have affected ongoing neural activity in the stimulated tissue.