Leonardo Chelazzi

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.

Associative knowledge controls deployment of visual selective attention

According to some models of visual selective attention, objects in a scene activate corresponding neural representations, which compete for perceptual awareness and motor behavior. During a visual search for a target object, top-down control exerted by working memory representations of the targets defining properties resolves competition in favor of the target. These models, however, ignore the existence of associative links among object representations. Here we show that such associations can strongly influence deployment of attention in humans. In the context of visual search, objects associated with the target were both recalled more often and recognized more accurately than unrelated distractors. Notably, both target and associated objects competitively weakened recognition of unrelated distractors and slowed responses to a luminance probe. Moreover, in a speeded search protocol, associated objects rendered search both slower and less accurate. Finally, the first saccades after onset of the stimulus array were more often directed toward associated than control items.

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.

Distribution in the visual field of the costs of voluntarily allocated attention and of the inhibitory after-effects of covert orienting

By using a simple reaction time (RT) paradigm we have investigated the spatial distribution of the benefits and costs of voluntarily directed attention and of the inhibitory after-effects of covert orienting. In the first experiment subjects deliberately allocated attention to each one of five stimulus positions disposed along the horizontal meridian, while at the same time fixing their eyes on the central position. The separation in visual angle between the central position and the two nearest positions, one on the left and the other on the right, was 10 degrees; that between the central position and the two most eccentric positions was 30 degrees. By comparing RT to brief flashes of light presented at each position during directed attention with RT to identical flashes at the same position during diffuse attention (i.e. in a condition in which subjects paid equal attention to all five positions), it was possible to determine that benefits, that is RT decreases relative to the diffuse-attention condition, were strictly limited to the attended position. Costs, i.e. RT increases relative to the diffuse-attention condition, showed a more diffuse and complex spatial pattern. When attention was directed to one of the noncentral positions, costs were apparent at the two contralateral positions and at the central position, but not at the ipsilateral position. When attention was directed to the central position, costs occurred at all other positions. This suggests a special role for the vertical meridian in delimiting the area of costs when one covertly orients towards the opposite right or left visual half field. Work of others and our preliminary evidence indicate that the area of costs is similarly limited by the horizontal meridian when one orients toward the opposite upper or lower visual field. In the second experiment we studied the inhibitory after-effect of covert orienting. Orienting to a light stimulus without moving the eyes to it may induce a short-lived facilitation of the speed of response to a second stimulus presented at the same position, but this facilitation is followed by a profound and prolonged RT retardation. By using a two-flashes paradigm we observed this RT retardation not only when the two stimuli appeared at the same position, but also when they occurred at different locations in the same altitudinal or lateral visual hemifield. There were no inhibitory after-effects when the two stimuli appeared on opposite sides of the vertical or horizontal meridian.(ABSTRACT TRUNCATED AT 400 WORDS)

My eyes want to look where your eyes are looking: exploring the tendency to imitate another individual's gaze.

In this study we investigated the tendency of humans to imitate the gaze direction of other individuals. Distracting gaze stimuli or non biological directional cues (arrows) were presented to observers performing an instructed saccadic eye movement task. Eye movement recordings showed that observers performed less accurately when the distracting gaze and the instructed saccade had opposite directions, with a substantial number of saccades matching the direction of the distracting gaze. Static (Experiment 1) and dynamic (Experiment 2) gaze distracters, but not pointing arrows (Experiment 3), produced the effect. Results show a strong predisposition of humans to imitate somebody elses oculomotor behaviour, even when detrimental to task performance. This is likely linked to a strong tendency to share attentional states of other individuals, known as joint attention.

Do peripheral non-informative cues induce early facilitation of target detection ?

It has been reported that simple reaction time (RT) to a peripheral visual target is faster if the target is presented within about 200 msec from the onset of a non-informative cue flashed at the same location, as compared with RT to a target presented at an uncued location. This period of facilitation is followed by a period of inhibition during which RT is longer if cue and target are shown at the same location or at different locations within the same hemifield, as opposed to contralateral cues and targets. Early facilitation has been explained by an automatic covert orienting towards the cue, while the following inhibition has been regarded as a consequence of such covert orienting. In a series of four experiments, we have investigated the dependency of these effects on the temporal and spatial relationships between cue and target. Normal, right-handed subjects responded to a target displayed for 16 msec simultaneously with, or following at stimulus-onset asynchronies (SOAs) of 60, 130, 300 or 900 msec, the onset of a non-informative cue. Both cues and targets could appear at random in one of four locations (Expts 1-3) or in one of two locations (Expt 4) disposed symmetrically across the fixation point along the horizontal meridian. Duration of the cue varied between experiments. In Expt 1 it was 16 msec. In Expt 2 the cue remained on view throughout the period of the SOA and terminated 300 msec after target onset. In the remaining two experiments cue duration was 130 msec. In the first experiment, at all cue-target SOAs RTs to target flashed either at the same location or in the same hemifield as the cue were significantly slower than RTs to contralateral cue-target combinations (RT inhibition). In the other experiments, there was no RT inhibition with targets in cued locations if the cue remained on during target presentation and outlasted target offset. Since at no SOA was RT to targets in cued locations shorter than RT to targets contralateral to cues, there was no direct evidence for facilitation. However, the facilitatory influence of these cues could be inferred from the fact that they countered and masked inhibition. RT to uncued targets ipsilateral to cues was consistently inhibited in all experimental conditions. These results show that at each cue-target SOA the consequences of a peripheral non-informative cue depend on whether or not the cue remains visible during target processing.(ABSTRACT TRUNCATED AT 400 WORDS)

Toward a Unified Theory of Visual Area V4

Visual area V4 is a midtier cortical area in the ventral visual pathway. It is crucial for visual object recognition and has been a focus of many studies on visual attention. However, there is no unifying view of V4s role in visual processing. Neither is there an understanding of how its role in feature processing interfaces with its role in visual attention. This review captures our current knowledge of V4, largely derived from electrophysiological and imaging studies in the macaque monkey. Based on recent discovery of functionally specific domains in V4, we propose that the unifying function of V4 circuitry is to enable selective extraction of specific functional domain-based networks, whether it be by bottom-up specification of object features or by top-down attentionally driven selection.

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.

Volitional Covert Orienting to a Peripheral Cue Does Not Suppress Cue-induced Inhibition of Return

Detection reaction time (RT) at an extrafoveal location can be increased by noninformative precues presented at that location or ipsilaterally to it. This cue-induced inhibition is called inhibition of return or ipsilateral inhibition. We measured detection RT to simple light targets at extrafoveal locations that could be designated for covert orienting by local or distant cues. We found that cue-induced inhibition co-occurred in an additive fashion with the direct effects of covert orienting, i.e., it detracted from facilitation at attended locations and increased the disadvantage for unattended locations. Thus, cue-induced inhibition cannot be suppressed by a volitional covert orienting to the cued location; the cooccurrence of different facilitatory and inhibitory effects confirms the simultaneous operation of multiple independent, attentional mechanisms during covert orienting.