Competition for Visual Selection in the Oculomotor System

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Many decisions we make require visually identifying and evaluating numerous alternatives quickly. These usually vary in reward, or value, and in low-level visual properties, such as saliency. Both saliency and value influence the final decision. In particular, saliency affects fixation locations and durations, which are predictive of choices. However, it is unknown how saliency propagates to the final decision. Moreover, the relative influence of saliency and value is unclear. Here we address these questions with an integrated model that combines a perceptual decision process about where and when to look with an economic decision process about what to choose. The perceptual decision process is modeled as a driftdiffusion model (DDM) process for each alternative. Using psychophysical data from a multiple-alternative, forced-choice task, in which subjects have to pick one food item from a crowded display via eye movements, we test four models where each DDM process is driven by (i) saliency or (ii) value alone or (iii) an additive or (iv) a multiplicative combination of both. We find that models including both saliency and value weighted in a one-third to two-thirds ratio (saliency-to-value) significantly outperform models based on either quantity alone. These eye fixation patterns modulate an economic decision process, also described as a DDM process driven by value. Our combined model quantitatively explains fixation patterns and choices with similar or better accuracy than previous models, suggesting that visual saliency has a smaller, but significant, influence than value and that saliency affects choices indirectly through perceptual decisions that modulate economic decisions.search | multiple targets | eye tracking | preference | attention O ne important goal of neuroscience and economics is to understand the computational mechanisms that underlie decision making between multiple alternatives. Interestingly, this goal has proceeded along two seemingly parallel paths that consider either perceptual decision making, namely decisions about perceptual properties of alternatives, or economic decision making, which considers the value of alternatives (1). Although these types of decisions can be constructed to be mutually exclusive in the laboratory, in more natural contexts, decisions nearly always involve perceptual decisions about how to sample information and value-based decisions about which alternatives are more valuable. Importantly, however, very little attention has been paid to how perceptual and economic decision processes may interact. One recent paper reported a visual saliency bias where, independent of consumer preferences, visually salient options are more likely to be chosen than less salient alternatives. It is not clear, however, which mechanism gives rise to this effect or how perceptual processes interact with economic choices (2).Choices and reaction times during perceptual decision making have been accurately modeled by stochastic accumulator models such as the drift-diffusion model (DDM) (3...

Section: Discussionmentioning

confidence: 99%

Simultaneous modeling of visual saliency and value computation improves predictions of economic choice

Towal¹,

Mormann

Koch

2013

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245

“…However, because the results for saccadic choices and for manual reactions were the same, it is likely that the results of these experiments depend mostly on the final state of the integration process. Markowitz et al (16) did measure the time course of how value and salience information compete for visual selection. Monkey observers had to choose between two targets that were defined by congruent or incongruent salience and reward information.…”

Section: Discussionmentioning

confidence: 99%

“…The results of these experiments indicate that value can be an important determinant of the neural activity underlying the selection of a saccadic target when one object bears a higher reward than another (12)(13)(14)(15)(16). In these studies, a monkey observer typically selects between two or more spatially and visually distinct response alternatives that are associated with different rewards.…”

mentioning

confidence: 97%

Dynamic integration of information about salience and value for saccadic eye movements

Schütz

Trommershäuser

Gegenfurtner

2012

131

117

Humans shift their gaze to a new location several times per second. It is still unclear what determines where they look next. Fixation behavior is influenced by the low-level salience of the visual stimulus, such as luminance, contrast, and color, but also by highlevel task demands and prior knowledge. Under natural conditions, different sources of information might conflict with each other and have to be combined. In our paradigm, we trade off visual salience against expected value. We show that both salience and value information influence the saccadic end point within an object, but with different time courses. The relative weights of salience and value are not constant but vary from eye movement to eye movement, depending critically on the availability of the value information at the time when the saccade is programmed. Shortlatency saccades are determined mainly by salience, but value information is taken into account for long-latency saccades. We present a model that describes these data by dynamically weighting and integrating detailed topographic maps of visual salience and value. These results support the notion of independent neural pathways for the processing of visual information and value.neuroeconomics | decision-making | cue combination | visual perception B ecause of foveal specialization for high acuity and color vision, humans frequently move their eyes to project different parts of the visual scene on the fovea. Although the basic networks for the programming and execution of saccades have been studied for decades (1, 2), surprisingly little is known about the neural processes that underlie selection of the point of fixation of the next saccade. To some degree, the weighted combination of basic visual-stimulus features can predict saccadic eye movements in natural scenes (3-5). These basic stimulus features are, among others, local differences in luminance, color, or orientation and are combined by the visual system in a bottom-up image-based salience map. However, the salience difference between fixated and nonfixated image locations is typically rather small (6, 7), indicating that the influence of salience may be modulated by other factors. Visual salience, by definition, is determined by features of the visual scene alone and therefore is determined exclusively by visual bottom-up processing. Other factors reflect the influence of top-down processing. Task demands, for example, exhibit constraints on gaze patterns in different activities such as visual searching (8), manipulating an object (9), playing ball sports, preparing a cup of tea (10), and navigating between obstacles (11). In all these examples, gaze is concentrated on objects that are relevant for the task.Along different lines, recent research in neuroeconomics has used saccadic eye movements as a tool to uncover the neural bases of primate choice behavior. The results of these experiments indicate that value can be an important determinant of the neural activity underlying the selection of a saccadic target when one object bear...

“…Saccadic target selection is determined in part by the reward value of potential targets (1)(2)(3). Given the clear role of the FEF in target selection, it is surprising that few studies have explored the contribution of FEF dopamine to this behavior.…”

Section: Discussionmentioning

confidence: 99%

Dissociable dopaminergic control of saccadic target selection and its implications for reward modulation

Soltani

Noudoost

Moore

2013

To investigate mechanisms by which reward modulates target selection, we studied the behavioral effects of perturbing dopaminergic activity within the frontal eye field (FEF) of monkeys performing a saccadic choice task and simulated the effects using a plausible cortical network. We found that manipulation of FEF activity either by blocking D1 receptors (D1Rs) or by stimulating D2 receptors (D2Rs) increased the tendency to choose targets in the response field of the affected site. However, the D1R manipulation decreased the tendency to repeat choices on subsequent trials, whereas the D2R manipulation increased that tendency. Moreover, the amount of shift in target selection resulting from the two manipulations correlated in opposite ways with the baseline stochasticity of choice behavior. Our network simulation results suggest that D1Rs influence target selection mainly through their effects on the strength of inputs to the FEF and on recurrent connectivity, whereas D2Rs influence the excitability of FEF output neurons. Altogether, these results reveal dissociable dopaminergic mechanisms influencing target selection and suggest how reward can influence adaptive choice behavior via prefrontal dopamine.computational modeling | decision making | oculomotor A s the primary means of exploring the visual environment, we shift our gaze several times each second via saccadic eye movements. Where we look depends not only on the physical salience of visual stimuli, but also on their reward value (1-3). For example, while shopping, your attention may be captured differently by colored sales tags upon realizing that they indicate different discounts (e.g., yellow tags for 20% vs. red tags for 40% off). Studies of value-based behavior have established that midbrain dopamine (DA) neurons signal different aspects of reward (4) and that neurons in many cortical structures receiving dopaminergic projections represent the reward value of visual stimuli (5). The frontal eye field (FEF), the area of prefrontal cortex (PFC) most directly involved in triggering saccadic eye movements, receives inputs from structures encoding reward value (6), and these inputs might be sufficient to control value-based, saccadic choice (target selection). It is also possible that this control operates via FEF projections to caudate in the basal ganglia, where DA-mediated plasticity modulates rewarddependent target selection (7). In addition, the direct dopaminergic inputs to the FEF (8) could provide a mechanism that independently modulates target selection based on reward signals. Determining how dopamine within the FEF influences saccades is thus important for understanding the mechanism by which reward modulates the selection of visual targets for eye movements.To address these questions, we manipulated dopaminergic activity within the FEF of monkeys performing a saccadic choice task. In the task, monkeys freely selected between two identical visual targets appearing at varying temporal asynchronies. By systematically altering the target onset asy...