Saccades are rapid eye movements through which foveate animals examine visual scenes. Converging evidence from humans and monkeys show that a key role of saccades is to samplie visual information to guide subsequent actions. Consistent with these behavioral observations, neurons throughout the monkey visual system respond selectively for task-relevant stimuli relative to distractors, and this enhancement is thought to arise in part from two interconnected areas, the lateral intraparietal area (LIP) and th frontal eye field (FEF). However, we have little understanding about how this selection is made: what are the computations by which FEF and LIP neurons identify relevant items? Here we examine a dual-control hypothesis that is suggested by computational modeling of natural behavior and states that top-down gaze control is based on two interacting factors: the gains in reward and gains in information that a saccade is expected to bring. We use a novel two- step task where monkeys make two saccades on each trial - a first saccade to sample visual information and a second saccade to report a decision based on that information. We manipulate the reward and informational demands (uncertainty) of the final decision, and examine how this affects target selection for the first, information sampling action. Using this paradigm we obtained preliminary evidence that supports the dual control hypothesis and shows that (1) target selective responses in LIP show a strong modulation by both reward and uncertainty (or equivalently, expected information gains), and (2) reversible inactivation of this area impairs target selection based on cue validity (expected information gains) but not simple reward associations. We propose to extend these findings to systematically explore how reward and information gains modulate saccade selection responses in FEF and LIP (Aim 1), how the two factors modulate responses related to covert selection (Aim 2), and how reversible inactivation of each area impacts reward and information-based selection (Aim 3). These studies are highly significant and innovative for oculomotor research because they (1) provide new and much needed empirical evidence to support computational modeling of top-down gaze control, (2) clarify functional distinctions between FEF and LIP, which so far appear to perform very similar functions, (3) clarify how oculomotor decisions depend on information gains in addition to primary rewards, thereby resolving longstanding confounds between reward and attention and linking neural studies with studies of natural gaze control. The studies are also significant and innovative on a broader scope because they are among the first to investigate the relation between attention and decision making and to probe the neural basis of decisions based on the value of information. Thus, the studies are expected to have a strong impact on our understanding of attention and decision making, two core cognitive functions that are critical in complex behaviors and psychiatric diseases including attention deficit disorder, drug addiction, anxiety and depression. 1

Public Health Relevance

Decision making is believed to involve the gradual accumulation of evidence followed by a commitment to a course of action. However it remains unknown how animals actively sample information to guide a given action. Here, we address this question using single neuron recordings in conjunction with reversible inactivation in monkeys. We focus on frontal and parietal mechanisms of oculomotor control, and examine how information sampling is guided by the uncertainty and rewards of subsequent actions. 1

National Institute of Health (NIH)
National Eye Institute (NEI)
Research Project (R01)
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Special Emphasis Panel (ZRG1)
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Flanders, Martha C
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Columbia University (N.Y.)
Schools of Medicine
New York
United States
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