Visual fixation patterns during economic choice reflect covert valuation processes that emerge with learning

Abstract

Visual fixations play a vital role in decision making. Recent studies have demonstrated that the longer subjects fixate an option, the more likely they are to choose it. However, the role of evaluating stimuli covertly (i.e., without fixating them), and how covert evaluations determine where to subsequently fixate, remains relatively unexplored. Here, we trained monkeys to perform a decision-making task where they made binary choices between reward-predictive stimuli which were well-learned (“overtrained”), recently learned (“novel”), or a combination of both (“mixed”). Subjects were free to saccade around the screen and make a choice (via joystick response) at any time. Subjects rarely fixated both options, yet choice behavior was better explained by assuming the values of both stimuli governed choices. The first fixation latency was fast (∼150 ms) but, surprisingly, its direction was value-driven. This suggests covert evaluation of stimulus values prior to first saccade. This was particularly evident for overtrained stimuli. For novel stimuli, first fixations became increasingly value-driven throughout a behavioral session. However, this improvement lagged behind learning of accurate economic choices, suggesting separate processes governed their learning. Finally, mixed trials revealed a strong bias toward fixating the novel stimulus first but no bias toward choosing it. Our results suggest that the primate brain contains fast covert evaluation mechanisms for guiding fixations toward highly valuable and novel information. By employing such covert mechanisms, fixation behavior becomes dissociable from the value comparison processes that drive final choice. This implies that primates use separable decision systems for value-guided fixations and value-guided choice.