Frontal eye field neurons selectively signal the reward value of prior actions.

Abstract

The consequences of individual actions are typically unknown until well after they are executed. This fact necessitates a mechanism that bridges delays between specific actions and reward outcomes. We looked for the presence of such a mechanism in the post-movement activity of neurons in the frontal eye field (FEF), a visuomotor area in prefrontal cortex. Monkeys performed an oculomotor gamble task in which they made eye movements to different locations associated with dynamically varying reward outcomes. Behavioral data showed that monkeys tracked reward history and made choices according to their own risk preferences. Consistent with previous studies, we observed that the activity of FEF neurons is correlated with the expected reward value of different eye movements before a target appears. Moreover, we observed that the activity of FEF neurons continued to signal the direction of eye movements, the expected reward value, and their interaction well after the movements were completed and when targets were no longer within the neuronal response field. In addition, this post-movement information was also observed in local field potentials, particularly in low-frequency bands. These results show that neural signals of prior actions and expected reward value persist across delays between those actions and their experienced outcomes. These memory traces may serve a role in reward-based learning in which subjects need to learn actions predicting delayed reward.