Reward prediction error modulates saccade vigor

Abstract

Movements toward rewarding stimuli exhibit greater vigor, i.e., increased velocity and reduced reaction-times. This invigoration may be due to release of dopamine before movement onset. Dopamine release is strongly modulated by reward prediction error (RPE). Here, we generated an RPE event in the milliseconds before movement onset and tested whether there was a causal relationship between RPE and vigor. Human subjects made saccades toward an image. During the execution of their primary saccade, we probabilistically changed the position and content of the image. This led to a secondary saccade following completion of the primary saccade. We focused on properties of this secondary saccade. On some trials, the content of the secondary image was more valuable than the first image, resulting in a +RPE event that preceded the secondary saccade. On other trials, this content was less valuable, resulting in a -RPE event. We found that reaction-time and velocity of the secondary saccade were affected in an orderly fashion by the magnitude and direction of the preceding RPE event: the most vigorous saccades followed the largest +RPE, whereas the least vigorous saccades followed the largest -RPE. Presence of the secondary saccade indicated that the primary saccade had experienced a movement error, inducing trial-to-trial adaptation: the subsequent primary saccade was changed in the direction of the movement error in the previous trial. However, motor learning from error was not affected by the RPE event. Therefore, reward prediction error, and not reward per se, modulated vigor of saccades. Author summaryDoes dopamine release before onset of a movement modulate vigor of the ensuing movement? To test this hypothesis, we relied on the fact that RPE is a strong modulator of dopamine. Our innovation was a task in which an RPE event occurred precisely before onset of a movement. We probabilistically produced a combination of large or small, negative or positive RPE events before onset of a saccade, and observed that the vigor of the saccade that followed carried a robust signature of the preceding RPE event: high vigor saccades followed +RPE events, while low vigor saccades followed -RPE events. This suggests that control of vigor is partly through release of dopamine in the moments before onset of the movement.