Reward Prediction Error Modulates Saccade Vigor

TY - JOUR

T1 - Reward Prediction Error Modulates Saccade Vigor

AU - Sedaghat-Nejad, Ehsan

AU - Herzfeld, David J.

AU - Shadmehr, Reza

PY - 2019/6/19

Y1 - 2019/6/19

N2 - Movement vigor, defined as the reciprocal of the latency from availability of reward to its acquisition, changes with reward magnitude: movements exhibit shorter reaction time and increased velocity when they are directed toward more rewarding stimuli. This invigoration may be due to release of dopamine before movement onset, which has been shown to be modulated by events that signal reward prediction error (RPE). Here, we generated an RPE event in the milliseconds before movement onset and tested whether there was a relationship between RPE and vigor. Human subjects (both sexes) made saccades toward an image. During execution of the primary saccade, we probabilistically changed the position and content of that image, encouraging a secondary saccade. On some trials, the content of the secondary image was more valuable than the first image, resulting in a positive RPE (+RPE) event that preceded the secondary saccade. On other trials, this content was less valuable (-RPE event). We found that reaction time of the secondary saccade was 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. However, this learning from movement error was not modulated by the RPE event. The data suggest that RPE events, which are thought to transiently alter the release of dopamine, modulate the vigor of the ensuing movement.SIGNIFICANCE STATEMENT Does dopamine release in response to a stimulus serve to invigorate the ensuing movement? To test this hypothesis, we relied on the fact that reward prediction error (RPE) is a strong modulator of dopamine. Our innovation was a task in which an RPE event occurred precisely before onset of a stimulus-driven movement. We probabilistically produced a combination of large or small, negative or positive RPE events and observed that saccade vigor carried a robust signature of the preceding RPE event: high vigor saccades followed +RPE events, whereas low vigor saccades followed -RPE events. This suggests that in humans, vigor is partly controlled through release of dopamine in the moments before onset of a movement.

AB - Movement vigor, defined as the reciprocal of the latency from availability of reward to its acquisition, changes with reward magnitude: movements exhibit shorter reaction time and increased velocity when they are directed toward more rewarding stimuli. This invigoration may be due to release of dopamine before movement onset, which has been shown to be modulated by events that signal reward prediction error (RPE). Here, we generated an RPE event in the milliseconds before movement onset and tested whether there was a relationship between RPE and vigor. Human subjects (both sexes) made saccades toward an image. During execution of the primary saccade, we probabilistically changed the position and content of that image, encouraging a secondary saccade. On some trials, the content of the secondary image was more valuable than the first image, resulting in a positive RPE (+RPE) event that preceded the secondary saccade. On other trials, this content was less valuable (-RPE event). We found that reaction time of the secondary saccade was 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. However, this learning from movement error was not modulated by the RPE event. The data suggest that RPE events, which are thought to transiently alter the release of dopamine, modulate the vigor of the ensuing movement.SIGNIFICANCE STATEMENT Does dopamine release in response to a stimulus serve to invigorate the ensuing movement? To test this hypothesis, we relied on the fact that reward prediction error (RPE) is a strong modulator of dopamine. Our innovation was a task in which an RPE event occurred precisely before onset of a stimulus-driven movement. We probabilistically produced a combination of large or small, negative or positive RPE events and observed that saccade vigor carried a robust signature of the preceding RPE event: high vigor saccades followed +RPE events, whereas low vigor saccades followed -RPE events. This suggests that in humans, vigor is partly controlled through release of dopamine in the moments before onset of a movement.

KW - dopamine

KW - latency

KW - motor control

KW - reward prediction error

KW - saccade

KW - vigor

UR - http://www.scopus.com/inward/record.url?scp=85068488271&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85068488271&partnerID=8YFLogxK

U2 - 10.1523/JNEUROSCI.0432-19.2019

DO - 10.1523/JNEUROSCI.0432-19.2019

M3 - Article

C2 - 31015343

AN - SCOPUS:85068488271

VL - 39

SP - 5010

EP - 5017

JO - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

IS - 25

ER -