TY - JOUR
T1 - Reward prediction error modulates saccade vigor
AU - Sedaghat-Nejad, Ehsan
AU - Herzfeld, David J.
AU - Shadmehr, Reza
N1 - Funding Information:
Received Feb. 11, 2019; revised April 16, 2019; accepted April 18, 2019. Author contributions: E.S.-N., D.J.H., and R.S. designed research; E.S.-N. performed research; E.S.-N. analyzed data; E.S.-N. and D.J.H. edited the paper; R.S. wrote the paper. The work was supported by the National Institutes of Health (Grant 5-R01-NS078311), the Office of Naval Research (Grant N00014-15-1-2312), and the National Science Foundation (Grant CNS-1714623). The authors declare no competing financial interests. D.J. Herzfeld’s present address: Department of Neurobiology, Duke University School of Medicine, Durham, NC. Correspondence should be addressed to Ehsan Sedaghat-Nejad at e.sedaghatnejad@gmail.com or Reza Shad-mehr at shadmehr@jhu.edu. https://doi.org/10.1523/JNEUROSCI.0432-19.2019 Copyright © 2019 the authors
Publisher Copyright:
© 2019, Society for Neuroscience. All rights reserved.
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.Onother trials, this content was less valuable (–PEevent).Wefound 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.
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.Onother trials, this content was less valuable (–PEevent).Wefound 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.
KW - Dopamine
KW - Latency
KW - Motor control
KW - Reward prediction error
KW - Saccade
KW - Vigor
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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 -