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Research Article

Reward does not facilitate visual perceptual learning until sleep occurs

View ORCID ProfileMasako Tamaki, Aaron V. Berard, Tyler Barnes-Diana, Jesse Siegel, View ORCID ProfileTakeo Watanabe, and Yuka Sasaki
PNAS January 14, 2020 117 (2) 959-968; first published December 31, 2019 https://doi.org/10.1073/pnas.1913079117
Masako Tamaki
aDepartment of Cognitive, Linguistic, and Psychological Sciences, Brown University, Providence, RI 02912
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  • ORCID record for Masako Tamaki
Aaron V. Berard
aDepartment of Cognitive, Linguistic, and Psychological Sciences, Brown University, Providence, RI 02912
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Tyler Barnes-Diana
aDepartment of Cognitive, Linguistic, and Psychological Sciences, Brown University, Providence, RI 02912
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Jesse Siegel
aDepartment of Cognitive, Linguistic, and Psychological Sciences, Brown University, Providence, RI 02912
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Takeo Watanabe
aDepartment of Cognitive, Linguistic, and Psychological Sciences, Brown University, Providence, RI 02912
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  • ORCID record for Takeo Watanabe
Yuka Sasaki
aDepartment of Cognitive, Linguistic, and Psychological Sciences, Brown University, Providence, RI 02912
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  • For correspondence: yuka_sasaki@brown.edu
  1. Edited by Barbara Anne Dosher, University of California, Irvine, CA, and approved December 9, 2019 (received for review July 31, 2019)

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Significance

Independent lines of research have shown that visual perceptual learning (VPL) is improved by reward or sleep. Here, we show that reward provided during training increased offline performance gains of VPL over sleep. Moreover, during posttraining sleep, reward was associated with longer REM sleep, increased activity in reward processing in the prefrontal region during REM sleep, and decreased activity in the untrained region of early visual areas during NREM and REM sleep. Offline performance gains were correlated with modulated oscillatory activity in reward processing during REM sleep and visual processing during NREM sleep. These results suggest that reward provided during training becomes effective on VPL through the interaction between reward and visual processing during sleep after training.

Abstract

A growing body of evidence indicates that visual perceptual learning (VPL) is enhanced by reward provided during training. Another line of studies has shown that sleep following training also plays a role in facilitating VPL, an effect known as the offline performance gain of VPL. However, whether the effects of reward and sleep interact on VPL remains unclear. Here, we show that reward interacts with sleep to facilitate offline performance gains of VPL. First, we demonstrated a significantly larger offline performance gain over a 12-h interval including sleep in a reward group than that in a no-reward group. However, the offline performance gains over the 12-h interval without sleep were not significantly different with or without reward during training, indicating a crucial interaction between reward and sleep in VPL. Next, we tested whether neural activations during posttraining sleep were modulated after reward was provided during training. Reward provided during training enhanced rapid eye movement (REM) sleep time, increased oscillatory activities for reward processing in the prefrontal region during REM sleep, and inhibited neural activation in the untrained region in early visual areas in non-rapid eye movement (NREM) and REM sleep. The offline performance gains were significantly correlated with oscillatory activities of visual processing during NREM sleep and reward processing during REM sleep in the reward group but not in the no-reward group. These results suggest that reward provided during training becomes effective during sleep, with excited reward processing sending inhibitory signals to suppress noise in visual processing, resulting in larger offline performance gains over sleep.

  • perceptual learning
  • reward
  • REM sleep

Footnotes

  • ↵1M.T. and A.V.B. contributed equally to this work.

  • ↵2To whom correspondence may be addressed. Email: yuka_sasaki{at}brown.edu.
  • Author contributions: Y.S. designed research; M.T., A.V.B., T.B.-D., and J.S. performed research; M.T., A.V.B., T.B.-D., and Y.S. analyzed data; and M.T., A.V.B., T.B.-D., T.W., and Y.S. wrote the paper.

  • The authors declare no competing interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1913079117/-/DCSupplemental.

Published under the PNAS license.

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Reward does not facilitate visual perceptual learning until sleep occurs
Masako Tamaki, Aaron V. Berard, Tyler Barnes-Diana, Jesse Siegel, Takeo Watanabe, Yuka Sasaki
Proceedings of the National Academy of Sciences Jan 2020, 117 (2) 959-968; DOI: 10.1073/pnas.1913079117

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Reward does not facilitate visual perceptual learning until sleep occurs
Masako Tamaki, Aaron V. Berard, Tyler Barnes-Diana, Jesse Siegel, Takeo Watanabe, Yuka Sasaki
Proceedings of the National Academy of Sciences Jan 2020, 117 (2) 959-968; DOI: 10.1073/pnas.1913079117
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