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Articles, Behavioral/Cognitive

Enhanced Spontaneous Oscillations in the Supplementary Motor Area Are Associated with Sleep-Dependent Offline Learning of Finger-Tapping Motor-Sequence Task

Masako Tamaki, Tsung-Ren Huang, Yuko Yotsumoto, Matti Hämäläinen, Fa-Hsuan Lin, José E. Náñez Sr, Takeo Watanabe and Yuka Sasaki
Journal of Neuroscience 21 August 2013, 33 (34) 13894-13902; DOI: https://doi.org/10.1523/JNEUROSCI.1198-13.2013
Masako Tamaki
1Department of Cognitive, Linguistic, and Psychological Sciences, Brown University, Providence, Rhode Island 02912,
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Tsung-Ren Huang
2Department of Psychology, Boston University, Boston, Massachusetts 02215,
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Yuko Yotsumoto
2Department of Psychology, Boston University, Boston, Massachusetts 02215,
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Matti Hämäläinen
3Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Charlestown, Massachusetts 02129,
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Fa-Hsuan Lin
4Institute of Biomedical Engineering, National Taiwan University, Taipei, 100 Taiwan, and
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José E. Náñez Sr
5School of Social and Behavioral Sciences, Arizona State University, Phoenix, Arizona 85004
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Takeo Watanabe
1Department of Cognitive, Linguistic, and Psychological Sciences, Brown University, Providence, Rhode Island 02912,
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Yuka Sasaki
1Department of Cognitive, Linguistic, and Psychological Sciences, Brown University, Providence, Rhode Island 02912,
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Abstract

Sleep is beneficial for various types of learning and memory, including a finger-tapping motor-sequence task. However, methodological issues hinder clarification of the crucial cortical regions for sleep-dependent consolidation in motor-sequence learning. Here, to investigate the core cortical region for sleep-dependent consolidation of finger-tapping motor-sequence learning, while human subjects were asleep, we measured spontaneous cortical oscillations by magnetoencephalography together with polysomnography, and source-localized the origins of oscillations using individual anatomical brain information from MRI. First, we confirmed that performance of the task at a retest session after sleep significantly increased compared with performance at the training session before sleep. Second, spontaneous δ and fast-σ oscillations significantly increased in the supplementary motor area (SMA) during post-training compared with pretraining sleep, showing significant and high correlation with the performance increase. Third, the increased spontaneous oscillations in the SMA correlated with performance improvement were specific to slow-wave sleep. We also found that correlations of δ oscillation between the SMA and the prefrontal and between the SMA and the parietal regions tended to decrease after training. These results suggest that a core brain region for sleep-dependent consolidation of the finger-tapping motor-sequence learning resides in the SMA contralateral to the trained hand and is mediated by spontaneous δ and fast-σ oscillations, especially during slow-wave sleep. The consolidation may arise along with possible reorganization of a larger-scale cortical network that involves the SMA and cortical regions outside the motor regions, including prefrontal and parietal regions.

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The Journal of Neuroscience: 33 (34)
Journal of Neuroscience
Vol. 33, Issue 34
21 Aug 2013
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Enhanced Spontaneous Oscillations in the Supplementary Motor Area Are Associated with Sleep-Dependent Offline Learning of Finger-Tapping Motor-Sequence Task
Masako Tamaki, Tsung-Ren Huang, Yuko Yotsumoto, Matti Hämäläinen, Fa-Hsuan Lin, José E. Náñez Sr, Takeo Watanabe, Yuka Sasaki
Journal of Neuroscience 21 August 2013, 33 (34) 13894-13902; DOI: 10.1523/JNEUROSCI.1198-13.2013

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Enhanced Spontaneous Oscillations in the Supplementary Motor Area Are Associated with Sleep-Dependent Offline Learning of Finger-Tapping Motor-Sequence Task
Masako Tamaki, Tsung-Ren Huang, Yuko Yotsumoto, Matti Hämäläinen, Fa-Hsuan Lin, José E. Náñez Sr, Takeo Watanabe, Yuka Sasaki
Journal of Neuroscience 21 August 2013, 33 (34) 13894-13902; DOI: 10.1523/JNEUROSCI.1198-13.2013
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