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Research Articles, Behavioral/Cognitive

Selective Enhancement of Post-Sleep Visual Motion Perception by Repetitive Tactile Stimulation during Sleep

Yoshiyuki Onuki, Oti Lakbila-Kamal, Bo Scheffer, Eus J. W. Van Someren and Ysbrand D. Van der Werf
Journal of Neuroscience 28 September 2022, 42 (39) 7400-7411; DOI: https://doi.org/10.1523/JNEUROSCI.1512-21.2022
Yoshiyuki Onuki
1Department of Sleep and Cognition, Netherlands Institute for Neuroscience, an institute of the Royal Netherlands Academy of Arts and Sciences, Amsterdam, 1105BA, The Netherlands
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Oti Lakbila-Kamal
1Department of Sleep and Cognition, Netherlands Institute for Neuroscience, an institute of the Royal Netherlands Academy of Arts and Sciences, Amsterdam, 1105BA, The Netherlands
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Bo Scheffer
1Department of Sleep and Cognition, Netherlands Institute for Neuroscience, an institute of the Royal Netherlands Academy of Arts and Sciences, Amsterdam, 1105BA, The Netherlands
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Eus J. W. Van Someren
1Department of Sleep and Cognition, Netherlands Institute for Neuroscience, an institute of the Royal Netherlands Academy of Arts and Sciences, Amsterdam, 1105BA, The Netherlands
2Department of Integrative Neurophysiology, Center for Neurogenomics and Cognitive Research, Amsterdam Neuroscience, VU University Amsterdam, Amsterdam, 1081HV, The Netherlands
3Amsterdam UMC, Vrije Universiteit, Psychiatry, Amsterdam Neuroscience, Amsterdam, 1081HV, The Netherlands
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Ysbrand D. Van der Werf
4Department of Anatomy and Neurosciences, Amsterdam UMC, location VU, University Medical Center, Amsterdam, 1081HZ, The Netherlands
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Abstract

Tactile sensations can bias visual perception in the awake state while visual sensitivity is known to be facilitated by sleep. It remains unknown, however, whether the tactile sensation during sleep can bias the visual improvement after sleep. Here, we performed nap experiments in human participants (n = 56, 18 males, 38 females) to demonstrate that repetitive tactile motion stimulation on the fingertip during slow wave sleep selectively enhanced subsequent visual motion detection. The visual improvement was associated with slow wave activity. The high activation at the high beta frequency was found in the occipital electrodes after the tactile motion stimulation during sleep, indicating a visual-tactile cross-modal interaction during sleep. Furthermore, a second experiment (n = 14, 14 females) to examine whether a hand- or head-centered coordination is dominant for the interpretation of tactile motion direction showed that the biasing effect on visual improvement occurs according to the hand-centered coordination. These results suggest that tactile information can be interpreted during sleep, and can induce the selective improvement of post-sleep visual motion detection.

SIGNIFICANCE STATEMENT Tactile sensations can bias our visual perception as a form of cross-modal interaction. However, it was reported only in the awake state. Here we show that repetitive directional tactile motion stimulation on the fingertip during slow wave sleep selectively enhanced subsequent visual motion perception. Moreover, the visual improvement was positively associated with sleep slow wave activity. The tactile motion stimulation during slow wave activity increased the activation at the high beta frequency over the occipital electrodes. The visual improvement occurred in agreement with a hand-centered reference frame. These results suggest that our sleeping brain can interpret tactile information based on a hand-centered reference frame, which can cause the sleep-dependent improvement of visual motion detection.

  • consolidation
  • cross-modal interaction
  • sleep
  • tactile
  • vision

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The Journal of Neuroscience: 42 (39)
Journal of Neuroscience
Vol. 42, Issue 39
28 Sep 2022
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Selective Enhancement of Post-Sleep Visual Motion Perception by Repetitive Tactile Stimulation during Sleep
Yoshiyuki Onuki, Oti Lakbila-Kamal, Bo Scheffer, Eus J. W. Van Someren, Ysbrand D. Van der Werf
Journal of Neuroscience 28 September 2022, 42 (39) 7400-7411; DOI: 10.1523/JNEUROSCI.1512-21.2022

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Selective Enhancement of Post-Sleep Visual Motion Perception by Repetitive Tactile Stimulation during Sleep
Yoshiyuki Onuki, Oti Lakbila-Kamal, Bo Scheffer, Eus J. W. Van Someren, Ysbrand D. Van der Werf
Journal of Neuroscience 28 September 2022, 42 (39) 7400-7411; DOI: 10.1523/JNEUROSCI.1512-21.2022
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Keywords

  • consolidation
  • cross-modal interaction
  • sleep
  • tactile
  • vision

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