Sleep is beneficial for learning. However, it remains unclear whether learning is facilitated by non-REM (NREM) sleep or by REM sleep, whether it results from plasticity increases or stabilization, and whether facilitation results from learning-specific processing. Here, we trained volunteers on a visual task, and measured the excitatory and inhibitory (E/I) balance in early visual areas during subsequent sleep as an index of plasticity. E/I balance increased during NREM sleep irrespective of whether pre-sleep learning occurred, but it was associated with post-sleep performance gains relative to pre-sleep performance. By contrast, E/I balance decreased during REM sleep but only after pre-sleep training, and the decrease was associated with stabilization of pre-sleep learning. These findings indicate that NREM sleep promotes plasticity, leading to performance gains independent of learning, while REM sleep decreases plasticity to stabilize learning in a learning-specific manner.
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.
19 A growing body of evidence indicates that visual perceptual learning (VPL) is enhanced 20 by reward provided during training. Another line of studies has shown that sleep following 21 training also plays a role in facilitating VPL, an effect known as the offline performance gain of 22 VPL. However, whether the effects of reward and sleep interact on VPL remains unclear. Here, 23 we show that reward interacts with sleep to facilitate offline performance gains of VPL. First, we 24 demonstrated a significantly larger offline performance gain over a 12-h interval including sleep 25 in a reward group than that in a No-reward group. However, the offline performance gains over 26 the 12-h interval without sleep were not significantly different with or without reward during 27 training, indicating a crucial interaction between reward and sleep in VPL. Next, we tested 28 whether neural activations during posttraining sleep were modulated after reward was provided 29 during training. Reward provided during training enhanced REM sleep time, increased 30 oscillatory activities for reward processing in the prefrontal region during REM sleep, and 31 inhibited neural activation in the untrained region in early visual areas in NREM and REM sleep. 32 The offline performance gains were significantly correlated with oscillatory activities of visual 33 processing during NREM sleep and reward processing during REM sleep in the reward group 34 but not in the No-reward group. These results suggest that reward provided during training 35 becomes effective during sleep, with excited reward processing sending inhibitory signals to 36 suppress noise in visual processing, resulting in larger offline performance gains over sleep. 37 38 Significance statement 39 Independent lines of research have shown that visual perceptual learning (VPL) is 40 improved by reward or sleep. Here, we show that reward provided during training increased 41 offline performance gains of VPL over sleep. Moreover, during posttraining sleep, reward was 42 associated with longer REM sleep, increased activity in reward processing in the prefrontal 43 region during REM sleep, and decreased activity in the untrained region of early visual areas 44 during NREM and REM sleep. Offline performance gains were correlated with modulated 45 oscillatory activity in reward processing during REM sleep and visual processing during NREM 46 sleep. These results suggest that reward provided during training becomes effective on VPL 47 through the interaction between reward and visual processing during sleep after training. 48 3 INTRODUCTION 49
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