Reward does not facilitate visual perceptual learning until sleep occurs

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.

Complementary contributions of non-REM and REM sleep to visual learning

“…It is controversial which spontaneous oscillatory activities in EEG, including those for sigma (13-16 Hz) 43 - 45 and delta (1-4 Hz) 46 activity during NREM sleep as well as that for theta (5-7 Hz) 47 , 48 activity during REM sleep, are involved in learning facilitation during sleep. Therefore, how oscillatory activities relate to the E/I balance during NREM sleep and REM is unclear.…”

“…To test whether subjects had an irregular sleep-wake schedule, they were asked to fill out a sleep-wake habits questionnaire 44 , 45 , as well as the Munich Chronotype Questionnaire (MCTQ) 52 . The purpose of the sleep-wake habits questionnaire 44 , 45 was to identify possible sleep problems. The MCTQ 52 was used to examine personal sleep-wake rhythms on both work and free days.…”

“…Sixth, subjects who played action video games frequently were regarded as ineligible because extensive video game playing affects visual and attention processing 53 , 54 . Subjects were asked to fill out a video game questionnaire 44 , 45 , 54 to report their video game habits. Subjects who had played games for more than 5 hours a week in the past 6 months were regarded as ineligible.…”

Does Sleep Selectively Strengthen Certain Memories Over Others Based on Emotion and Perceived Future Relevance?

“…The reward method used in the Tamaki et al 116 1290 studies. Rewards were given during encoding, but participants were not informed about a future reward for successful remembering during a re-test.…”

Reward biases spontaneous neural reactivation during sleep

“…We would thus expect that emotionally-relevant memories have an advantage for reactivation processes occurring during sleep. Initial converging support for this hypothesis comes the following observations: (i) memory for both aversive and rewarding information benefits from sleep [12][13][14][15][16] , (ii) emotional and reward networks (including the amygdala and ventral striatum) are activated during human sleep 17 , and (iii) after a place-reward association task, hippocampal-striatal neuronal ensembles display coordinated replay during sleep in rats 18 . However, prior work did not test for whether and how the reactivation of neural activity corresponding to a rewarded event may compete with that of an equivalent, but nonrewarded event.…”