scholarly journals Reward does not facilitate visual perceptual learning until sleep occurs

2019 ◽  
Author(s):  
Masako Tamaki ◽  
Aaron V. Berard ◽  
Tyler Barnes-Diana ◽  
Jesse Siegel ◽  
Takeo Watanabe ◽  
...  

ABSTRACTA 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 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 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.Significance statementIndependent 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.

2019 ◽  
Vol 117 (2) ◽  
pp. 959-968 ◽  
Author(s):  
Masako Tamaki ◽  
Aaron V. Berard ◽  
Tyler Barnes-Diana ◽  
Jesse Siegel ◽  
Takeo Watanabe ◽  
...  

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.


2020 ◽  
Author(s):  
Masako Tamaki ◽  
Yuka Sasaki

SummaryAre the sleep-dependent offline performance gains of visual perceptual learning (VPL) consistent with a use-dependent or learning-dependent model? Here, we found that a use-dependent model is inconsistent with the offline performance gains in VPL. In two training conditions with matched visual usages, one generated VPL (learning condition), while the other did not (interference condition). The use-dependent model predicts that slow-wave activity (SWA) during posttraining NREM sleep in the trained region increases in both conditions, in correlation with offline performance gains. However, compared with those in the interference condition, sigma activity, not SWA, during NREM sleep and theta activity during REM sleep, source-localized to the trained early visual areas, increased in the learning condition. Sigma activity correlated with offline performance gain. These significant differences in spontaneous activity between the conditions suggest that there is a learning-dependent process during posttraining sleep for the offline performance gains in VPL.


SLEEP ◽  
2017 ◽  
Vol 40 (suppl_1) ◽  
pp. A85-A85 ◽  
Author(s):  
M Tamaki ◽  
T Watanabe ◽  
Y Sasaki

2017 ◽  
Vol 17 (10) ◽  
pp. 34
Author(s):  
Yuka Sasaki ◽  
Masako Tamaki ◽  
Takeo Watanabe

2019 ◽  
Author(s):  
Masako Tamaki ◽  
Zhiyan Wang ◽  
Tyler Barnes-Diana ◽  
Aaron V. Berard ◽  
Edward Walsh ◽  
...  

AbstractSleep is beneficial for learning. However, whether NREM or REM sleep facilitates learning, whether the learning facilitation results from plasticity increases or stabilization and whether the facilitation results from learning-specific processing are all controversial. Here, after training on a visual task we measured the excitatory and inhibitory neurochemical (E/I) balance, an index of plasticity in human visual areas, for the first time, while subjects slept. Off-line performance gains of presleep learning were associated with the E/I balance increase during NREM sleep, which also occurred without presleep training. In contrast, increased stabilization was associated with decreased E/I balance during REM sleep only after presleep training. These indicate that the above-mentioned issues are not matters of controversy but reflect opposite neurochemical processing for different roles in learning during different sleep stages: NREM sleep increases plasticity leading to performance gains independently of learning, while REM sleep decreases plasticity to stabilize learning in a learning-specific manner.


2018 ◽  
Author(s):  
Masako Tamaki ◽  
Zhiyan Wang ◽  
Takeo Watanabe ◽  
Yuka Sasaki

AbstractIt has been suggested that sleep provides additional enhancement of visual perceptual learning (VPL) acquired before sleep, termed offline performance gains. A majority of the studies that found offline performance gains of VPL used discrimination tasks including the texture discrimination task (TDT). This makes it questionable whether offline performance gains on VPL are generalized to other visual tasks. The present study examined whether a Gabor orientation detection task, which is a standard task in VPL, shows offline performance gains. In Experiment 1, we investigated whether sleep leads to offline performance gains on the task. Subjects were trained with the Gabor orientation detection task, and re-tested it after a 12-hr interval that included either nightly sleep or only wakefulness. We found that performance on the task improved to a significantly greater degree after the interval that included sleep and wakefulness than the interval including wakefulness alone. In addition, offline performance gains were specific to the trained orientation. In Experiment 2, we tested whether offline performance gains occur by a nap. Also, we tested whether spontaneous sigma activity in early visual areas during non-rapid eye movement (NREM) sleep, previously implicated in offline performance gains of TDT, was associated with offline performance gains of the task. A different group of subjects had a nap with polysomnography. The subjects were trained with the task before the nap and re-tested after the nap. The performance of the task improved significantly after the nap only on the trained orientation. Sigma activity in the trained region of early visual areas during NREM sleep was significantly larger than in the untrained region, in correlation with offline performance gains. These aspects were also found with VPL of TDT. The results of the present study demonstrate that offline performance gains are not specific to a discrimination task such as TDT, and can be generalized to other forms of VPL tasks, along with trained-feature specificity. Moreover, the present results also suggest that sigma activity in the trained region of early visual areas plays an important role in offline performance gains of VPL of detection as well as discrimination tasks.


2020 ◽  
Author(s):  
Zhiyan Wang ◽  
Masako Tamaki ◽  
Kazuhisa Shibata ◽  
Michael S. Worden ◽  
Takashi Yamada ◽  
...  

AbstractWhile numerous studies have shown that visual perceptual learning (VPL) occurs as a result of exposure to a visual feature in a task-irrelevant manner, the underlying neural mechanism is poorly understood. In a previous psychophysical study, subjects were repeatedly exposed to a task-irrelevant global motion display that induced the perception of not only the local motions but also a global motion moving in the direction of the spatiotemporal average of the local motion vectors. As a result, subjects enhanced their sensitivity only to the local moving directions, suggesting that early visual areas (V1/V2) that process local motions are involved in task-irrelevant VPL. However, this hypothesis has never been examined by directly examining the involvement of early visual areas (V1/V2). Here, we employed a decoded neurofeedback technique (DecNef) using functional magnetic resonance imaging. During the DecNef training, subjects were trained to induce the activity patterns in V1/V2 that were similar to those evoked by the actual presentation of the global motion display. The DecNef training was conducted with neither the actual presentation of the display nor the subjects’ awareness of the purpose of the experiment. As a result, subjects increased the sensitivity to the local motion directions but not specifically to the global motion direction. The training effect was strictly confined to V1/V2. Moreover, subjects reported that they neither perceived nor imagined any motion during the DecNef training. These results together suggest that that V1/V2 are sufficient for exposure-based task-irrelevant VPL to occur unconsciously.Significance StatementWhile numerous studies have shown that visual perceptual learning (VPL) occurs as a result of exposure to a visual feature in a task-irrelevant manner, the underlying neural mechanism is poorly understood. Previous psychophysical experiments suggest that early visual areas (V1/V2) are involved in task-irrelevant VPL. However, this hypothesis has never been examined by directly examining the involvement of early visual areas (V1/V2). Here, using decoded fMRI neurofeedback, the activity patterns similar to those evoked by the presentation of a complex motion display were repeatedly induced only in early visual areas. The training sensitized only the local motion directions and not the global motion direction, suggesting that V1/V2 are involved in task-irrelevant VPL.


2017 ◽  
Vol 29 (10) ◽  
pp. 1766-1777 ◽  
Author(s):  
Lampros Perogamvros ◽  
Benjamin Baird ◽  
Mitja Seibold ◽  
Brady Riedner ◽  
Melanie Boly ◽  
...  

Thoughts occur during wake as well as during dreaming sleep. Using experience sampling combined with high-density EEG, we investigated the phenomenal qualities and neural correlates of spontaneously occurring thoughts across wakefulness, non-rapid eye movement (NREM) sleep, and REM sleep. Across all states, thoughts were associated with activation of a region of the midcingulate cortex. Thoughts during wakefulness additionally involved a medial prefrontal region, which was associated with metacognitive thoughts during wake. Phenomenologically, waking thoughts had more metacognitive content than thoughts during both NREM and REM sleep, whereas thoughts during REM sleep had a more social content. Together, these results point to a core neural substrate for thoughts, regardless of behavioral state, within the midcingulate cortex, and suggest that medial prefrontal regions may contribute to metacognitive content in waking thoughts.


2018 ◽  
Vol 18 (10) ◽  
pp. 255
Author(s):  
Masako Tamaki ◽  
Aaron Berard ◽  
Takeo Watanabe ◽  
Yuka Sasaki

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