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

Abstract

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.

Sleep-dependent offline performance gain in visual perceptual learning is consistent with a learning-dependent model

“…The involvement of brain activity during NREM sleep in the offline performance gains in VPL is consistent with the results of a recent study (Tamaki et al, 2020b). This study demonstrated that the visual plasticity indexed as an excitation and inhibition balance by magnetic resonance spectroscopy was increased during NREM sleep and was correlated with the offline performance gains in VPL (Tamaki et al, 2020b). The results together suggest that after visual training, visual plasticity increases in the early visual areas during posttraining NREM sleep to create a neural environment that promotes sigma activity in the early visual areas, leading to offline performance gains.…”

“…The involvement of brain activity during NREM sleep in the offline performance gains in VPL is consistent with the results of a recent study (Tamaki et al, 2020b). This study demonstrated that the visual plasticity indexed as an excitation and inhibition balance by magnetic resonance spectroscopy was increased during NREM sleep and was correlated with the offline performance gains in VPL (Tamaki et al, 2020b).…”

“…This suggests that sigma activity is primarily involved in offline performance gains, and theta activity may be secondarily involved. A recent study suggests the possibility that theta activity during REM sleep is involved in the stabilization of presleep learning to be resilient to new postsleep learning (Tamaki et al, 2020b). Stabilization of learning is another benefit of sleep (Ellenbogen et al, 2006;Fischer et al, 2002;Gonzalez et al, 2020).…”

“…Numerous studies have demonstrated that sleep is beneficial for various types of learning and memory (Bang et al, 2014;Born & Wilhelm, 2012;Gais et al, 2002;Huber et al, 2004;Maquet et al, 2000;McDevitt et al, 2014;Mednick et al, 2003;Stickgold, 2005;Tamaki et al, 2020a;Tamaki et al, 2020b;Walker et al, 2002;Yotsumoto et al, 2009b). Visual perceptual learning (VPL), which is defined as long-term enhanced performance on a visual task (Lu et al, 2011;Sagi, 2011;Sasaki et al, 2010;Shibata et al, 2011;Watanabe et al, 2001), is one type of learning that shows higher performance after sleep than before sleep.…”

“…Visual perceptual learning (VPL), which is defined as long-term enhanced performance on a visual task (Lu et al, 2011;Sagi, 2011;Sasaki et al, 2010;Shibata et al, 2011;Watanabe et al, 2001), is one type of learning that shows higher performance after sleep than before sleep. Such improvement over sleep in skill learning (Fischer et al, 2002;Karni et al, 1994) is called offline performance gain (Albouy et al, 2013;Korman et al, 2007;Lugassy et al, 2018;Tamaki et al, 2020b;Vien et al, 2019). However, the underlying mechanism of how sleep results in offline performance gain in learning has been controversial.…”