Reward does not facilitate visual perceptual learning until sleep occurs

Abstract

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

Identifying Long- and Short-Term Processes in Perceptual Learning

“…In addition, different training tasks may engage different long- and short-term processes. For example, sleep-enabled between-session improvement has been observed in texture discrimination and orientation identification tasks (Mascetti et al, 2013; Stickgold et al, 2000; Tamaki et al, 2020) but not in the chevron- and face-identification tasks (Aberg et al, 2009; Hussain et al, 2008).…”

“…1b and 1g; Beard et al, 1995; Levi et al, 1997) or improvement (off-line gain; Figs. 1c and 1h; Karni et al, 1994; Tamaki et al, 2020) in the beginning of each new session.…”

“…Perceptual learning often improves performance through thousands of trials of practice across multiple days (Karni & Sagi, 1993). Although long-term benefits of perceptual learning (Sagi, 2011; Watanabe & Sasaki, 2015) have been observed in a wide range of tasks, from simple feature detection (Fine & Jacobs, 2002) to complex object discrimination (Frank et al, 2020), a number of short-term phenomena, including within-session adaptation (Censor et al, 2006), between-session consolidation (Karni et al, 1994; Stickgold et al, 2000; Tamaki et al, 2020; Yotsumoto et al, 2009), and off-line gain (Bang et al, 2018; Shibata et al, 2017), have also been documented in some tasks. However, other well-known phenomena such as between-session forgetting (De Groot & Keijzer, 2000; Pavlik & Anderson, 2005; Storm et al, 2011) and faster relearning (Jaber, 2005), well documented in other learning domains such as language learning (De Groot & Keijzer, 2000) and skill acquisition (Rickard, 2007), have not been observed in perceptual learning (but see Beard et al, 1995; Mascetti et al, 2013).…”

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

“…Fifth, based on a self-report questionnaire (Tamaki et al, 2020b;, anyone who had a physical or psychiatric disease, was currently under medication, or was suspected to have a sleep disorder was excluded. No subjects were suspected of having insomnia, sleep apnea, restless leg syndrome, sleep walking, narcolepsy, or REM sleep behavior disorder based on a self-reported questionnaire that asked whether the participant had any symptoms known for these sleep disorders (Tamaki et al, 2020a;. Sixth, they had to be aged between 18-30 years.…”

“…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.…”