Embracing sleep-onset complexity.

Sleep is crucial for many vital functions and has been extensively studied. By contrast, the sleep-onset period (SOP), often portrayed as a mere prelude to sleep, has been largely overlooked and remains poorly characterized. Recent findings, however, have reignited interest in this transitional period and have shed light on its neural mechanisms, cognitive dynamics, and clinical implications. This review synthesizes the existing knowledge about the SOP in humans. We first examine the current definition of the SOP and its limits, and consider the dynamic and complex electrophysiological changes that accompany the descent to sleep. We then describe the interplay between internal and external processing during the wake-to-sleep transition. Finally, we discuss the putative cognitive benefits of the SOP and identify novel directions to better diagnose sleep-onset disorders.

A doorway into possibility.

The borderland between wakefulness and sleep promotes creativity.

Memory loss at sleep onset.

Every night, we pass through a transitory zone at the borderland between wakefulness and sleep, named the first stage of nonrapid eye movement sleep (N1). N1 sleep is associated with increased hippocampal activity and dream-like experiences that incorporate recent wake materials, suggesting that it may be associated with memory processing. Here, we investigated the specific contribution of N1 sleep in the processing of memory traces. Participants were asked to learn the precise locations of 48 objects on a grid and were then tested on their memory for these items before and after a 30-min rest during which participants either stayed fully awake or transitioned toward N1 or deeper (N2) sleep. We showed that memory recall was lower (10% forgetting) after a resting period, including only N1 sleep compared to N2 sleep. Furthermore, the ratio of alpha/theta power (an electroencephalography marker of the transition toward sleep) correlated negatively with the forgetting rate when taking into account all sleepers (N1 and N2 groups combined), suggesting a physiological index for memory loss that transcends sleep stages. Our findings suggest that interrupting sleep onset at N1 may alter sleep-dependent memory consolidation and promote forgetting.

Sleep onset is a creative sweet spot.

The ability to think creatively is paramount to facing new challenges, but how creativity arises remains mysterious. Here, we show that the brain activity common to the twilight zone between sleep and wakefulness (nonrapid eye movement sleep stage 1 or N1) ignites creative sparks. Participants (N = 103) were exposed to mathematical problems without knowing that a hidden rule allowed solving them almost instantly. We found that spending at least 15 s in N1 during a resting period tripled the chance to discover the hidden rule (83% versus 30% when participants remained awake), and this effect vanished if subjects reached deeper sleep. Our findings suggest that there is a creative sweet spot within the sleep-onset period, and hitting it requires individuals balancing falling asleep easily against falling asleep too deeply.

Sleepers Selectively Suppress Informative Inputs during Rapid Eye Movements.

Sleep leads to a disconnection from the external world. Even when sleepers regain consciousness during rapid eye movement (REM) sleep, little, if any, external information is incorporated into dream content [1-3]. While gating mechanisms might be at play to avoid interference on dreaming activity [4], a total disconnection from an ever-changing environment may prevent the sleeper from promptly responding to informative events (e.g., threat signals). In fact, a whole range of neural responses to external events turns out to be preserved during REM sleep [5-9]. Thus, it remains unclear whether external inputs are either processed or, conversely, gated during REM sleep. One way to resolve this issue is to consider the specific impact of eye movements (EMs) characterizing REM sleep. EMs are a reliable predictor of reporting a dream upon awakening [10, 11], and their absence is associated with a lower arousal threshold to external stimuli [12]. We thus hypothesized that the presence of EMs would selectively prevent the processing of informative stimuli, whereas periods of REM sleep devoid of EMs would be associated with the monitoring of external signals. By reconstructing speech in a multi-talker environment from electrophysiological responses, we show that informative speech is amplified over meaningless speech during REM sleep. Yet, at the precise timing of EMs, informative speech is, on the contrary, selectively suppressed. These results demonstrate the flexible amplification and suppression of sensory information during REM sleep and reveal the impact of EMs on the selective gating of informative stimuli during sleep.

Increased creative thinking in narcolepsy.

Some studies suggest a link between creativity and rapid eye movement sleep. Narcolepsy is characterized by falling asleep directly into rapid eye movement sleep, states of dissociated wakefulness and rapid eye movement sleep (cataplexy, hypnagogic hallucinations, sleep paralysis, rapid eye movement sleep behaviour disorder and lucid dreaming) and a high dream recall frequency. Lucid dreaming (the awareness of dreaming while dreaming) has been correlated with creativity. Given their life-long privileged access to rapid eye movement sleep and dreams, we hypothesized that subjects with narcolepsy may have developed high creative abilities. To test this assumption, 185 subjects with narcolepsy and 126 healthy controls were evaluated for their level of creativity with two questionnaires, the Test of Creative Profile and the Creativity Achievement Questionnaire. Creativity was also objectively tested in 30 controls and 30 subjects with narcolepsy using the Evaluation of Potential Creativity test battery, which measures divergent and convergent modes of creative thinking in the graphic and verbal domains, using concrete and abstract problems. Subjects with narcolepsy obtained higher scores than controls on the Test of Creative Profile (mean ± standard deviation: 58.9 ± 9.6 versus 55.1 ± 10, P = 0.001), in the three creative profiles (Innovative, Imaginative and Researcher) and on the Creative Achievement Questionnaire (10.4 ± 25.7 versus 6.4 ± 7.6, P = 0.047). They also performed better than controls on the objective test of creative performance (4.3 ± 1.5 versus 3.7 ± 1.4; P = 0.009). Most symptoms of narcolepsy (including sleepiness, hypnagogic hallucinations, sleep paralysis, lucid dreaming, and rapid eye movement sleep behaviour disorder, but not cataplexy) were associated with higher scores on the Test of Creative Profile. These results highlight a higher creative potential in subjects with narcolepsy and further support a role of rapid eye movement sleep in creativity.