Dataset Information

Night Watch in One Brain Hemisphere during Sleep Associated with the First-Night Effect in Humans.

ABSTRACT: We often experience troubled sleep in a novel environment [1]. This is called the first-night effect (FNE) in human sleep research and has been regarded as a typical sleep disturbance [2-4]. Here, we show that the FNE is a manifestation of one hemisphere being more vigilant than the other as a night watch to monitor unfamiliar surroundings during sleep [5, 6]. Using advanced neuroimaging techniques [7, 8] as well as polysomnography, we found that the temporary sleep disturbance in the first sleep experimental session involves regional interhemispheric asymmetry of sleep depth [9]. The interhemispheric asymmetry of sleep depth associated with the FNE was found in the default-mode network (DMN) involved with spontaneous internal thoughts during wakeful rest [10, 11]. The degree of asymmetry was significantly correlated with the sleep-onset latency, which reflects the degree of difficulty of falling asleep and is a critical measure for the FNE. Furthermore, the hemisphere with reduced sleep depth showed enhanced evoked brain response to deviant external stimuli. Deviant external stimuli detected by the less-sleeping hemisphere caused more arousals and faster behavioral responses than those detected by the other hemisphere. None of these asymmetries were evident during subsequent sleep sessions. These lines of evidence are in accord with the hypothesis that troubled sleep in an unfamiliar environment is an act for survival over an unfamiliar and potentially dangerous environment by keeping one hemisphere partially more vigilant than the other hemisphere as a night watch, which wakes the sleeper up when unfamiliar external signals are detected.

SUBMITTER: Tamaki M

PROVIDER: S-EPMC4864126 | biostudies-literature | 2016 May

REPOSITORIES: biostudies-literature

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Night Watch in One Brain Hemisphere during Sleep Associated with the First-Night Effect in Humans.

Tamaki Masako M Bang Ji Won JW Watanabe Takeo T Sasaki Yuka Y

Current biology : CB 20160421 9

We often experience troubled sleep in a novel environment [1]. This is called the first-night effect (FNE) in human sleep research and has been regarded as a typical sleep disturbance [2-4]. Here, we show that the FNE is a manifestation of one hemisphere being more vigilant than the other as a night watch to monitor unfamiliar surroundings during sleep [5, 6]. Using advanced neuroimaging techniques [7, 8] as well as polysomnography, we found that the temporary sleep disturbance in the first slee ...[more]

PMID: 27112296

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Project description:We experience disturbed sleep in a new place, and this effect is known as the first-night effect (FNE) in sleep research. We previously demonstrated that the FNE is associated with a surveillance system in one brain hemisphere during NREM sleep, which manifests as interhemispheric asymmetry in sleep depth in the default-mode network (DMN) and increased vigilance toward monitoring external stimuli. This surveillance system may be useful for protecting vulnerable sleepers from abnormal events in unfamiliar environments. The present study investigated whether a similar surveillance system is exhibited during rapid eye movement (REM) sleep. The impacts of the FNE could be different between the phasic period, in which eyes move rapidly, and the tonic period, in which eye movement ceases, of REM sleep; without the FNE, vigilance to external stimuli is generally reduced during the phasic period but not the tonic period. Thus, REM sleep was split into phasic and tonic periods. First, we replicated previous findings showing interhemispheric asymmetry in delta activity in the DMN associated with the FNE during NREM sleep. However, during REM sleep, interhemispheric asymmetry in delta activity or theta activities, two oscillatory activities during REM sleep, was not found during the phasic or tonic periods. Next, we tested whether vigilance, as measured by evoked brain responses (P2) to deviant tones, associated with the FNE was increased in one hemisphere during REM sleep. The P2 amplitudes during the phasic period were augmented by the FNE on day 1 and were significantly larger than those on day 2 when the FNE was not present. In contrast, the P2 amplitudes during the tonic period were not different across days. The P2 amplitudes showed no interhemispheric asymmetry during the phasic or tonic periods. These results suggest that while the surveillance system exhibits interhemispheric asymmetry in sleep depth and vigilance during NREM sleep, this system shows no interhemispheric asymmetry in oscillatory activities and exhibits increased vigilance in both hemispheres only during the phasic period of REM sleep. Therefore, the surveillance system associated with the FNE may involve different mechanisms during NREM and REM sleep.

Project description:Background: Sleep loss contributes to obesity through a variety of mechanisms, including neuroendocrine functioning, increased hunger, and increased food intake. Additionally, sleep loss alters functional activation within brain regions associated with reward and behavioral control. However, it remains unknown whether individual differences in baseline neural functioning can predict eating behaviors during total sleep deprivation (TSD). We used functional magnetic resonance imaging (fMRI) to test the hypothesis that individuals with increased baseline responsiveness within reward regions are more vulnerable to TSD-induced overeating. Methods: N = 45 subjects completed several fMRI scans during a single pre-TSD session that included performance on the Multi-Source Interference Task (MSIT) and the n-back task. Subjects returned to the laboratory for an overnight TSD session, during which they were given ad libitum access to 10,900 kcal of food. Leftover food and packaging were collected every 6 h (00:00, 06:00, and 12:00) to measure total food consumption. Subjects reported sleepiness every hour and performed a food rating task every 3 h. Results: Functional activation within the ventral striatum during the MSIT and n-back positively correlated with total caloric and carbohydrate intake during the final 6 h (06:00-12:00) of TSD. Activation within the middle and superior temporal gyri during the MSIT also correlated with total carbohydrates consumed. Food consumption did not correlate with subjective sleepiness, hunger, or food desire. Conclusions: Individual differences in neural activity of reward processing areas (i.e., nucleus accumbens) prior to sleep deprivation are associated with an individual's propensity to overeat during subsequent sleep deprivation. This suggests that individual differences within reward processing pathways are potential key factors in sleep loss related overeating. Sleep loss and obesity are tightly linked. Both phenomena have been associated with increased neural activation in regions associated with reward, inhibitory control, and disrupted dopamine signaling. Elevated baseline reward sensitivity in the ventral striatum appears to be further compounded by sleep deprivation induced dysfunction in the reward neurocircuitry, increasing the likelihood of overeating. Our findings suggest that large individual differences in baseline responsiveness of hedonic reward pathways may modulate the association between sleep loss and obesity.

Dataset Information

Night Watch in One Brain Hemisphere during Sleep Associated with the First-Night Effect in Humans.

Publications

Night Watch in One Brain Hemisphere during Sleep Associated with the First-Night Effect in Humans.

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