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.

Figure 1. SWA asymmetry in the DMN during slow-wave sleep in association with the FNE

(A) SWA in the DMN during slow-wave sleep. Red bars show the left hemisphere, and the blue bars show the right hemisphere. The values are mean ± SEM. Asterisks indicate a significant difference in the post-hoc tests after the 4-way repeated measures ANOVA (*p<0.05). (B) Scatter plots for the asymmetry index of DMN SWA against the sleep-onset latency for day 1 (r=−0.68, p=0.022), and (C) day 2 (r=0.03, p=0.935, n.s.). *p<0.05. The correlation coefficient on day 1 was significantly different from day 2 (zpf₁₀=−1.99, p=0.046). See Figure S1 for SWA in other networks, details of ANOVA results and details of the asymmetry index. See also Figure S2 for additional data on SWA.

Figure 2. Brain responses during slow-wave sleep

(A) The amplitudes of the brain responses to deviant sounds in the left (red) and right (blue) hemispheres (μV). Asterisks indicate a significant difference in the post-hoc tests after the 3-way repeated measures ANOVA (**p<0.01, *p<0.05). (B) The amplitudes of the brain responses to standard sounds in the left (red) and right (blue) hemispheres (μV). The values are mean ± SEM. See Figure S3 for additional information regarding brain responses including detailed results of the ANOVA, timecourse, and the brain responses in other sleep stages.

Figure 3. Arousals followed by deviant sounds presented during slow-wave sleep

(A) The total number of arousals per min during slow-wave sleep. There was a significant difference in the number of arousals per min between days (Wilcoxon signed-rank test, z₁₂=3.18, p=0.002). (B) The percentage of arousal occurrences that followed left-hemisphere trials (red) and right-hemisphere trials (blue). The values are mean ± SEM. ***p<0.005, *p<0.05, the false discovery rate (FDR) was controlled to be at 0.05.

Figure 4. Awakening and behavioral responses followed by deviant sounds

(A) The number of subjects who were woken in the left- (red) and right- (blue) hemisphere trials. The numbers of subjects who were woken on the left- and right hemisphere trials were significantly different between days (McNemar’s test, p=0.033). The number of subjects who were woken on the left-hemisphere trials was significantly larger than chance on day 1 (Wilcoxon signed-rank test, z₁₀=2.11, p=0.035). (B) The reaction time between the deviant sound and the finger tapping. The reaction time was significantly faster on day 1 than day 2 (Wilcoxon signed-rank test, z₁₀=2.31, p=0.021). The values are mean ± SEM. *p<0.05. See Figure S4 for additional information on the reaction time.