Significance: Sleeping disrupts the conscious awareness of external sounds. We investigated the stage of processing at which this disruption occurs. In the awake brain, when a regular sequence of sounds is presented, a hierarchy of brain areas uses the available regularities to predict forthcoming sounds and to respond with a series of “prediction error” signals when these predictions are violated. Using simultaneous recordings of electroencephalography and magnetoencephalography signals, we discovered that both short-term and long-term brain responses to auditory prediction errors are disrupted during non-rapid eye movement and rapid eye movement sleep; however, the brain still exhibits detectable auditory responses and a capacity to habituate to frequently repeated sounds. Thus, sleep appears to selectively affect the brain’s prediction and error detection systems.
It is well recognized that sleep is severely disturbed in patients in intensive care units (ICU) and that this can compromise their rehabilitation potential. However, it is still difficult to objectively assess sleep quantity and quality and the determinants of sleep disturbance remain unclear. The aim of this study was therefore to evaluate carefully the impact of ICU sound intensity levels and their sources on ICU patients’ sleep over a 24-h period. Sleep and sound levels were recorded in 11 ICU intubated patients who met the criteria. Sleep was recorded using a miniaturized multi-channel ambulatory recording device. Sound intensity levels and their sources were recorded with the Nox-T3 monitor. A 30-s epoch-by-epoch analysis of sleep stages and sound data was carried out. Multinomial and binomial logistic regressions were used to associate sleep stages, wakefulness and sleep–wake transitions with sound levels and their sources. The subjects slept a median of 502.2 [283.2–718.9] min per 24 h; 356.9 [188.6–590.9] min at night (22.00–08.00) and 168.5 [142.5–243.3] during daytime (8 am–10 pm). Median sound intensity level reached 70.2 [65.1–80.3] dBC at night. Sound thresholds leading to disturbed sleep were 63 dBC during the day and 59 dBC during the night. With levels above 77 dBC, the incidence of arousals (OR 3.9, 95% CI 3.0–5.0) and sleep-to-wake transitions (OR 7.6, 95% CI 4.1–14) increased. The most disturbing noises sources were monitor alarms (OR 4.5, 95% CI 3.5–5.6) and ventilator alarms (OR 4.2, 95% CI 2.9–6.1). We have shown, in a small group of 11 non-severe ICU patients, that sound level intensity, a major disturbance factor of sleep continuity, should be strictly controlled on a 24-h profile.
Sleep is known to benefit memory consolidation, but little is known about the contribution of sleep stages within the sleep cycle. The sequential hypothesis proposes that memories are first replayed during nonrapid-eye-movement (NREM or N) sleep and then integrated into existing networks during rapid-eye-movement (REM or R) sleep, two successive critical steps for memory consolidation. However, it lacks experimental evidence as N always precedes R sleep in physiological conditions. We tested this sequential hypothesis in patients with central hypersomnolence disorder, including patients with narcolepsy who present the unique, anti-physiological peculiarity of frequently falling asleep in R sleep before entering N sleep. Patients performed a visual perceptual learning task before and after daytime naps stopped after one sleep cycle, starting in N or R sleep and followed by the other stage (i.e. N-R vs. R-N sleep sequence). We compared over-nap changes in performance, reflecting memory consolidation, depending on the sleep sequence during the nap. Thirty-six patients who slept for a total of 67 naps were included in the analysis. Results show that sleep spindles are associated with memory consolidation only when N is followed by R sleep, that is in physiologically ordered N-R naps, thus providing support to the sequential hypothesis in humans. In addition, we found a negative effect of rapid-eye-movements in R sleep on perceptual consolidation, highlighting the complex role of sleep stages in the balance to remember and to forget.
Can the sleeping brain develop predictions of future auditory stimuli? Past research demonstrated disrupted prediction capabilities during sleep in the context of novel, arbitrary auditory sequences, but the availability of over-learned knowledge already stored in long-term memory could still be preserved. We tested the sleeping brain capabilities to detect violations of simple arithmetic facts. Sleeping subjects were presented with spoken arithmetic facts such as “two plus two is nine” and brain responses to correct or incorrect results were recorded in electro and magneto-encephalography. Sleep responses were compared to both attentive and inattentive wakefulness. During attentive wakefulness, arithmetic violations elicited a succession of N400 and P600 effects, while no such activations could be recorded in sleep or in inattentive wakefulness. Still, small but significant effects remained in sleep, advocating for a preserved but partial accessibility to arithmetic facts stored in long-term memory and preserved predictions of low-level and already learned knowledge. Those effects were very different from residual activities seen in inattention, highlighting the differences of information processing between the sleeping and the inattentive brain.