The Fate of Incoming Stimuli during NREM Sleep is Determined by Spindles and the Phase of the Slow Oscillation

Abstract

The present study aimed at identifying the neurophysiological responses associated with auditory stimulation during non-rapid eye movement (NREM) sleep using simultaneous electroencephalography (EEG)/functional magnetic resonance imaging (fMRI) recordings. It was reported earlier that auditory stimuli produce bilateral activation in auditory cortex, thalamus, and caudate during both wakefulness and NREM sleep. However, due to the spontaneous membrane potential fluctuations cortical responses may be highly variable during NREM. Here we now examine the modulation of cerebral responses to tones depending on the presence or absence of sleep spindles and the phase of the slow oscillation. Thirteen healthy young subjects were scanned successfully during stage 2–4 NREM sleep in the first half of the night in a 3 T scanner. Subjects were not sleep-deprived and sounds were post hoc classified according to (i) the presence of sleep spindles or (ii) the phase of the slow oscillation during (±300 ms) tone delivery. These detected sounds were then entered as regressors of interest in fMRI analyses. Interestingly wake-like responses – although somewhat altered in size and location – persisted during NREM sleep, except during present spindles (as previously published in Dang-Vu et al., 2011) and the negative going phase of the slow oscillation during which responses became less consistent or even absent. While the phase of the slow oscillation did not alter brain responses in primary sensory cortex, it did modulate responses at higher cortical levels. In addition EEG analyses show a distinct N550 response to tones during the presence of light sleep spindles and suggest that in deep NREM sleep the brain is more responsive during the positive going slope of the slow oscillation. The presence of short temporal windows during which the brain is open to external stimuli is consistent with the fact that even during deep sleep meaningful events can be detected. Altogether, our results emphasize the notion that spontaneous fluctuations of brain activity profoundly modify brain responses to external information across all behavioral states, including deep NREM sleep.

Sleep Spindles and Intellectual Ability: Epiphenomenon or Directly Related?

“…The functional significance and biological basis of these interindividual differences remain to be fully elucidated; however, the relationship between spindles and intellectual ability is well established across numerous studies employing various but related tests including the MAB-II (Fogel et al, 2007;Fogel & Smith, 2006;Nader & Smith, 2001, 2003, the Raven's Standard and Advanced Progressive Matrices Tests (Ujma et al, 2014;Schabus et al, 2006;Bódizs et al, 2005), the Wechsler Memory Scale-Revised (Schabus et al, 2006), and the Cattell's Culture Fair Intelligence Test (Ujma et al, 2014). Importantly, sleep spindles are also associated with sleep maintenance (Schabus et al, 2012;Dang-Vu et al, 2010;Vyazovskiy et al, 2004;Cote et al, 2000;Elton et al, 1997;Steriade, 1991) and circadian rhythmicity (Dijk & Cajochen, 1997;Dijk & Czeisler, 1995;Dijk et al, 1993. In addition, sleep quality (Nebes et al, 2009;Blackwell et al, 2006;Achilles, 2003;Bastien et al, 2003;Hauri, 1997;Bonnet & Arand, 1995) and circadian rhythmicity (Achilles, 2003;Taillard, Philip Roberts & Kyllonen, 1999;Dijk & Cajochen, 1997;Dijk & Czeisler, 1995;Dijk et al, 1993 are also associated with cognitive abilities.…”

“…For example, Dang-Vu and colleagues (2010) demonstrated that individuals who generate a greater number of sleep spindles maintain sleep better in the face of disruptive stimuli. In addition, brain responses to external auditory stimuli are absent when the stimuli are presented during a sleep spindle (Schabus et al, 2012;Cote et al, 2000), but not outside spindle events. Furthermore, related studies also demonstrated that sleep spindles measured on a normal, quiet/undisturbed night of sleep were predictive of sleep quality on a subsequent night in a noisy environment (Dang-Vu et al, 2010).…”

“…Sleep spindles have also been shown to protect sleep from external stimuli (Schabus et al, 2012;Dang-Vu, McKinney, Buxton, Solet, & Ellenbogen, 2010;Vyazovskiy, Achermann, Borbely, & Tobler, 2004;Cote, Epps, & Campbell, 2000;Elton et al, 1997;Peters & Jones, 1991). For example, Dang-Vu and colleagues (2010) demonstrated that individuals who generate a greater number of sleep spindles maintain sleep better in the face of disruptive stimuli.…”

Sleep Fragmentation Does Not Explain Misperception of Latency or Total Sleep Time

“…Future work should assess other aspects of sleep physiology (such as EEG) that may contribute to misperception. For example, spindle and alpha activities have been linked to resistance to sensory perturbation, [37][38][39] which may impact perception. REM sleep has been reported as contributing to the subjective sense of wakefulness in sleep, which could be consistent with our observation that more stable REM was linked to TST misperception.…”

Automatic Sleep Spindle Detection with EEG Based on Complex Demodulation Method and Decision Tree Model

“…The frequency of sleep spindle is about 12 -14 Hz, and its duration should be at least 0.5 seconds [1]. Sleep spindle is related to the investigation of sleep [3]. In addition, the characters of spindle such as power [4] and density [5] are related to cognition and memory of human.…”