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. 2018 Oct 24;38(43):9175-9185.
doi: 10.1523/JNEUROSCI.0855-18.2018. Epub 2018 Sep 10.

Dreaming in NREM Sleep: A High-Density EEG Study of Slow Waves and Spindles

Francesca Siclari  1 , Giulio Bernardi  2   3 , Jacinthe Cataldi  2 , Giulio Tononi  4
Affiliations

Dreaming in NREM Sleep: A High-Density EEG Study of Slow Waves and Spindles

Francesca Siclari et al. J Neurosci. .

Abstract

Dreaming can occur in both rapid eye movement (REM) and non-REM (NREM) sleep. We recently showed that in both REM and NREM sleep, dreaming is associated with local decreases in slow wave activity (SWA) in posterior brain regions. To expand these findings, here we asked how specific features of slow waves and spindles, the hallmarks of NREM sleep, relate to dream experiences. Fourteen healthy human subjects (10 females) underwent nocturnal high-density EEG recordings combined with a serial awakening paradigm. Reports of dreaming, compared with reports of no experience, were preceded by fewer, smaller, and shallower slow waves, and faster spindles, especially in central and posterior cortical areas. We also identified a minority of very steep and large slow waves in frontal regions, which occurred on a background of reduced SWA and were associated with high-frequency power increases (local "microarousals") heralding the successful recall of dream content. These results suggest that the capacity of the brain to generate experiences during sleep is reduced in the presence of neuronal off-states in posterior and central brain regions, and that dream recall may be facilitated by the intermittent activation of arousal systems during NREM sleep.SIGNIFICANCE STATEMENT By combining high-density EEG recordings with a serial awakening paradigm in healthy subjects, we show that dreaming in non-rapid eye movement sleep occurs when slow waves in central and posterior regions are sparse, small, and shallow. We also identified a small subset of very large and steep frontal slow waves that are associated with high-frequency activity increases (local "microarousals") heralding successful recall of dream content. These results provide noninvasive measures that could represent a useful tool to infer the state of consciousness during sleep.

Keywords: consciousness; dream; high-density EEG; sleep; slow wave.

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Figures

Figure 1.
Figure 1.
Top row, Topographical distribution of t values for the contrast between dream experiences and no experiences for different slow-wave parameters, averaged over the last 60 s before the awakening. Bottom row, Same as the top row, but electrodes within a cluster showing a statistically significant effect are marked in white (p < 0.05, cluster-based correction for multiple comparisons, two-tailed paired t tests; n = 12 subjects).
Figure 2.
Figure 2.
Top row, Topographical distribution of slow-wave parameters for dream experiences (DEs) (first row) and no experiences (NEs) (second row). Slow-wave parameters were averaged over the last 60 s before the awakening and across 12 subjects. In the third row, the mean differences between DE and NE (DE − NE) are shown for each parameter, so that red colors indicate higher values in DE, and blue colors higher values in NE. In the fourth row, p values for paired electrode-by-electrode t tests are shown (p < 0.05, uncorrected).
Figure 3.
Figure 3.
Top row, Topographical distribution of t values for the contrast between dream experiences without recall of content and no experiences for different slow-wave parameters averaged over the last 60 s before the awakening. Bottom row, Same as the top row, but electrodes within a cluster showing a statistically significant effect are marked in white (p < 0.05, cluster-based correction for multiple comparisons, two-tailed paired t tests; n = 12 subjects).
Figure 4.
Figure 4.
Top row, Topographical distribution of t values for the contrast between dream experiences and no experiences for different slow-wave parameters averaged over the last 60 s before the awakening. For each subject, only slow waves larger than the 75th amplitude percentile (across all slow waves detected in NREM sleep) were included. Bottom row, Same as the top row, but electrodes within a cluster showing a statistically significant effect are now marked in white (p < 0.05, cluster-based correction for multiple comparisons, two-tailed paired t tests; n = 12 subjects).
Figure 5.
Figure 5.
Top row, Topographical distribution of slow-wave parameters for DEs (first row) and NEs (second row). Slow-wave parameters were averaged over the last 60 s before the awakening and across 12 subjects. In the third row, the mean differences between dream experiences (DEs) and no experiences (NEs) (DE − NE) are shown for each parameter, so that red colors indicate higher values in DE, and blue colors higher values in NE. In the fourth row, p values for paired electrode-by-electrode t tests are shown (p < 0.05, uncorrected). Here only slow waves larger than the 75th amplitude percentile were included for each subject.
Figure 6.
Figure 6.
Top row, Topographical distribution of t values for the contrast between dream experiences and dream experiences without recall of content for different slow-wave parameters averaged over the last 60 s before the awakening. For each subject, only slow waves larger than the 75th amplitude percentile were included. Bottom row, Same as the top row, but electrodes within a cluster showing a statistically significant effect are marked in white (p < 0.05, cluster-based correction for multiple comparisons; n = 14 subjects).
Figure 7.
Figure 7.
Correlation between slow-wave amplitude in a frontal and occipital region of interest for two representative subjects. Top row, All slow waves (no amplitude threshold). Bottom row, An amplitude threshold (above the 75th percentile of all waves for each subject) was applied to frontal slow waves.
Figure 8.
Figure 8.
Type I and type II slow-wave characteristics. A, Proportion of slow waves classified as type I (left) or type II (right) based on synchronization efficiency that were also defined as large based on the channel-by-channel amplitude criterion (>75th percentile; for comparison, slow waves were identified in a 250 ms time window centered on the peak of the type I/II slow wave). Each bar in the graph represents the average (%) across subjects ± SD. B, Type I/type II ratio for the 60 s preceding DE, DEWR, and NE (mean and SEM). Asterisks indicate statistically significant differences at p < 0.05 (paired two-tailed t tests). C, Correlation between low-frequency spectral power in the 1–4 Hz range (in the 6 s preceding the slow wave) and the synchronization index (reflecting slow-wave amplitude and slope) for type I and type II slow waves (Spearman rank correlation coefficient). Type I and type II slow waves were separated according to their synchronization index (for details, see Materials and Methods). Electrodes within a cluster showing a statistically significant effect are marked in white (p < 0.05, cluster-based correction for multiple comparisons). D, Spectral power changes (%) induced by type I and type II slow waves in a frontal electrode cluster (Fz and immediately neighboring electrodes). Spectral power in the 6 s following the slow wave was compared with spectral power in the 6 s preceding each slow wave for different frequency bands (1–40 Hz; resolution of 2 Hz bins). Bottom row, p Values for the comparison between PSD changes induced by type I and type II slow waves (paired two-tailed t tests). E, Cortical distribution of spectral power changes in the 18–30 Hz for type I slow waves at the source level.
Figure 9.
Figure 9.
Representative examples of high-frequency increases following type I slow waves. Time 0 corresponds to the maximum negative peak of the type I slow wave. Four representative midline channels are displayed [Fz (frontal), Cz (central), Pz (parietal), and Oz (occipital)], referenced to the average of two mastoid channels.
Figure 10.
Figure 10.
Topographical distribution of t values for the contrast in 18–30 Hz changes induced by type I slow waves between dream experiences (DEs), no experiences (NEs) (left), DE and dream experiences without recall of content (DEWR) (middle), and DEWR and NE (right), averaged over the last 60 s before the awakening. Electrodes within a cluster showing a statistically significant effect are marked in white (p < 0.05, cluster-based correction for multiple comparisons, two-tailed paired t tests: n = 12 subjects for DE; n = 11 subjects for NE; n = 13 subjects for DEWR).
Figure 11.
Figure 11.
Top row, Topographical distribution of t values for the contrast between dream experiences and no experiences for different spindle parameters (60 s before awakening). Electrodes within a cluster showing a statistically significant effect are marked in white (p < 0.05, cluster-based correction for multiple comparisons, two-tailed paired t tests; n = 12 subjects) are marked in white. Bottom row, Same as the top row for dream experiences without recall of content vs no experience.
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