Recalling and forgetting dreams: theta and alpha oscillations during sleep predict subsequent dream recall

Abstract

Under the assumption that dream recall is a peculiar form of declarative memory, we have hypothesized that (1) the encoding of dream contents during sleep should share some electrophysiological mechanisms with the encoding of episodic memories of the awake brain and (2) recalling a dream(s) after awakening from non-rapid eye movement (NREM) and rapid eye movement (REM) sleep should be associated with different brain oscillations. Here, we report that cortical brain oscillations of human sleep are predictive of successful dream recall. In particular, after morning awakening from REM sleep, a higher frontal 5-7 Hz (theta) activity was associated with successful dream recall. This finding mirrors the increase in frontal theta activity during successful encoding of episodic memories in wakefulness. Moreover, in keeping with the different EEG background, a different predictive relationship was found after awakening from stage 2 NREM sleep. Specifically, a lower 8-12 Hz (alpha) oscillatory activity of the right temporal area was associated with a successful dream recall. These findings provide the first evidence of univocal cortical electroencephalographic correlates of dream recall, suggesting that the neurophysiological mechanisms underlying the encoding and recall of episodic memories may remain the same across different states of consciousness.

Figure 1.

REM sleep. A, One 20 s segment of the PSG recording of tonic REM sleep preceding morning awakening. B, The mean proportion of time [P_episode (f)] of the EEG segment shown in A, where oscillations were detected at each frequency in the 0.25–25.00 Hz frequency range. The detection of oscillations has been made by the BOSC detection method (see Materials and Methods) on the 19 EEG electrodes. Error bars denote interlocation variability. Units of frequency are in hertz and are plotted in five logarithmically spaced frequency values.

Figure 2.

Stage 2 sleep. A, One 20 s segment of the PSG recording of stage 2 sleep preceding morning awakening. B, The detection of oscillations in the segment of stage 2 sleep by the BOSC method, as in Figure 1.

Figure 3.

EEG power spectra (mean over all 19 scalp locations, obtained by collapsing EEG power across all the derivations) of EEG activity during REM sleep in the REC (black line) and NREC (gray line) groups. Mean absolute values (expressed in logarithmic scale) are plotted in the frequency range from 0.50 to 24.75 Hz for 0.25 Hz bins. SEs refer to interlocation variability.

Figure 4.

From the left, the first two columns show the topographic distribution of absolute EEG power during REM sleep in the REC group and in the NREC group. The maps were scaled between minimal (min) and maximal (max) power values in the REC and NREC groups. The first column on the right shows topographic statistical EEG power differences (assessed by unpaired t tests) between the REC and NREC groups. Values are expressed in terms of t values: positive t values indicate a prevalence of the REC over the NREC group, and vice versa. The two-tailed level of significance (p ≤ 0.00738) corresponds to t ≥ 2.60. Average values are normalized by total power, color coded, plotted at the corresponding position on the planar projection of the scalp surface, and interpolated (biharmonic spline) between electrodes. The maps are based on the 19 unipolar EEG derivations of the international 10–20 system with averaged mastoid reference. Maps are plotted for the following EEG bands: delta (0.50–4.75 Hz), theta (5.00–7.75 Hz), alpha (8.00–11.75 Hz), sigma (12.00–15.75 Hz), and beta (16.00–24.75 Hz).

Figure 5.

EEG power spectra (mean over all 19 scalp locations, obtained by collapsing EEG power across all the derivations) of EEG activity during stage 2 NREM sleep in the REC (black line) and NREC (gray line) groups. Mean absolute values (expressed in logarithmic scale) are plotted in the frequency range from 0.50 to 24.75 Hz for 0.25 Hz bins. SEs refer to interlocation variability.

Figure 6.

From the left, the first two columns show the topographic distribution of absolute EEG power during stage 2 NREM sleep in the REC and NREC groups. The maps were scaled between minimal (min) and maximal (max) power values in the REC and NREC groups. The first column on the right shows topographic statistical EEG power differences (assessed by unpaired t tests) between the REC and NREC groups. Values are expressed in terms of t values: positive t values indicate a prevalence of the REC over the NREC group, and vice versa. The two-tailed level of significance (p ≤ 0.00447) corresponds to a t ≥ 2.78. Average values are normalized by total power, color coded, plotted at the corresponding position on the planar projection of the scalp surface, and interpolated (biharmonic spline) between electrodes. The maps are based on the 19 unipolar EEG derivations of the international 10–20 system with averaged mastoid reference. Maps are plotted for the following EEG bands: delta (0.50–4.75 Hz), theta (5.00–7.75 Hz), alpha (8.00–11.75 Hz), sigma (12.00–15.75 Hz), and beta (16.00–24.75 Hz).

Figure 7.

The topographic distribution of correlation values (rho values) between the actual number of dreams recalled after morning awakenings with the amount of theta activity in REM sleep (top map) and with alpha activity in stage 2 (bottom map). Values are expressed in terms of rho values: positive rho values indicate the presence of a positive correlation, and vice versa. The alpha level for REM and NREM sleep was, respectively, adjusted to 0.007 (ρ ≥ 0.47) and to 0.004 (ρ ≥ 0.46). Average values were normalized by total power, color coded, plotted at the corresponding position on the planar projection of the scalp surface, and interpolated (biharmonic spline) between electrodes. The maps are based on the 19 unipolar EEG derivations of the international 10–20 system with averaged mastoid reference.

Figure 8.

Mean proportion of time [P_episode (f)] of EEG activity during REM sleep during which oscillations were detected at each frequency in the 0.50–25.00 Hz frequency range. Individual oscillations detected across all frequencies by the BOSC method have been averaged across all subjects, and error bars denote SEM P_episodes (f). Units of frequency are in hertz and are plotted in five logarithmically spaced frequency values. See Materials and Methods for more details on the BOSC method.

Figure 9.

Mean proportion of time [P_episode (f)] of EEG activity during stage 2 sleep during which oscillations were detected by the BOSC method at each frequency in the 0.25–25.00 Hz frequency range, as in Figure 8.

Figure 10.

Theta activity during REM sleep and alpha activity during stage 2 across consecutive sleep cycles. The maps report topographic statistical EEG power differences (assessed by unpaired t tests) between the REC and NREC groups. Values are expressed in terms of t values: positive t values indicate a prevalence of the REC over the NREC group, and vice versa. The two-tailed level of significance (p ≤ 0.003) corresponds to t ≥ 3.34 in the second and third sleep cycles and to t ≥ 3.38 in the fourth sleep cycle for REM sleep; for stage 2, the level of significance (p ≤ 0.004) corresponds to a t ≥ 3.12 in the second and third sleep cycles and to t ≥ 3.13 in the fourth sleep cycle. Average values are normalized by total power, color coded, plotted at the corresponding position on the planar projection of the scalp surface, and interpolated (biharmonic spline) between electrodes. The maps are based on the 19 unipolar EEG derivations of the international 10–20 system with averaged mastoid reference.