6674 • The Journal of Neuroscience, May 4, 2011 • 31(18):6674 – 6683

Behavioral/Systems/Cognitive

Recalling and Forgetting Dreams: Theta and Alpha

Oscillations during Sleep Predict Subsequent Dream Recall
Cristina Marzano,1 Michele Ferrara,2 Federica Mauro,1 Fabio Moroni,1,3 Maurizio Gorgoni,1 Daniela Tempesta,2
Carlo Cipolli,3 and Luigi De Gennaro1,4
1Department of Psychology, University of Rome “Sapienza,” 00185 Rome, Italy, 2Department of Health Sciences, University of L’Aquila, 67010 L’Aquila,

Italy, 3Department of Psychology, University of Bologna, 40127 Bologna, Italy, and 4Associazione Fatebenefratelli per la Ricerca, Department of
Neuroscience, Hosp. Fatebenefratelli, Isola Tiberina, 00186 Rome, Italy

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.

Introduction (Fosse et al., 2003), which is encoded in declarative memory dur-

Although studied extensively in the last 50 years, the brain mech- ing sleep. Two main hypotheses directly descend from this as-
anisms underlying the elaboration of dreaming and its encoding sumption: (1) the encoding of dream content during sleep should
in memory during sleep are as yet primarily unknown, as a con- share some electrophysiological mechanisms with the successful
sequence of two limitations. First, since dreams are not directly encoding of episodic information during wakefulness; and (2)
accessible, the study of dreaming has been restricted to the anal- resulting from the intrinsic electrophysiology of REM and NREM
ysis of mental activity after spontaneous or provoked awakening. sleep, dream recall after awakening from these sleep states should
Second, the study of the brain mechanisms involved in dreaming be associated with different brain oscillations.
has usually been restricted to rapid eye movement (REM) sleep, These hypotheses rely on a large body of experimental evi-
on the basis of the implicit assumption that dreaming is strictly dence. In humans engaged in a learning task, a successful mem-
dependent on its specific physiology. However, dream recall is ory formation is predicted by a tight coordination of spike timing
also obtained after awakening from all non-rapid eye movement with local theta oscillations (Rutishauser et al., 2010). Moreover,
(NREM) stages, with some difference in the frequency and con- evoked potentials and hemodynamic measures of human brain
tent characteristics (Nielsen, 2000; Fagioli, 2002). activity differentiate the encoding of items to be later recalled
In the present investigation, we renounced to study dream from that of items not later recalled (Paller and Wagner, 2002).
reports and their characteristics and focused on the EEG oscilla- Scalp recordings have shown that low-frequency brain oscilla-
tions associated with the presence/absence of dream recall after tions increase during encoding of episodic memories to be later
awakening. The basic assumption is that dream recall regards recalled (Klimesch et al., 1996; Weiss and Rappelsberger, 2000;
such peculiar form of episodic information as dream content Osipova et al., 2006). Intracranial recordings have confirmed that
an increase in frontal theta oscillations during the encoding phase
predicts subsequent recall (Sederberg et al., 2003) and that theta
Received Jan. 25, 2011; revised March 2, 2011; accepted March 13, 2011. oscillations in wakefulness mediate interactions between pre-
Author contributions: C.M., M.F., C.C., and L.D.G. designed research; C.M., F. Mauro, F. Moroni, M.G., and D.T.
performed research; L.D.G. analyzed data; and C.M. and L.D.G. wrote the paper.
frontal cortex and medial temporal lobe in memory encoding
This work was supported by grants from the Compagnia di San Paolo, Programma Neuroscienze 2008/09 (3889 (Anderson et al., 2010).
SD/sd, 2008.1300 to L.D.G.) and Fondazione CARISBO (2010.0139 to C.C. and F. Moroni). We thank Clayton Dickson Keeping in mind the main EEG difference between REM and
and Jeremy Caplan for providing the libraries for the BOSC detection method. NREM sleep, we attempted to identify which specific electroen-
Correspondence should be addressed to Luigi De Gennaro, Department of Psychology, Section of Neuroscience,
University of Rome “Sapienza,” Via dei Marsi, 78, 00185 Rome, Italy. E-mail: [email protected].
cephalographic activity within localized cortical areas is associ-
DOI:10.1523/JNEUROSCI.0412-11.2011 ated with dream recall after awakening from different sleep
Copyright © 2011 the authors 0270-6474/11/316674-10$15.00/0 stages. Concerning REM sleep, we expected that a higher frontal
Marzano et al. • EEG Oscillations Predict Dream Recall J. Neurosci., May 4, 2011 • 31(18):6674 – 6683 • 6675

theta activity should be associated with the awakenings followed Table 1. Means and SEs of the PSG variables of the REC and NREC groups awakened
by successful dream recall compared with those with recall fail- from REM sleep
ure. Indeed, a recent investigation has shown that the extent of REC NREC
postsleep facilitation for emotional memory is correlated with Variables Mean SE Mean SE F(1,28) p
prefrontal theta oscillations only during REM sleep (Nishida et
al., 2009). Stage 1 latency (min) 7.32 1.55 9.47 2.35 0.61 0.44
Stage 2 latency (min) 11.11 2.32 13.27 2.37 0.34 0.56
According to previous observations (Esposito et al., 2004), we REM latency (min) 84.78 6.87 86.00 11.36 0.009 0.92
expected that a successful recall after awakening from NREM Stage 1 (%) 6.28 0.68 6.64 1.18 0.08 0.78
stage 2 should be associated with a lower alpha power compared Stage 2 (%) 60.00 1.39 59.26 1.54 0.11 0.74
with awakening with no dream recall, larger in corresponding SWS (%) 10.54 1.62 8.16 1.45 0.89 0.35
temporo-parietal areas. REM (%) 23.17 0.88 25.94 1.70 2.58 0.12
Here, we report that a higher frontal theta activity during WASO (min) 32.01 8.42 23.56 4.10 0.47 0.50
TST (min) 443.30 9.32 435.27 8.79 0.30 0.59
REM sleep and a lower alpha activity of the right temporal region SEI % (TST/TBT) 91.98 1.63 92.87 1.08 0.13 0.72
during NREM sleep actually predict successful dream recall after
The results of the one-way ANOVA are also reported.
awakening. Both these findings are further strengthened by the
significant correlations between the number of recalled dreams
and these stage-specific brain oscillations during sleep. Table 2. Means and SEs of the PSG variables of the REC and NREC groups awakened
from stage 2
REC NREC
Materials and Methods Variables Mean SE Mean SE F(1,33) p
Subjects
Data for this analysis were obtained by selecting an ad hoc sample of 65 Stage 1 latency (min) 8.89 2.08 9.51 2.94 0.03 0.86
university students [35 males (M) and 30 females (F); mean age, 23.6 ⫾ Stage 2 latency (min) 12.93 2.44 16.02 4.50 0.41 0.52
2.1 years] from the database of our laboratory. Subjects were selected REM latency (min) 91.64 6.09 87.09 9.34 0.18 0.67
from those who participated to distinct protocols (De Gennaro et al., Stage 1 (%) 11.92 5.26 7.17 0.88 0.60 0.44
2008, 2010; C. Marzano, M. Ferrara, F. Moroni, and L. De Gennaro, Stage 2 (%) 61.77 1.62 58.60 1.82 1.69 0.20
unpublished observations), on the basis of the following study-specific SWS (%) 9.50 1.49 10.57 1.67 0.23 0.64
criteria: (1) polysomnographic (PSG) recordings of 2 consecutive nights REM (%) 21.81 1.07 23.66 1.27 1.24 0.27
(for adaptation and baseline, respectively) of undisturbed sleep; (2) the WASO (min) 31.51 4.74 40.44 9.29 0.84 0.36
TST (min) 441.72 6.20 437.00 14.43 0.07 0.80
collection of a sleep and dream diary (see below) after morning awaken-
SEI % (TST/TBT) 88.94 1.98 88.43 2.41 0.03 0.87
ing in the second night; and (3) the absence of stage shifts in the last 5 min
of sleep preceding the provoked awakening at the end of the second The results of the one-way ANOVA are also reported.
night.
Additionally, the subjects had to meet the following general criteria: estimate). To this aim, subjects had been preliminarily (i.e., at the end of
normal sleep duration and schedule; no daytime nap habits; no excessive the adaptation night) instructed to consider any distinct mental activity
daytime sleepiness; no other sleep, medical, or psychiatric disorder (as occurring during sleep with one or more perceptually vivid contents as a
assessed by a 1 week sleep log and by a clinical interview); a habitual sleep dream.
time between 12:00 A.M. and 8:00 A.M. plus or minus 1 h; and an average Of 35 subjects awakened from stage 2 sleep, 20 were successful in
sleep duration of 7.5 ⫾ 1 h hours per night. dream recall [recallers (REC); mean number of recalled dreams, 1.65; SE,
In such a way, we considered 35 (16 M and 19 F) subjects awakened 0.17] and 15 were not successful [nonrecallers (NREC)]. Of 30 subjects
from stage 2 sleep and 30 (19 M and 11 F) from REM sleep, also taking awakened from REM sleep, 20 were dream REC (mean number of re-
into consideration the need to have comparable sizes for the groups called dreams, 1.32; SE, 0.13) and 10 were NREC. These recall rates were
recalling and nonrecalling dreams after either REM or stage 2 sleep. slightly different from the normative values of dream recall after morning
The protocol of the present study was approved by the local Institu- awakening from REM and stage 2 sleep (Nielsen, 2000), because of the
tional Ethics Committee and was conducted in accordance with the Dec- constrains of the current experimental design (mainly, the need to have
laration of Helsinki. All subjects had previously given their written comparable sample sizes and the absence of stage shifts over the last 5 min
informed consent for the collection and treatment of data. of sleep). Actually, the dream recall rates in the original database (De
Gennaro et al., 2008; 2010; Marzano, Ferrara, Moroni, and De Gennaro,
Procedure
For each subject, a polysomnogram was recorded in a sound-proof, unpublished observations) were 69% for the REM awakenings and 51%
temperature-controlled room after an adaptation night. Hence, the for the stage 2 awakenings.
recordings were obtained during second nights in the sleep labora- PSG recordings
tory, and any procedural aspect was completely identical to the first A VEGA 24 polygraph (Esaote Biomedica) was used for polygraphic
adaptation night. The subjects’ sleep was undisturbed, started at 12:00 recordings. EEG signals were analogically high-pass filtered with a time
A.M., and ended after ⬃7.5 h of accumulated sleep. Awakenings were constant of 0.3 s and low-pass filtered at 30 Hz. The 19 unipolar EEG
scheduled from stage 2 sleep (n ⫽ 35) or from REM sleep (n ⫽ 30) derivations of the international 10 –20 system (Fp1, Fp2, F7, F8, F3, F4,
after at least 5 min without stage shifts (by calling out his/her name Fz, C3, C4, Cz, P3, P4, Pz, T3, T4, T5, T6, O1, O2) were recorded from
and entering in the sleep room). The decision to wake up the subject scalp electrodes with averaged mastoid reference.
was taken by the sleep researcher who examined PSG recording on- The submental EMG was recorded with a time constant of 0.03 s.
line, and the absence of stage shifts over the last 5 min of sleep was Bipolar horizontal eye movements were recorded with a time con-
then confirmed by an independent expert, who off-line scored PSG stant of 1 s. The bipolar horizontal electrooculogram (EOG) was
recording. recorded from electrodes placed about 1 cm from the medial and
Just after morning awakening, subjects were requested to fill out a lateral canthi of the dominant eye. Impedance of these electrodes was
sleep and dream diary (De Gennaro et al., 2010), to collect subjective kept below 5 k⍀.
estimates of sleep characteristics (sleep onset latency, number of awak-
enings, total sleep time, sleep quality) and of dream recall, namely the Data analysis
feeling of having or having not dreamt (as a qualitative estimate) and the Polysomnography. Sleep stages were visually scored according to the stan-
number of recalled dreams of the preceding night (as a quantitative dard criteria (Rechtschaffen and Kales, 1968), and slow-wave sleep
6676 • J. Neurosci., May 4, 2011 • 31(18):6674 – 6683 Marzano et al. • EEG Oscillations Predict Dream Recall

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 [Pepisode (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.

(SWS) scoring strictly followed the ⬎75 ␮V amplitude criterion. The To ascertain whether REC and NREC subjects differed with respect
following sleep parameters were considered as dependent variables: (1) to one or more PSG measures, we performed one-way ANOVAs sep-
stage 1 latency; (2) stage 2 latency; (3) REM latency; (4) total sleep time arately for the two groups with awakening from REM or stage 2
(TST), defined as the sum of time spent in stage 1, stage 2, SWS, and NREM sleep.
REM; (5) sleep efficiency index (SEI ⫽ TST/total bed time (TBT) ⫻ Data processing and statistics. The polygraphic signals (19 EEG chan-
100); (6) percentage of each sleep stage (time spent in a sleep stage/ nels, an EMG, and an EOG) of the 5 min of sleep preceding the morning
TST); and (7) wakefulness after sleep onset (WASO), expressed as the awakening were analog-to-digital converted on-line with a sampling rate
intrasleep time (minutes) spent awake. of 128 Hz and stored on the disk of a personal computer. Artifacts were
Marzano et al. • EEG Oscillations Predict Dream Recall J. Neurosci., May 4, 2011 • 31(18):6674 – 6683 • 6677

excluded off-line on an 8 s basis by visual inspection; with regard to REM

sleep, only tonic periods were included in the analyses, to avoid artifacts
from rapid eye movements on EEG power. Power spectra of the 19 der-
ivations were computed by a fast Fourier transform (FFT) routine for
consecutive 4 s epochs, resulting in a frequency resolution of 0.25 Hz.
Values above 25 Hz were not used in the analysis.
Power EEG data at this frequency resolution were first averaged over
all electrodes to provide a synthetic picture of EEG spectra as a function
of the different conditions (REC and NREC awakened from REM sleep
and from stage 2 NREM sleep).
Then, adjacent 0.25 Hz bins (0.50 –25 Hz) were collapsed, reducing
power EEG data to the following 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). The EEG power values for each frequency band
were considered as dependent measures for the statistical analyses. For
graphical purposes, these values were normalized by total power of the
recording, color coded, plotted at the corresponding position on the
planar projection of the scalp surface, and interpolated (biharmonic
spline) between electrodes.
EEG power maps were computed separately for REM and stage 2 sleep,
and statistical comparisons (unpaired t tests) were performed on log- Figure 3. EEG power spectra (mean over all 19 scalp locations, obtained by collapsing EEG
transformed values between REC and NREC groups, separately for the power across all the derivations) of EEG activity during REM sleep in the REC (black line) and
two sleep stages. To adjust ␣ value for multiple comparisons, the Bon- NREC (gray line) groups. Mean absolute values (expressed in logarithmic scale) are plotted in
ferroni correction was applied taking into account the mean correlation the frequency range from 0.50 to 24.75 Hz for 0.25 Hz bins. SEs refer to interlocation variability.
between the dependent variables (Perneger, 1998; Sankoh et al., 1997).
According to this procedure, we calculated the mean correlation between
the dependent variables in REM (r ⫽ 0.58) and NREM (r ⫽ 0.47) sleep. a 5 min sleep was termed Pepisode (Caplan and Glaholt, 2007; Caplan et
Considering this mean correlation and the number of statistical compar- al., 2001, 2003; van Vugt et al., 2007).
isons (95 t tests), ␣ value was adjusted to 0.007 (t ⱖ 2.60) for REM and to The BOSC is a robust detection method that has been successfully used
0.004 (t ⱖ 2.78) for NREM statistical comparisons. to identify and quantify theta oscillations in the human neocortex (Ca-
Aimed to confirm the results of the t maps, the existence of significant plan and Glaholt, 2007; Caplan et al., 2001, 2003) and hippocampus
changes of theta activity in the comparisons between REC and NREC (Ekstrom et al., 2005), which were correlated with memory encoding and
subjects during REM sleep localized over the frontal region also has been retrieval. Here, the Pepisode measure provided by the BOSC method at
evaluated by a 2 ⫻ 5 ⫻ 19 mixed design, group (REC vs NREC) ⫻ band each frequency [Pepisode (f )] was used to detect the oscillatory activity
(delta, theta, alpha, sigma, beta) ⫻ scalp location (the 19 derivations of within those electrodes and EEG bands that had previously found to
the 10 –20 international system) ANOVA on log-transformed EEG predict the presence of dream recall after awakening from REM and stage
2 on the basis of the FFT analysis.
power values. Separate ANOVAs have been performed for REM and
As a final control, we checked whether the results on the final 5 min of
stage 2 sleep.
sleep represent a pattern fairly stable over the night. In fact, our choice of
Then, to strengthen the results of the FFT analysis, we also applied an
studying EEG activity just preceding final morning awakening was
oscillation detection method to the EEG signals. Indeed, the presence of
mainly attributable to methodological reasons: (1) to more easily assume
a spectral peak resulting from a Fourier transform of the EEG signal does
a quasi-stationarity of EEG signals; (2) to be closer to the time in which
not necessarily imply an underlying oscillatory activity at that frequency,
dream was retrieved; (3) to avoid the potential confound of the effects of
given that nonoscillatory and transient signals can produce power
homeostatic and ultradian factors on EEG changes across a night sleep.
changes at specific frequencies. For this reason, we also applied the better
Nevertheless, as a consequence of this methodological choice, it may
oscillation (BOSC) detection method to the EEG signals. The BOSC is a remain unclear whether any association between sleep EEG oscillations
method, introduced by Caplan et al. (2001) and recently revised by Whit- and dream recall applies only to a short interval preceding awakening or
ten et al. (2010), that is aimed to detect oscillatory activity within a signal whether it represents an interindividual pattern that may be detected
containing a nonrhythmic portion. This method detects oscillatory ac- throughout the night. To specifically address this question, 5 min EEG
tivity in EEG signals by taking into account the functional form of a segments were selected around the midpoint of three episodes of REM
“background,” nonrhythmic portion of the signal and revealing seg- sleep and stage 2 during the course of the night. To this aim, we consid-
ments of the recording that deviate significantly from the spectral char- ered the second, third, and fourth sleep cycles (i.e., NREM–REM cycles).
acteristics of the background. The first cycle was discarded because its short duration and the stage
The analysis was performed separately at each frequency of interest (in shifts of the first REM period did not allow us to fulfill the criterion of a
the 0.50 –25 Hz range) and each electrode. For a given frequency, an continuous 5 min segment in the middle of the sleep cycle. The fourth
oscillatory episode was defined as an epoch longer than a duration sleep episode was also not considered in the cases in which the 5 min
threshold, DT (set to three cycles in our analysis) during which wavelet central EEG segment would have been partly overlapped with the final 5
power at frequency exceeded a power threshold (pT). This PT was chosen min interval before the final awakening. Therefore, the entire subject
as follows in the 5 min segments. (1) The EEG was wavelet transformed sample was included in the analyses on the second and the third sleep
(Morlet wavelet, window of 6 cycles) at 47 logarithmically spaced fre- cycles, whereas 22 subjects (15 REC and 7 NREC) were considered for
quencies in the range 0.50 –25 Hz. The average of the log-transform of the analyses on the fourth REM sleep episode and 33 subjects (19 REC
these wavelet values yielded the wavelet power spectrum. (2) The back- and 14 NREC) were considered for those on the fourth stage 2 epi-
ground noise spectrum assumed the form Power(f ) ⫽ Af ⫺␣. The esti- sode. Sleep cycles were defined according to standard criteria (Fein-
mate of this background has been obtained by fitting the observed berg and Floyd, 1979).
spectrum (at each electrode) with a linear regression in log–log units. The EEG power maps have been computed separately for REM and stage 2
background at f * has been estimated on the mean of its corresponding sleep, and statistical comparisons (unpaired t tests) have been performed
␹ 2(2) probability distribution function. The power threshold (pT) was set on log-transformed values between REC and NREC groups, separately
to the 95th percentile of the theoretical probability distribution. The for the two sleep stages and for the three sleep cycles. Considering the
proportion of time in which significant oscillations were detected within mean correlation between dependent variables in REM (r ⫽ 0.30) and
6678 • J. Neurosci., May 4, 2011 • 31(18):6674 – 6683 Marzano et al. • EEG Oscillations Predict Dream Recall

NREM sleep (r ⫽ 0.36), and the number of

statistical comparisons (57 t tests), ␣ value was
adjusted to 0.003 (t ⱖ 3.24 for second and third
cycles; t ⱖ 3.38 for fourth cycle) for REM sleep
and to 0.004 (t ⱖ 3.12 for second and third
cycles; t ⱖ 3.13 for fourth cycle) for stage 2
NREM sleep statistical comparisons.

Results
PSG measures do not differ in REC and
NREC groups
Tables 1 and 2, respectively, report the re-
sults of the univariate ANOVAs compar-
ing the values of PSG measures in the REC
and NREC groups, awakened from REM
and stage 2 sleep. Comparisons do not
show significant changes for any consid-
ered measure. This means that there were
no substantial differences in the sleep archi-
tecture of the subjects grouped as a function
of sleep stage at awakening (REM/stage 2)
and dream recall (success/failure).

Sleep EEG topography before

awakening discriminates between
recalling and nonrecalling dreams
after awakening
A representative segment of REM sleep
without eye movements is depicted in Fig-
ure 1 A, and theta oscillations are evident
at more anterior regions. As shown by the
BOSC detection analysis on this segment
of the last 5 min EEG preceding awaken-
ing, theta oscillations dominate this seg-
ment (Fig. 1 B).
Similarly, Figure 2 shows a typical
segment of stage 2 preceding awakening
(A), dominated by oscillations in the
range of the delta, alpha, and sigma fre-
quency (B).
Figure 4. From the left, the first two columns show the topographic distribution of absolute EEG power during REM sleep in the
REM sleep REC group and in the NREC group. The maps were scaled between minimal (min) and maximal (max) power values in the REC and
The typical EEG spectrum of REM sleep is NREC groups. The first column on the right shows topographic statistical EEG power differences (assessed by unpaired t tests)
depicted in Figure 3, which reports EEG between the REC and NREC groups. Values are expressed in terms of t values: positive t values indicate a prevalence of the REC over
power values (0.50 –24.75 Hz) of REC and the NREC group, and vice versa. The two-tailed level of significance (p ⱕ 0.00738) corresponds to t ⱖ 2.60. Average values are
NREC groups, obtained by collapsing normalized by total power, color coded, plotted at the corresponding position on the planar projection of the scalp surface, and
power values across all the derivations. interpolated (biharmonic spline) between electrodes. The maps are based on the 19 unipolar EEG derivations of the international
An inspection of the figure suggests that 10 –20 system with averaged mastoid reference. Maps are plotted for the following EEG bands: delta (0.50 – 4.75 Hz), theta
EEG activity of the two groups mostly (5.00 –7.75 Hz), alpha (8.00 –11.75 Hz), sigma (12.00 –15.75 Hz), and beta (16.00 –24.75 Hz).
overlaps, with a notable exception for a
range of frequencies encompassing up- A 2 ⫻ 19 ⫻ 5 mixed-model ANOVA, condition (REC vs
per delta and lower theta activity (from 3.25 to 6.75 Hz). NREC) ⫻ electrode ⫻ band (delta, theta, alpha, sigma, beta),
The topographic distribution of EEG power, illustrated on the pointed to a significant condition ⫻ electrode ⫻ band interaction
left side of Figure 4, depicts EEG power maps for each frequency (f(1,18) ⫽ 1.50; p ⬍ 0.005). This interaction suggests that the mag-
band, scaled between the maximum and minimum values, in the nitude of the differences between REC versus NREC changes as a
REC and NREC groups; maps of statistical differences between function of both EEG bands and electrodes. In fact, the topo-
groups are also reported on the right side of Figure 4. The data of graphic distribution of statistical comparisons (t values), illus-
maxima and minima exhibited the typical features of power spec- trated in the right side of Figure 4, allows assessing for which
tra during REM sleep (Marzano et al., 2010). The delta and theta electrode and band the two groups significantly differ. These sta-
bands exhibit a fronto-central midline predominance of power tistical maps point to a significant difference only for the theta
and minimum values over the temporal regions, whereas the power: REC showed higher power values than NREC subjects
highest values of the alpha band are seen at the parietal-occipital in the corresponding Fz scalp location (t(28) ⫽ 3.28; two-tailed
midline areas. p ⫽ 0.0028).
Marzano et al. • EEG Oscillations Predict Dream Recall J. Neurosci., May 4, 2011 • 31(18):6674 – 6683 • 6679

Stage 2 NREM
The typical EEG spectrum of NREM sleep is depicted in Figure 5,
which reports EEG power values (0.50 –24.75 Hz) of the REC and
NREC groups, obtained by collapsing EEG power across all der-
ivations. An inspection of the Figure 5 suggests that EEG activity
of the two groups diverges for a range of frequencies mostly en-
compassing the alpha and sigma bands.
Again, the topographic distributions of EEG power, illus-
trated in Figure 6, show the comparison of regional differences
between the two groups. Figure 6 depicts EEG power maps of
REC and NREC groups for each frequency band, scaled between
the maximum and minimum values, and the statistical maps of
the between-group differences. The topographic distributions
point to stable patterns within different frequency bands. Data of
maxima and minima exhibited the typical features of power spec-
tra during NREM sleep, with a fronto-central midline predomi-
nance of delta, theta, and alpha bands and minimum values over
the temporal regions [consistently with previous observations
(Finelli et al., 2001; Marzano et al., 2010)], whereas the sigma
band confirms centro-parietal maxima (De Gennaro and Fer- Figure 5. EEG power spectra (mean over all 19 scalp locations, obtained by collapsing EEG
rara, 2003). These regional patterns are roughly maintained in power across all the derivations) of EEG activity during stage 2 NREM sleep in the REC (black line)
the REC and NREC groups. and NREC (gray line) groups. Mean absolute values (expressed in logarithmic scale) are plotted
A 2 ⫻ 19 ⫻ 5 mixed-model ANOVA, condition (REC vs in the frequency range from 0.50 to 24.75 Hz for 0.25 Hz bins. SEs refer to interlocation
NREC) ⫻ electrode ⫻ band (delta, theta, alpha, sigma, beta), did variability.
not show a significant condition ⫻ electrode ⫻ band interaction
(f(1,18) ⫽ 0.32; p ⫽ 0.99). The inspection of the left side of Figure
6 suggests a high similarity of the whole EEG maps of the alpha the 19 ones in NREM sleep was, respectively, adjusted to 0.007
and sigma bands, and a comparable right temporo-parietal de- (␳ ⱖ 0.47) and to 0.004 (␳ ⱖ 0.46).
crease associated with dream recalling across theta, alpha, and Figure 7 illustrates topographically (i.e., across all electrodes)
sigma bands. Likely, these regional patterns across some fre- these correlations. The number of dreams recalled after morning
quency bands had precluded the significance of the higher-order awakening was associated positively with the amount of theta
interaction, and we then performed a separate 2 ⫻ 19, condi- activity in REM sleep (Fig. 7, top) and negatively with alpha ac-
tion ⫻ electrode ANOVA for each frequency band. The crucial tivity in stage 2 (Fig. 7, bottom). Significant correlations strictly
condition ⫻ electrode interaction was not significant for the overlapped the results of between-group analyses: the positive
delta, theta, and beta bands (delta: F(1,18) ⫽ 0.31, p ⫽ 0.99; theta: relationship with theta activity in REM was significant only at the
F(1,18) ⫽ 0.59, p ⫽ 0.91; beta: F(1,18) ⫽ 0.71, p ⫽ 0.80); approached Fz site (␳ ⫽ 0.47; p ⫽ 0.007), whereas the negative relationship
to significance for the sigma band (f(1,18) ⫽ 1.37; p ⫽ 0.14); and with alpha activity in stage 2 was significant only at the T4 site
was significant for the alpha band (f(1,18) ⫽ 1.97; p ⫽ 0.009). This (␳ ⫽ ⫺0.49; p ⫽ 0.004).
means that the statistical maps on the right side of Figure 6 point
to a significant difference only for the alpha power: REC showed Oscillatory or “background” EEG activity?
lower power values than NREC subjects in the corresponding T4 Since the FFT does not allow the discrimination between back-
scalp location (t(28) ⫽ ⫺3.48; two-tailed p ⫽ 0.001). A similar ground EEG activity and an oscillatory (rhythmic) activity, we
difference, albeit not significant after the correction for multiple applied the BOSC detection method to the 5 min EEG segments
testing, is apparent for the sigma activity at T4 and P4 sites and for of REM sleep or stage 2 sleep preceding the final awakening. On
the alpha activity at the P4 site (in all cases, p ⫽ 0.01). the basis of the above reported results, this analysis was per-
To summarize, the patterns of statistical comparisons for formed on the Fz recordings during REM sleep and on the T4
REM and stage 2 sleep showed that REC and NREC groups can be recordings during stage 2 sleep.
discriminated on the basis of the theta activity at Fz in REM sleep BOSC analysis clearly showed that EEG activity of the pre-
and the alpha activity at T4 in stage 2 NREM sleep. awakening segments of REM sleep contains specific oscillatory
activities, mainly theta and beta (Fig. 8). Theta oscillations pre-
dominated in this 5 min of REM sleep EEG, with a mean peak of
The increase in theta power in REM sleep and the decrease in Pepisode at 6.5 Hz and an averaged 26% of time elapsed in this
alpha power in stage 2 also predict the number of recalled oscillatory activity. The individual maximal Pepisode values of
dreams these oscillations range from 4.9 to 7.5 Hz. In corresponding
To further support the hypothesis of a direct link between EEG frequencies, theta oscillations are present in the 5 min EEG seg-
activity preceding awakening and presence/absence of dream re- ment for 9.5– 40.9% of the time.
call, we examined also whether the number of recalled dreams is During stage 2 sleep, preawakening EEG segments mainly
predicted by the theta power after awakening from REM sleep contained three oscillatory activities, delta, alpha, and sigma (Fig.
and by the alpha power after awakening from stage 2 of NREM 9), with alpha and sigma oscillations essentially predominant.
sleep, respectively. Alpha oscillations show a mean peak of Pepisode at 8.5 Hz and an
Significance of these Spearman correlation coefficients was averaged 23% of time in this oscillatory activity. The individual
evaluated against the null hypothesis of ␳ ⫽ 0 in the general maximal Pepisode values of these oscillations range from 7.5 to 11.3
population. The alpha level for the 19 correlations in REM and Hz. In corresponding frequencies, alpha oscillations are present
6680 • J. Neurosci., May 4, 2011 • 31(18):6674 – 6683 Marzano et al. • EEG Oscillations Predict Dream Recall

in the individual 5 min EEG segments for

6.8 –55.9% of the time. Sigma oscillations
exhibit a mean peak at 13.0 Hz and an
averaged 22% of time in this oscillatory
activity. The individual maximal Pepisode
values range from 12.1 to 14.9 Hz. In cor-
responding frequencies, sigma oscilla-
tions are present in the individual 5 min
EEG segments for 6.2–33.6% of the time.

Trait-like differences or
state-like differences?
To address the question of whether the
predictive relationships between theta os-
cillations in REM sleep, alpha oscillations
in stage 2 sleep, and dream recall apply
only to the 5 min EEG segments before
awakening or represent stable patterns
over the night, we also examined EEG seg-
ments selected around the midpoint of
the second, third, and fourth episodes of
REM sleep and stage 2 NREM (see Mate-
rials and Methods).
The topographic distributions of sta-
tistical comparisons (t values) across sleep
cycles regarding theta power in REM sleep
and alpha power in stage 2 sleep are re-
ported in Figure 10. No difference was sig-
nificant after the correction for multiple
comparisons. However, it seems worth
pointing out that theta power was
higher in REC compared with NREC
subjects during REM sleep at Fz (t(20) ⫽
3.01; two-tailed p ⫽ 0.007), T6 (t(20) ⫽
3.30; two-tailed p ⫽ 0.004), and O2
(t(20) ⫽ 3.27; two-tailed p ⫽ 0.004) in
the fourth sleep episode, whereas no sta-
tistical comparison during stage 2 was
close to significance.
According to the specific aims of these
analyses, we also calculated the effect sizes Figure 6. From the left, the first two columns show the topographic distribution of absolute EEG power during stage 2 NREM
(Cohen’s d coefficients) for the REC ver- sleep in the REC and NREC groups. The maps were scaled between minimal (min) and maximal (max) power values in the REC and
sus NREC comparisons at Fz in REM NREC groups. The first column on the right shows topographic statistical EEG power differences (assessed by unpaired t tests)
sleep and at T4 in stage 2 sleep. These co- 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 ⱕ 0.00447) corresponds to a t ⱖ 2.78. Average values are
efficients showed a relative increase of the normalized by total power, color coded, plotted at the corresponding position on the planar projection of the scalp surface, and
differences between REC versus NREC interpolated (biharmonic spline) between electrodes. The maps are based on the 19 unipolar EEG derivations of the international
in the EEG segment preceding the final 10 –20 system with averaged mastoid reference. Maps are plotted for the following EEG bands: delta (0.50 – 4.75 Hz), theta
awakening compared with the other (5.00 –7.75 Hz), alpha (8.00 –11.75 Hz), sigma (12.00 –15.75 Hz), and beta (16.00 –24.75 Hz).
sleep episodes (Cohen’s d coefficients
for REM sleep: second sleep episode,
0.79; third sleep episode, 0.61; fourth sleep episode, 1.41; Co- dictive power of frontal theta activity in REM sleep and of right
hen’s d coefficients for stage 2 sleep: second sleep episode, temporal alpha activity in NREM sleep for dream recall.
0.86; third sleep episode, 0.89; fourth sleep episode, 1.09). Although the identification of oscillatory activity in quasi-
stationary EEG traces (i.e., in a relatively short interval, in which
Discussion the parameters of interest vary minimally) is still an open ques-
Our results provide a clear electrophysiological evidence that tion, theta and alpha power values extracted by the FFT, respec-
stage-specific cortical brain oscillations in the 5 min of sleep be- tively, in REM and stage 2 NREM sleep actually appear to subtend
fore morning awakening are predictive of a successful dream re- an oscillatory activity. As a matter of fact, the BOSC detection
call. A higher frontal theta activity predicts successful dream method confirmed that a large part of EEG segments of REM
recall after awakening from REM sleep, as well as a lower alpha sleep and stage 2 before morning awakening contains theta and
oscillatory activity of the right temporal area after awakening alpha oscillations, respectively.
from stage 2 NREM sleep. Moreover, the significant correlations Together, the changes of cortical oscillatory activity during
with the estimated number of recalled dreams confirm the pre- sleep localized over the frontal and temporo-occipital regions
Marzano et al. • EEG Oscillations Predict Dream Recall J. Neurosci., May 4, 2011 • 31(18):6674 – 6683 • 6681

Figure 9. Mean proportion of time [Pepisode (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 7. The topographic distribution of correlation values (rho values) between the actual It is of note that the cortical regions whose oscillatory activity
number of dreams recalled after morning awakenings with the amount of theta activity in REM predicts dream recall are reminiscent of those involved in the
sleep (top map) and with alpha activity in stage 2 (bottom map). Values are expressed in terms global cessation of dreaming after brain injuries. The largest in-
of rho values: positive rho values indicate the presence of a positive correlation, and vice versa. vestigation on 361 brain-damaged patients (Solms, 1997, 2000)
The alpha level for REM and NREM sleep was, respectively, adjusted to 0.007 (␳ ⱖ 0.47) and to
showed that global cessation of dreaming follows a lesion of two
0.004 (␳ ⱖ 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 (bihar- different cortical regions: (1) the temporoparieto-occipital junc-
monic spline) between electrodes. The maps are based on the 19 unipolar EEG derivations of the tion, more often unilaterally than bilaterally (Solms, 2000); and
international 10 –20 system with averaged mastoid reference. (2) white matter tracts surrounding the frontal horns of the lat-
eral ventricles, underlying ventromedial prefrontal cortex, more
often bilaterally than unilaterally (Solms, 1997).

The continuity hypothesis

The present findings confirm the basic assumption that the neu-
rophysiological mechanisms of encoding and recall of episodic
memories are homogeneous across wake and sleep, but also com-
plement the so-called “continuity hypothesis” of dreaming. This
hypothesis states that (1) qualitative and quantitative aspects of
dreams largely reflect waking-life experience (Domhoff, 2003;
Schredl, 2003; Schredl, 2009) and (2) the likelihood of specific
experiences, thoughts, and feelings of the waking life to be incor-
porated into subsequent dreams is modulated by several factors
[such as emotional involvement, type of waking-life experience,
personality traits, and time of the night (Schredl, 2003, 2009)].
Beyond this essentially psychological perspective, the hypothesis
has been supported by a recent neuroimaging study that showed
direct relationships between volumetric and ultrastructural
Figure 8. Mean proportion of time [Pepisode (f )] of EEG activity during REM sleep during measures of the hippocampus–amygdala complex and specific
which oscillations were detected at each frequency in the 0.50 –25.00 Hz frequency range. qualitative (mainly, emotions and bizarreness) features of
Individual oscillations detected across all frequencies by the BOSC method have been averaged
across all subjects, and error bars denote SEM Pepisodes (f ). Units of frequency are in hertz and are
dreaming (De Gennaro et al., 2010). In fact, the amygdala,
plotted in five logarithmically spaced frequency values. See Materials and Methods for more involved during wakefulness in both control of the encoding
details on the BOSC method. and retrieval of emotional memories and the physical expres-
sion of emotions (Misane et al., 2005), also seems involved in
the access and processing of the emotional sources of dream-
appear indicative of the involvement also in dreaming of those ing (Hobson and Pace-Schott, 2002).
regions, which control successful memory encoding in wak- The current EEG results, in suggesting that the mechanisms
ing. In more general terms, our results suggest that the neuro- involved in encoding and recall of episodic memories across
physiological mechanisms underlying the encoding and recall wakefulness and sleep are the same, undoubtedly strengthen
of episodic memories remain the same across different states the general notion of a continuity between waking and sleep
of consciousness. mentation.
6682 • J. Neurosci., May 4, 2011 • 31(18):6674 – 6683 Marzano et al. • EEG Oscillations Predict Dream Recall

NREM dream recall

Our findings also allow us to further clar-
ify the differences in dream recall after
awakening from NREM and REM sleep.
In our view, the different findings for
REM and NREM sleep are consistent with
both the quantitative (and, probably, also
qualitative) differences in dreams re-
ported after awakening from the two
states (Nielsen, 2000), and the peculiar
physiology of REM sleep, whose electro-
physiological and neurochemical milieu re-
sembles that of wakefulness more than that
of NREM sleep (Nir and Tononi, 2010).
Positron emission tomography studies have
also shown that global brain metabolism is
comparable between wakefulness and REM
sleep (Braun et al., 1997; Maquet, 2000).
Our finding of a decreased alpha activ-
ity in stage 2 NREM sleep substantially Figure 10. Theta activity during REM sleep and alpha activity during stage 2 across consecutive sleep cycles. The maps report
replicates the finding by Esposito et al. topographic statistical EEG power differences (assessed by unpaired t tests) between the REC and NREC groups. Values are ex-
(2004), who showed that successful recall pressed in terms of t values: positive t values indicate a prevalence of the REC over the NREC group, and vice versa. The two-tailed
after awakening from stage 2 is associated level of significance (p ⱕ 0.003) corresponds to t ⱖ 3.34 in the second and third sleep cycles and to t ⱖ 3.38 in the fourth sleep
with a lower alpha power, particularly in cycle for REM sleep; for stage 2, the level of significance (p ⱕ 0.004) corresponds to a t ⱖ 3.12 in the second and third sleep cycles
and to t ⱖ 3.13 in the fourth sleep cycle. Average values are normalized by total power, color coded, plotted at the corresponding
corresponding centro-temporo-parietal position on the planar projection of the scalp surface, and interpolated (biharmonic spline) between electrodes. The maps are
areas. Also during wakefulness, a more ef- based on the 19 unipolar EEG derivations of the international 10 –20 system with averaged mastoid reference.
ficient encoding of words and faces has
been shown to be associated with a lower dream reports, the larger between-group differences we find. How-
alpha activity (10 –12 Hz) in the right temporo-parietal cortical ever, the current study cannot provide a definitive response to this
region (Molle et al., 2002). Interestingly, Molle et al. (2002) also specific question. This issue can be disentangled only by multiple-
found an increased frontal and temporal theta activity when night within-subject studies, in which preawakening sleep periods
comparing trials with efficient versus poor encoding. Moreover, followed by successful/failed dream recall could be compared and,
intracranial recordings of awake humans have given further sup- complementarily, from multinight studies on subjects who stably
port for an association between a successful episodic memory recall or do not recall dreams.
encoding and a decreased temporo-parietal alpha activity (Sed-
erberg et al., 2003). Complementarily, increases in alpha power
have been correlated with decreased memory performance (Kli- Concluding remarks
mesch et al., 1997; Klimesch, 1999), and EEG–functional mag- The current model of episodic memory based on human studies
netic resonance imaging recordings have shown that alpha (for review, see Nyhus and Curran, 2010) states that theta oscil-
activity is negatively correlated with the BOLD signal in the me- lations allow for top-down control from the frontal cortex to the
dial prefrontal cortex, primary visual cortex, and middle tempo- hippocampus, modulating the encoding and retrieval of episodic
ral gyrus during memory retention (Scheeringa et al., 2009). memories. The theta activity is also higher during encoding than
During NREM sleep, alpha oscillations are indicative of a cor- retrieval, being related more to the access of a stored code than to
tical EEG synchronization, since it increases during postdepriva- more general processes (Klimesch et al., 2001). On the other
tion recovery sleep (Marzano et al., 2010) and is positively hand, the alpha activity seems functionally related to the activa-
correlated with delta–theta activity in the first sleep cycle (Ferrara tion of stored information, and both the alpha power decrease
et al., 2002). Notably, decreases of alpha activity in NREM sleep and the theta power increase are functionally independent
are associated with corresponding increases in REM sleep (Mar- (Khader and Rösler, 2010). Our results, in showing that success/
zano et al., 2010). Together, these findings suggest that the de- failure of dream recall is related to specific cortical EEG activity
creased alpha activity in stage 2 sleep, which is likely to involve and oscillations during the sleep stage preceding awakening, also
the thalamo– cortical network (Klimesch, 1999), is indicative of a suggest that the intrinsic differences in the basic electrophysiol-
lower cortical activation, which is in turn associated with a de- ogy of the NREM stage 2 and REM sleep may determine which
creased likelihood of successful dream recall after awakening. cortical EEG oscillation (i.e., frontal theta or right temporal al-
pha) is predictive of dream recall after awakening. In this view,
Stable interindividual differences? the alpha oscillations likely involve the thalamo-cortical network,
According to the results obtained by analyzing three consecu- whereas the theta rhythm likely involves the hippocampal–corti-
tive sleep cycles, the current findings do not support an interpre- cal network, and these networks might be differently related to
taion in terms of a stable interindividual EEG pattern characterizing semantic and episodic memory (Klimesch, 1999; Nyhus and
subjects in the entire night. Actually, the pattern of topographical Curran, 2010). Suggestively, this dissociation resembles some dif-
differences for the theta activity after REM sleep awakenings and for ferences between qualitative features of dream reports after
the alpha activity after stage 2 awakenings suggests that the predictive awakenings from REM and NREM sleep (for review, see Nielsen,
relationship with dream recall is a function of the proximity to the 2000). Also this suggestion, currently mostly speculative, may be
time of awakening. In other words, the closer the time of collecting tested by combining the intracranial recordings of hippocampal
Marzano et al. • EEG Oscillations Predict Dream Recall J. Neurosci., May 4, 2011 • 31(18):6674 – 6683 • 6683

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