18/7/2021 The cognitive neuroscience of lucid dreaming

Try out PMC Labs and tell us what you think. Learn More.

Neurosci Biobehav Rev. Author manuscript; available in PMCID: PMC6451677

PMC 2020 May 1. NIHMSID: NIHMS1525230
Published in final edited form as: PMID: 30880167
Neurosci Biobehav Rev. 2019 May; 100: 305–323.
Published online 2019 Mar 14.
doi: 10.1016/j.neubiorev.2019.03.008

The cognitive neuroscience of lucid dreaming

Benjamin Baird,a,* Sergio A. Mota-Rolim,b and Martin Dreslerc
aWisconsin Institute for Sleep and Consciousness, University of Wisconsin-Madison,

Madison, Wisconsin, USA

bBrain Institute, Physiology Department and Onofre Lopes University Hospital -

Federal University of Rio Grande do Norte, Natal, Brazil

cDonders Institute for Brain, Cognition and Behaviour, Radboud University Medical

Centre, Nijmegen, The Netherlands

*Corresponding author

Address for correspondence: Dr. Benjamin Baird, Department of Psychiatry, School

of Medicine and Public Health, University of Wisconsin – Madison, 6001 Research
Park Blvd, Madison, WI, 53719, [email protected]

Copyright notice

Publisher's Disclaimer

Abstract
Lucid dreaming refers to the phenomenon of becoming aware of the fact that
one is dreaming during ongoing sleep. Despite having been physiologically
validated for decades, the neurobiology of lucid dreaming is still incompletely
characterized. Here we review the neuroscientific literature on lucid dreaming,
including electroencephalographic, neuroimaging, brain lesion,
pharmacological and brain stimulation studies. Electroencephalographic studies
of lucid dreaming are mostly underpowered and show mixed results.
Neuroimaging data is scant but preliminary results suggest that prefrontal and
parietal regions are involved in lucid dreaming. A focus of research is also to
develop methods to induce lucid dreams. Combining training in mental set with
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 1/61
18/7/2021 The cognitive neuroscience of lucid dreaming

cholinergic stimulation has shown promising results, while it remains unclear

whether electrical brain stimulation could be used to induce lucid dreams.
Finally, we discuss strategies to measure lucid dreaming, including best-
practice procedures for the sleep laboratory. Lucid dreaming has clinical and
scientific applications, and shows emerging potential as a methodology in the
cognitive neuroscience of consciousness. Further research with larger sample
sizes and refined methodology is needed.

Keywords: lucid dreaming, consciousness, meta-awareness, dreaming, REM

sleep

1. Introduction
Becoming aware that one is dreaming while dreaming, what is today referred to
as lucid dreaming, has been known about since antiquity. In Western literature,
it may have first been mentioned by Aristotle in the fourth century BCE in the
treatise On dreams of his Parva Naturali, in which he states: “often when one
is asleep, there is something in consciousness which declares that what then
presents itself is but a dream” (Aristotle, 1941, p. 624). Likewise, in Eastern
cultures, particularly of the south Asian subcontinent, reports of individuals
engaging in practices to cultivate awareness of dream and sleep states date
back millennia (LaBerge, 2003; Norbu and Katz, 1992; Wallace and Hodel,
2012). These include meditative practices specifically designed to “apprehend
the dream state” (Padmasambhava, 1998, p. 156).

Although numerous references to lucid dreaming can be found throughout

world literature (see LaBerge, 1988a for an overview), the modem
nomenclature of lucid dream was not introduced until 1913 by the Dutch
psychiatrist Frederik Van Eeden. In a detailed and engaging account of his
personal experiences with dreams, Van Eeden (1913) referred to lucid dreams
as dreams in which “…the reintegration of the psychic functions is so complete
that the sleeper remembers day-life and his own condition, reaches a state of
perfect awareness, and is able to direct his attention, and to attempt different
acts of free volition” (pp. 149-150). Research over the last four decades has
largely confirmed Van Eeden’s accounts: as we review below, evidence
suggests that during lucid dreams individuals can be physiologically asleep
while at the same time aware that they are dreaming, able to intentionally
perform diverse actions, and in some cases remember their waking life (Dresler
et al., 2011; LaBerge, 1985, 1990; LaBerge, 2015; LaBerge, Nagel, Dement
and Zarcone, 1981c; Windt, 2015).

Despite the fact that such personal accounts of lucid dreams have been
described for centuries, the topic faced skepticism from some scientists and
philosophers (e.g., Malcolm, 1959), in part due to the lack of objective
evidence for the phenomenon. This began to change in the late 1970s and early
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 2/61
18/7/2021 The cognitive neuroscience of lucid dreaming

1980s, however, with the first validation of lucid dreaming as an objectively

verifiable phenomenon occurring during rapid eye movement (REM) sleep.
Building on prior research that showed that shifts in the direction of gaze
within a dream can be accompanied by corresponding movements of the
sleeper’s eyes (Dement and Wolpert, 1958), lucid dreamers were asked to
move their eyes in a distinct pre-agreed upon sequence (full-scale up-down or
left-right movements) as soon as they became lucid (Hearne, 1978; LaBerge et
al., 1981c).

Through this technique, which has since become the gold standard, reports of
lucid dreams could be objectively verified by the presence of distinct volitional
eye movement patterns as recorded in the electrooculogram (EOG) during
polysomnography-verified sleep (Figure 1). The most common version of the
eye signaling technique asks participants to signal when they realize they are
dreaming by rapidly looking all the way to the left then all the way to the right
two times consecutively then back to center in the dream without pausing
(referred to as left-right-left-right eye signals, abbreviated as LRLR). As can be
seen in Figure 1, the LRLR signal is readily discernable in the horizontal EOG,
which exhibits a distinctive shape containing four consecutive full-scale eye
movements that have larger amplitude compared to typical REMs. As we
describe in detail below, lucid dreams can be validated by this method through
the convergence between reports obtained after awakening of becoming lucid
and making the eye movement signals during the dream, accompanied by the
objective eye movement signals recorded in the EOG with concurrent
polysomonographic evidence of REM sleep.

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 3/61
18/7/2021 The cognitive neuroscience of lucid dreaming

Fig 1.
Lucid REM sleep eye movement signaling paradigm.

Exemplary left-right-left-right-center (LRLR) eye movement signal during

polysomnographcally-verified REM sleep. Participants signal when they realize
they are dreaming by rapidly looking all the way to the left (as if looking at their
ear) then all the way to the right two times consecutively then back to center
without pausing. The LRLR signal is readily discernable in the HEOG, which
exhibits a distinctive shape of four consecutive full-scale eye movements of
higher amplitude compared to typical REMs. Note high-frequency
electroencephalogram (EEG) with theta rhythm (~5 Hz) and lack of alpha at OZ
as well as minimal electromyogram (EMG) amplitude due to muscle atonia
characteristic of REM sleep (left) compared to wakefulness (right).

The eye signaling technique also offers a way of objectively contrasting lucid
REM sleep to baseline non-lucid REM sleep, providing a method to investigate
the changes in brain activity associated with lucid dreaming. Furthermore,
lucid dreamers can not only signal to indicate that they are aware that they are
dreaming, but they can also make the eye movement signals to time-stamp the
start and end of experimental tasks performed during lucid dreams (LaBerge,
1990). By providing objective temporal markers, this technique has opened up
a new method for studying the psychophysiology of REM sleep, allowing, for
example, investigations into the neural correlates of dreamed behaviors (e.g.,
Dresler et al., 2011; Erlacher, Schredl and LaBerge, 2003; LaBerge, 1990;
Oudiette et al., 2018). Lucid dreaming thus provides a way to establish precise
psychophysiological correlations between the contents of consciousness during
sleep and physiological measures, as well as enables experimental control over
the content of dreams, and therefore provides a potentially highly useful
experimental methodology.

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 4/61
18/7/2021 The cognitive neuroscience of lucid dreaming

While neuroscientific studies on lucid dreaming have been performed since the
late 1970s, the topic has received increasing attention in recent years due to its
relevance to the emerging neuroscience of consciousness. In this article, we
review the existing literature on the neuroscience of lucid dreaming, including
electrophysiological, neuroimaging, brain lesion, pharmacological and brain
stimulation studies. Additionally, we review recent studies that illustrate how
lucid dreaming can be used as a methodology in the cognitive neuroscience of
consciousness. Finally, we present strategies to measure lucid dreaming both
physiologically and with questionnaires, and discuss procedures to investigate
lucid dreaming in the sleep laboratory.

2. Electrophysiology of lucid dreaming

As noted in the introduction, the first physiological studies of lucid dreaming
began in the late 1970s and early 1980s. These pioneer works established that
lucid dreams occur in REM sleep, characterized by all of the EEG features of
REM sleep according to the Rechtschaffen and Kales (1968) sleep scoring
criteria (Hearne, 1978; LaBerge et al., 1981c). LaBerge (1980b) also observed
that lucid dreams are associated with increased physiological activation, as
measured by increased phasic activity (e.g., increased REM density).
Autonomic nervous system arousal (e.g., heart rate, respiration rate, and skin
potential) were also found to be elevated during lucid REM sleep compared to
non-lucid REM sleep (LaBerge, Levitan and Dement, 1986). Additionally,
lucid dreams were found to occur in REM sleep periods later in the night
(LaBerge et al., 1986). These findings suggest that lucid dreaming is associated
with increased cortical activation (LaBerge, Nagel, Taylor, Dement and
Zarcone, 1981a), which reaches its peak during phasic REM sleep. In addition
to physiological markers of phasic activity, lucid REM sleep was found to be
associated with h-reflex suppression (Brylowski, Levitan and LaBerge, 1989),
a spinal reflex that is reliably suppressed during REM sleep (Hodes and
Dement, 1964). Together these results indicate that lucid dreams occur in
activated periods of REM sleep, as opposed to, for example, a state that is
intermediate between waking and REM sleep.

These findings also raise the further question of whether lucid REM sleep is
associated with localized activation of specific brain regions or changes in
specific frequencies of neural oscillations compared to non-lucid REM sleep.
In this section, we will review EEG studies that have attempted to address this
question. As will be discussed below, while these studies represent important
first steps toward measuring the electrophysiological changes associated with
lucid dreaming, all of them have interpretive issues and most suffer from low
statistical power. As a result, there is considerable discrepancy among findings.
Below we group and discuss results based on the regional EEG band power
changes reported to be associated with lucid REM sleep dreaming.
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 5/61
18/7/2021 The cognitive neuroscience of lucid dreaming

2.1. EEG studies of lucid REM sleep dreaming

2.1.1. Central and posterior alpha Ogilvie and colleagues conducted some of
the first studies to examine EEG spectral changes during lucid REM sleep. In
an early case study, Ogilvie, Hunt, Sawicki and McGowan (1978) compared
two lucid REM sleep epochs to six non-lucid REM sleep epochs and found an
increase in the percentage of alpha band (8-12 Hz) power in a single central
EEG channel. A follow-up study examined a larger group of ten participants
for two nights in the sleep laboratory (Ogilvie, Hunt, Tyson, Lucescu and
Jeakins, 1982). Participants were awakened during the two periods of highest
alpha power and two periods of lowest alpha power from a central EEG
electrode during REM sleep, after which they were asked several questions
about their lucidity, “prelucidity” (i.e., thoughts pertaining to dreaming without
becoming lucid), and degree of dream control. Unfortunately, statistics for the
number of lucid dreams reported by participants were not documented in this
study, nor whether there was a significant difference between conditions in the
number of lucid dreams. Instead, a composite measure was constructed by
collapsing across pre-lucidity, lucidity and control, which was significantly
elevated in the high alpha trials. Therefore, the number (if any) of lucid dreams
that were captured by this procedure is unknown (see LaBerge (1988b) for
further discussion).

Subsequent research has not supported the hypothesis that lucid REM sleep is
associated with increased alpha activity. For example, in a follow-up study
Tyson, Ogilvie and Hunt (1984) found that only pre-lucid but not lucid dreams
significantly differed in alpha activity compared to non-lucid REM sleep. In
another study of eight frequent lucid dreamers using a similar experimental
design, Ogilvie, Hunt, Kushniruk and Newman (1983) observed no difference
in the number of lucid dreams following awakenings from periods of high or
low alpha activity. Furthermore, in a replication attempt of the original case
report that observed an increase in alpha during lucid REM sleep (Ogilvie et
al., 1978), LaBerge and colleagues found no significant differences in alpha
power at the same central channel (C3) from a single subject (LaBerge, 1988b).
Finally, a later follow-up case study analyzed EEG spectral power in five lucid
REM sleep epochs compared to non-lucid REM sleep periods, and observed no
differences in alpha power (Ogilvie, Vieira and Small, 1991). Together this
evidence does not support a reliable association between alpha power and lucid
dreaming. However, the limited spatial coverage of EEG montages in these
studies (in several cases consisting of only one EEG channel) makes it unclear
to what extent these results can be generalized to other brain areas.

2.1.2. Parietal beta Holzinger, LaBerge and Levitan (2006) examined EEG
spectral changes during lucid REM sleep in a group of eleven participants who
reported prior experience with lucid dreaming. Six out of the eleven

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 6/61
18/7/2021 The cognitive neuroscience of lucid dreaming

participants succeeded in becoming lucid in the sleep laboratory, and some

during multiple REM periods, for a total of 16 signal-verified lucid dreams.
The authors found increased power in the low beta frequency range (13-19 Hz)
in parietal electrodes for lucid compared to non-lucid REM sleep. This study
has the advantage of analyzing a larger number of lucid REM sleep periods.
However, a limitation is that EEG signals were only evaluated at four
electrodes (F3, F4, P3, P4). Consequently, localized changes in EEG spectra
may have been missed by the low spatial resolution. Furthermore, due to
technical limitations, the online low-pass filter for the EEG recordings in this
study was set at 35 Hz, and therefore changes in higher-frequency activity were
unable to be evaluated.

The potential functional significance of increased low beta band power in

parietal areas to lucid dreaming is not understood. Holzinger et al. (2006)
speculated that the increased beta power in the parietal EEG could reflect the
understanding of the meaning of the words “This is a dream.” As discussed
below, recent neuroimaging studies have linked parietal regions to several other
cognitive functions associated with lucid dreaming, including self-reflection
(Kjaer, Nowak and Lou, 2002; Lou et al., 2004), episodic memory (Berryhill,
Phuong, Picasso, Cabeza and Olson, 2007; Wagner, Shannon, Kahn and
Buckner, 2005) and agency (Cavanna and Trimble, 2006), suggesting several
other possible interpretations of the results. Neural oscillations in this
frequency range were originally thought to reflect sensorimotor behavior;
however, evidence now suggests that oscillations in this range could play a role
in cognitive processing as well as facilitate large-scale neural integration (e.g.,
Donner and Siegel, 2011; Engel and Fries, 2010). If these results can be
replicated in future studies, one hypothesis is that the increased oscillatory
activity in the beta band could reflect a mechanism of integration between
parietal regions and other areas, which, in some way still to be understood,
helps facilitate lucid dreaming. However, it is also possible that differences in
sensorimotor behavior between lucid and non-lucid REM sleep could boost
brain rhythms that overlap with this frequency range (Koshino and
Niedermeyer, 1975; Pfurtscheller, Stancak and Neuper, 1996; Vanni, Portin,
Virsu and Hari, 1999). Additional research is needed to clarify these findings.

2.1.3. Frontolateral gamma Mota-Rolim et al. (2008) and Voss, Holzmann,

Tuin and Hobson (2009) reported increased gamma band (40 Hz) power in
frontolateral scalp electrodes during lucid compared to non-lucid REM sleep in
three participants each. However, besides an unsuccessful replication in
patients with narcolepsy (Dodet et al., 2014), interpretation of these results are
restricted by several experimental limitations, including the small sample size
(LaBerge, 2010). Importantly, caution is warranted in interpreting these
findings given that, as briefly discussed by Voss et al. (2009), scalp
measurement of cortical gamma, particularly when selectively localized in the
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 7/61
18/7/2021 The cognitive neuroscience of lucid dreaming

frontal and periorbital regions, may be confounded with mircrosaccades.

Ocular myogenic artifacts, which occur during both saccades and
microsaccades and are distinct from the artifacts associated with corneo-retinal
dipole offsets, may confound scalp measurement of gamma activity. One type
of such artifacts is referred to as the saccadic spike potential (SP), which occurs
due to contraction of the ocular muscles during both saccades and
microsaccades (Yuval-Greenberg and Deouell, 2009; Yuval-Greenberg, Tomer,
Keren, Nelken and Deouell, 2008). The influence of the SP artifact on gamma
power was overlooked for a number of years; however, the need to account for
this artifact on scalp measurement of induced gamma activity has now been
thoroughly documented (e.g., Hipp and Siegel, 2013; Keren, Yuval-Greenberg
and Deouell, 2010).

Voss et al. (2009) corrected for eye movement artifacts using regression of the
EOG signal (Gratton, Coles and Donchin, 1983) and by computing current
source densities (CSD) in addition to scalp potentials. However, regression-
based correction procedures are insufficient to remove the SP artifact, and
while the CSD derivation attenuates the SP artifact at posterior channels, it is
not sufficient to remove it at anterior scalp locations (Keren et al., 2010; Yuval-
Greenberg and Deouell, 2009). As Keren et al. (2010) state: “In conclusion,
SCD [CSD] seems to be effective in attenuating the SP effect at posterior sites.
However at sites anterior to Cz and closer to the orbits efficacy gradually
decreases, preserving the temporal and spectral signature of the SP and its
amplitude relative to baseline.” (p. 2258). The influence of the SP artifact on
gamma band power in the comparison of lucid to non-lucid REM sleep is
particularly relevant given that, as noted above, lucid REM sleep has been
associated with increased phasic activation and higher eye movement density
(e.g., LaBerge, 1990).

It is important to note that the need to account for the SP artifact does not
preclude a potential association between increased frontal gamma power and
lucid REM sleep. Indeed, given the link between gamma band power, local
field potentials (LFPs) and the blood-oxygen-level dependent (BOLD) signal
(Lachaux et al., 2007; Nir et al., 2007), if the transition from non-lucid to lucid
REM sleep involves activation or recruitment of additional frontal brain
regions (a plausible hypothesis, also in light of the findings of Dresler et al.
(2012); see Neuroimaging of lucid dreaming below), regional increases in
gamma power might be predicted. However, the spatial topography and
frequency localization of any such effects are likely to be strongly influenced
by the correction and removal of the SP artifact.

With the aforementioned considerations in mind, more research is needed to

clarify whether the increase in frontolateral gamma power during lucid REM
sleep observed by Mota-Rolim et al. (2008) and Voss et al. (2009) reflects

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 8/61
18/7/2021 The cognitive neuroscience of lucid dreaming

ocular myogenic or neural activity. Furthermore, future studies evaluating the

relationship between lucid REM sleep and gamma activity from sensor-level
EEG, particularly at anterior electrodes, need to control for the SP artifact in
order for the results to be interpretable. Several methods have been shown to be
suitable for removal this artifact, including direct identification and removal of
contaminated data by rejecting overlapping windows of time-frequency
transformed data or data correction using independent component analysis
(Hipp and Siegel, 2013). A study that evaluates the effect of direct removal
and/or correction of the SP artifact on gamma power during lucid contrasted
with baseline REM sleep would be an important addition to the literature. In
summary, studies that rigorously control for myogenic artifacts, and in
particular the SP artifact, are needed before conclusions can be drawn
regarding the relationship between lucid REM sleep and frontal gamma
activity.

2.1.4. Fronto-central delta Dodet, Chavez, Leu-Semenescu, Golmard and

Arnulf (2014) evaluated changes in EEG band power during lucid REM sleep
in a group of narcoleptic patients. Given that narcoleptic patients often report a
high rate of lucid dreams (Rak, Beitinger, Steiger, Schredl and Dresler, 2015),
they are a potentially useful population for cognitive neuroscience studies of
lucid dreaming. In the experiment, while both control and narcoleptic patients
reported achieving lucidity and performing the LRLR signals during overnight
and afternoon nap recordings, only the eye signals of the patients during the
nap recordings could be unambiguously identified. This is likely at least
partially attributable to the specific instructions used for making the eye
movement signal (see Section 9 below for discussion of this issue). Despite
this, the study succeeded in recording 14 signal-verified lucid dreams during
naps from seven narcoleptic patients. The main finding was that EEG power
was reduced in the delta band during lucid REM sleep at frontal and central
electrodes. The study also reported that the coherence between several
electrodes was reduced in lucid compared to non-lucid REM sleep in delta,
theta, beta and gamma bands, but these differences are difficult to interpret
since no statistics were reported for this analysis and no corrections for
multiple comparisons were made.

A limitation of the Dodet et al. (2014) study is that EEG signals were only
evaluated at six electrodes, and only in frontal and central scalp regions (Fp1,
Fp2, F7, F8, C3, C4). Parietal electrodes were not included in the EEG
montage, and occipital channels reportedly could not be evaluated due to noise.
Thus, it is possible that local changes in EEG spectra in posterior regions, such
as parietal or occipital areas, were missed due to the limited electrode montage.

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 9/61
18/7/2021 The cognitive neuroscience of lucid dreaming

The finding of lower delta activity during lucid REM sleep is in line with
previous observations that lucid dreams tend to occur during periods of
increased cortical activation (LaBerge, 1990). Specifically, slow waves,
reflected by delta (~0.5-4 Hz) power in the EEG, are associated with neuronal
down states (“off’ periods) in which neurons are hyperpolarized (Steriade,
Timofeev and Grenier, 2001). Decreased delta power (EEG activation)
therefore reflects recovery of neural activity. While the bi-stability between
“on” and “ off’ periods is a central feature of non-REM sleep, slow wave
activity has also been observed in REM sleep (Baird et al., 2018b; Funk,
Honjoh, Rodriguez, Cirelli and Tononi, 2016). Neuronal down states have also
been linked to the loss of consciousness during both anesthesia and sleep
(Purdon et al., 2013; Tononi and Massimini, 2008), which is hypothesized to be
related to the breakdown of causal interactions between bi-stable neurons
(Pigorini et al., 2015; Tononi, Boly, Massimini and Koch, 2016). Therefore,
one potential explanation is that this finding reflects reduced bi-stability and
increased causal interactions between cortical neurons in these areas during
lucid REM sleep. Notably, reduced delta power in posterior cortex has been
found to be associated with dreaming as opposed to dreamless sleep in both
REM and NREM sleep (Siclari et al., 2017). An intriguing speculation based
on these results is therefore that this reduction in delta power also extends to
frontal regions during lucid REM sleep dreaming. However, it remains to be
seen whether these findings can be replicated and whether the results
generalize to non-clinical populations.

2.2. General discussion of EEG studies of lucid REM sleep

In summary, EEG studies show substantial disagreement regarding the spatial
and spectral changes associated with lucid dreaming. As reviewed above,
different studies have observed an increase in central or posterior alpha,
parietal beta, frontolateral gamma or a reduction in frontocentral delta during
lucid compared to baseline REM sleep. Aside from the general uncertainty in
the results of some studies due to low statistical power, these discrepant results
might be partially explained by the use of limited electrode montages and
evaluation of different EEG frequency bands. In the spatial domain in
particular, many studies have used less than six scalp electrodes, in several
cases only covering some scalp regions but not others, precluding analysis of
EEG activity in regions in which significant effects were found in other studies.
For instance, the study by Dodet et al. (2014) did not include electrodes in
parietal or occipital regions, precluding the possibility to replicate the findings
of increased parietal beta by Holzinger et al. (2006). Studies by Ogilvie et al.
(1978, 1982) evaluated only a single central EEG channel (C3). These non-
overlapping spatial montages limit the comparison of results across some of
these studies.

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 10/61
18/7/2021 The cognitive neuroscience of lucid dreaming

Another factor that might contribute to the discrepant findings is the fact that
lucid dreaming can be achieved and executed in different ways. For example,
the observed changes in the EEG during lucid REM sleep might depend in part
on the degree of vividness, working memory, emotional tone, self-
consciousness, attention and insight, which could vary across individuals as
well as specific dreams. Relatedly, different subjective experiences and
contents during lucid dreams plausibly have their own neurobiological
substrates (Mota-Rolim, Erlacher, Tort, Araujo and Ribeiro, 2010), just as in
non-lucid dreams (Siclari et al., 2017). Changes in brain activity during lucidity
may also partly depend on how experienced the lucid dreamer is. For instance,
lucid dreams of less experienced individuals may often be more ephemeral and
involve less control over dream content, while more experienced lucid
dreamers may be more likely to have longer and more stable lucid dreams, as
well as the capacity to exert greater amounts of control. This might lead to a
more distinct signal in the EEG for experienced lucid dreamers on the one
hand, but also presumably less neural activity related to the effort needed to
maintain the state (neural efficiency). In line with this, Dodet et al. (2014)
suggested that the mental effort needed to achieve and sustain lucidity might be
reduced in narcoleptic patients, who may access the lucid REM sleep state with
less effort.

These comments should not be taken to indicate that there is not a consistent
neurobiology of lucid dreaming. However, it does suggest that analysis of the
EEG spectral changes associated with lucid dreaming used in previous studies
may need to be optimized for detecting more subtle and localized effects. All
studies reviewed above have measured the average power over a given spectral
band and region over comparably long time intervals. However, it is possible
that lucid dreaming is associated with spectral changes that can only be
detected by a better time resolved analysis, such as time-frequency analysis,
that may be overlooked by averaging over large windows in time or frequency
space.

Furthermore, these considerations emphasize the need for more careful

assessment of the phenomenology of lucid dreams. In this regard, we would
like to note that it is plausible that there are at least two different neural
signatures associated with lucid dreaming. The first captures what might be
termed the “moment of lucidity”—that is, the transient moment of meta-
awareness in which one has the metacognitive insight that one is currently
dreaming (Schooler, 2002). The second captures potential sustained differences
in brain activity between lucid and non-lucid REM sleep dreaming. This
second neural signature is unlikely to be a signature of meta-awareness per se,
as during lucid dreams individuals do not continuously engage in
metacognitive reflection on their state of consciousness. Rather, this second
signature captures the “state-shift” in consciousness that occurs from non-lucid
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 11/61
18/7/2021 The cognitive neuroscience of lucid dreaming

to lucid dreaming, with enhanced volition, episodic memory and accessibility

of metacognition (Dresler et al., 2014; Spoormaker, Czisch and Dresler, 2010).
Changes in these aspects of cognition in the shift to lucidity have been
hypothesized to reflect an overall change in the conscious experience of being
a cognitive subject (Windt and Metzinger, 2007). Both the physiological
correlates of the moment of lucidity as well as overall differences in brain
activity between lucid and non-lucid dreams are interesting research targets.
However, these research targets are at least conceptually distinct, a point that
has, in our view, not received adequate attention in the research literature. To
our knowledge, no studies have yet evaluated differences in brain activity with
EEG or functional magnetic resonance imaging (fMRI) specifically associated
with the moment of lucidity, and this remains an interesting question for future
work.

Larger sample sizes are needed in future studies to achieve adequate statistical
power. One way to approach this would be to undertake more extensive
population screening for high-frequency lucid dreamers. For example, through
mass surveys, thousands of potential participants could be screened and the top
few percent reporting the highest lucid dream frequency could be selected for
training before undergoing sleep laboratory recordings. As we discuss below,
new techniques for lucid dream induction also have the potential to enable
efficient collection of larger datasets.

Overall, studies with higher statistical power, better assessment of

phenomenological content, higher spatial resolution EEG montages, and more
sophisticated analysis of the EEG signal will be needed to address these issues
and shed light on the conflicting findings of EEG studies of lucid dreams
conducted to date. Studies using high-density EEG would also be valuable,
enabling both higher temporal as well as higher spatial resolution analysis of
neural oscillatory activity. Source modeling of such data could also potentially
be informative for localizing changes in neural oscillations associated with
lucid dreaming to specific cortical areas, though it remains unclear whether
methods for source localization will be able to produce a valid specification of
the generators relevant for lucid dreaming. In particular, the generators might
be distributed widely in the brain and active concurrently.

Another interesting question with respect to the electrophysiology of lucid

dreaming is whether there are possible sleep pattern traits that are associated
with lucid dreaming. It would be informative to investigate whether there are
common sleep patterns seen in frequent lucid dreamers compared to non-
frequent lucid dreamers. For example, do frequent lucid dreamers tend to have
more phasic REM sleep, or more fragmented REM sleep with a higher number

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 12/61
18/7/2021 The cognitive neuroscience of lucid dreaming

of transitions (especially gradual transitions) between REM sleep and waking?

As far as we know, no study has investigated lucid dreaming with this
approach; therefore, studies addressing these questions would be valuable.

2.3. EEG studies of lucid dreaming during non-REM sleep

The activated EEG of REM sleep was originally thought to be exclusively
associated with dreaming (Antrobus and Antrobus, 1967; Dement and Wolpert,
1958), while the low-frequency activity of non-REM (NREM) sleep was
thought to be associated with the absence of dreaming. Subsequent research
has shown, however, that participants report dreams or related forms of sleep
mentation in up to 70% of awakenings from NREM sleep (Siclari et al., 2017;
Siclari, LaRocque, Postle and Tononi, 2013; Stickgold, Malia, Fosse and
Hobson, 2001). NREM dreams tend to be less emotional and visually vivid, as
well as more thought-like (Cavallero, Cicogna, Natale, Occhionero and Zito,
1992; Hobson, Pace-Schott and Stickgold, 2000). Research suggests that lucid
dreams, on the other hand, are predominantly a REM sleep phenomenon
(LaBerge et al., 1986; LaBerge et al., 1981c). However, this does not imply that
lucid dreams cannot occur during NREM sleep. There have been several
reports of lucid dreams during NREM sleep stages N1 (transition from wake
state to sleep) and N2 (consolidated light sleep), although in many of the
published cases it is uncertain whether the lucid episode occurred in an
unambiguous stage of NREM sleep (Dane and Van de Caslte, 1984; LaBerge,
1980b, 1990; LaBerge et al., 1981c; Stumbrys and Erlacher, 2012).

In one study, LaBerge (1980b) recorded polysomnography from a single

subject who reported frequently experiencing lucid dreams at sleep onset. The
participant rested quietly while drifting to sleep and upon falling asleep was
awakened and asked for a dream report. Forty-two dream reports were
collected over three nights, 25 of which the participant reported as a lucid
dream, and all of which reportedly occurred during stage N1. However, the
dream reports were mostly short “dreamlets”, thus it is plausible that these N1
lucid dreams could differ phenomenologically from REM sleep lucid dreams.
Furthermore, none of these lucid dreams were verified with eye movement
signals. In another study, two participants reported lucid dreams upon
spontaneous awakening from N1 and N2 (LaBerge et al., 1981c). In the N2
instance, the participant reported only a brief moment of lucidity just before
waking up. Furthermore, the participant did not make eye movement signals to
time-stamp the moment of lucidity, and it is therefore difficult to ascertain
whether the moment of lucidity occurred in the process of awakening. The N1
case was also ambiguous: while in this case the participant reported making
eye movements to signal lucidity, the signals could not be verified on the
polysomnogram.

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 13/61
18/7/2021 The cognitive neuroscience of lucid dreaming

In a study on the effects of posthypnotic suggestion on lucid dreaming, Dane

and Van de Caslte (1984) tested hypnotically susceptible females with no prior
experience in lucid dreaming. Importantly for the present discussion, lucid
dreams were reported following awakening from both REM and NREM sleep.
Five lucid dreams were reported in total from stage N2, but in all cases the
LRLR eye signal occurred after arousal/awakening, and thus none of these
could be objectively confirmed. However, several N1 lucid dreams were
confirmed by LRLR signaling. This study was thus the first to provide
objective evidence for lucid dreaming during stage 1 NREM sleep. However,
as noted above, how these N1 dreams compare phenomenologically to REM
sleep lucid dreams remains unclear.

Stumbrys and Erlacher (2012) reported two potential cases of lucid dreams
during NREM with eye signaling. However, due to the study protocol, the
experimenters could only collect dream reports the following morning. In the
first case, the participant reported the next morning making an eye movement
signal in a lucid dream early in the night, but given the long amount of time
between the report and the signal there is uncertainty whether the report
corresponds to the observed signal during NREM sleep. Furthermore, while the
two 30-second polysomnography epochs for sleep scoring preceding the eye
signal appear to be unambiguous N2 sleep, the EEG dynamic shifts during the
30-second epoch containing the eye-signal to lower amplitude activity without
apparent spindles or K-complexes. Without knowing the stage of the epochs
following the eye signal, which was not reported in the study, it is possible that
the eye signal occurred in a transitional sleep stage. In the second case reported
by Stumbrys and Erlacher (2012), the eye signals occurred with some signs of
arousal and the participant had no memory of executing the eye signals the
following morning. These data therefore provide ambiguous evidence for
signal-verified lucid dreams during NREM sleep.

In three further case reports of eye movement signaled NREM lucid dreams,
one case was reported to occur in N1 and two cases in N2 visually scored sleep
stages (Mota-Rolim et al., 2015). The first case was scored as N1, since an
increase in theta (4-7 Hz) and a decrease in alpha (7-14 Hz) power was
observed in more than half of the 30 second scoring epoch, meeting the AASM
criteria for classification of stage N1 sleep. The other two cases were scored as
occurring during N2 episodes since they had spindles and K-complexes in the
30 second scoring epoch with the eye signals. These data thus replicate signal-
verification of N1 lucid dreams and provide preliminary evidence for signal-
verified N2 lucid dreams.

Together, these results suggest that although most lucid dreams occur during
REM sleep, they can also occur during NREM sleep. However, additional
studies providing objective evidence of NREM lucid dreams confirmed by eye-

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 14/61
18/7/2021 The cognitive neuroscience of lucid dreaming

signaling, particularly in N2 sleep, are needed. Currently there are no reports of

lucid dreams recorded during NREM stage 3 (N3), also known as deep sleep,
or slow wave sleep. While there are intriguing reports of practitioners of both
Transcendental Meditation and Tibetan Dream Yoga claiming to have
developed the ability to maintain a type of lucid awareness throughout the
entire sleep cycle, including also states of “lucid dreamless sleep”
(Gackenbach, Cranson and Alexander, 1986; Mason and Orme-Johnson, 2010;
Wallace, 2013; Windt, Nielsen and Thompson, 2016), these claims have not
been corroborated with physiological measures. However, several studies have
found a relationship between meditation practice and lucid dreaming (e.g.,
Baird, Riedner, Boly, Davidson and Tononi, 2018c; Gackenbach et al., 1986;
Mota-Rolim et al., 2013; Stumbrys, Erlacher and Malinowski, 2015), which
could be due to changes in REM sleep patterns induced by meditation practice
and/or to neurocognitive changes associated with meditation practice (e.g.,
increased mental control or meta-awareness).

3. Neuroimaging of lucid dreaming

As noted, dream-like mental activity can be observed during all sleep stages.
However, REM sleep dreams tend to be more vivid, emotional, bizarre, and
more often include a narrative structure (Cavallero et al., 1992; Hobson et al.,
2000). These phenomenological characteristics have been suggested to be
associated with the neural activation and deactivation patterns observed during
REM sleep (e.g., Nir and Tononi, 2010). For example, higher visual areas show
increased regional cerebral blood flow during REM sleep compared to both
wakefulness and slow wave sleep (Braun et al., 1998), which is in line with the
visuospatial experiences that are common during REM sleep dreaming (e.g.,
Windt, 2010). Additionally, the amygdala, medial prefrontal cortex and anterior
cingulate cortex show increased regional cerebral blood flow during REM
sleep (Braun et al., 1997; Maquet et al., 1996). All of these brain areas have
been implicated in emotional processing, mirroring the intense emotions that
can be experienced in REM sleep dreams. In contrast, the anterior prefrontal
cortex (aPFC) and parietal cortex, including the inferior parietal lobule and
precuneus, show low regional cerebral blood flow during normal REM sleep
(Braun et al., 1997; Maquet et al., 1996). Deactivation of these regions has
been postulated to underlie the diminished insight into the global state of
consciousness and restricted volitional control typical of non-lucid dreaming
(e.g., Hobson and Pace-Schott, 2002; Nir and Tononi, 2010).

3.1. Neuroimaging lucid REM sleep dreaming

At the current time, there is only one fMRI study of lucid REM sleep, and it is
a case study (Dresler et al., 2012). Two separate signal-verified lucid dreams
were recorded from a single subject during EEG-verified REM sleep inside the
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 15/61
18/7/2021 The cognitive neuroscience of lucid dreaming

MRI scanner. Compared to non-lucid REM sleep, lucid REM sleep showed
increased fMRI BOLD signal in a number of cortical regions, including the
superior frontal gyrus, aPFC, medial and lateral parietal cortex, inferior/middle
temporal gyri and occipital cortex (Figure 2a). Interestingly, several of these
regions, particularly the parietal regions and frontal pole, are areas that, as
noted above, consistently show reduced regional cerebral blood flow during
non-lucid REM sleep compared to wakefulness (Nir and Tononi, 2010).

Figure 2.

a) Blood-oxygen-level dependent (BOLD) activation in fMRI case study of

lucid dreaming (Dresler et al., 2012). Clusters show regions with significantly
increased BOLD signal during lucid REM sleep (pFDR < 0.005) in the left
lateral hemisphere view (left) and right lateral hemisphere view (right).
Increased activity was observed in anterior prefrontal cortex (aPFC), medial and
lateral parietal cortex, including the supramarginal and angular gyrus and
inferior/middle temporal gyrus during lucid REM sleep contrasted with non-
lucid REM sleep. b) Seed-based resting-state functional connectivity
differences between frequent lucid dreamers and controls (Baird et al.,
2018a). To estimate connectivity, spherical regions-of-interest were defined in
aPFC based on the peak voxel reported in Dresler et al. (2012) (red circle).
Frequent lucid dreamers had increased resting-state functional connectivity
between left aPFC and bilateral angular gyrus, bilateral middle temportal gyrus
and right inferior frontal gyrus. All clusters are significant at p<0.05, corrected
for multiple comparisons at the cluster level.

Evidence linking frontopolar cortex to lucid dreaming is consistent with a role

of this region in metacognition and self-reflection. For example, research has
found that aPFC shows increased activation during self-reflection on internal
states, such as the evaluation of one’s own thoughts and feelings (Christoff,
Ream, Geddes and Gabrieli, 2003; McCaig, Dixon, Keramatian, Liu and
Christoff, 2011). Individuals can also learn to voluntarily modulate activity in
aPFC through a metacognitive awareness strategy (McCaig et al., 2011).
Furthermore, inter-individual variance in metacognitive ability has also been
linked to aPFC gray matter volume (Fleming, Weil, Nagy, Dolan and Rees,
2010) and aPFC resting-state functional connectivity (Baird, Smallwood,
Gorgolewski and Margulies, 2013). Finally, patients with damage to this region
frequently display metacognitive deficits such as inability to monitor disease
symptoms or accurately appraise their cognitive functioning (Joseph, 1999;

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 16/61
18/7/2021 The cognitive neuroscience of lucid dreaming

Schmitz, Rowley, Kawahara and Johnson, 2006), which might be compared to

the lack of metacognitive insight into the state of consciousness characteristic
of non-lucid REM sleep dreams (Dresler et al., 2015).

Dresler et al. (2012) additionally observed increased BOLD signal during lucid
dreaming in the bilateral precuneus and inferior parietal lobules (angular and
supramarginal gyri). As noted above, parietal cortex and the precuneus in
particular has been implicated in self-referential processing, episodic memory,
and the experience of agency (Cavanna and Trimble, 2006), mirroring the
increase of these cognitive capabilities during lucid dreaming. Finally,
activation increases during lucid dreaming were also found in some occipital
and inferior temporal regions, which are part of the ventral stream of visual
processing involved in conscious visual perception (Rees et al., 2002). While
these activations may seem puzzling at first sight, as non-lucid dreams are also
characterized by vivid dream imagery, they are in line with reports that lucid
dreams can be associated with increased visual vividness and clarity of the
dream scene (e.g., Green, 1968).

There are several limitations to the study by Dresler et al. (2012) that are
important to note. First, as mentioned above, the findings are based on
observations from a single subject and caution is therefore warranted in
generalizing from the results. Currently no group-level fMRI study of lucid
dreaming has been conducted, and such a study, along with systematic
replications, will be needed before firm conclusions can be drawn. Another
limitation is that, as described below (see Section 7.1), the participant was
performing a task during the lucid REM sleep segment (repeated eye signaling
and hand clenching). While Dresler and colleagues accounted for task
activation via nuisance regression of the left and right fist clenching task, it is
possible that some of the activations observed still partially reflect task
execution and maintenance of attention/task-set rather than lucidity per se. One
way to address this in future studies would be to contrast periods of lucid REM
sleep when the participant is not performing an explicit task to non-lucid REM
sleep, i.e., a “no-task, within-state paradigm” (Siclari et al., 2013).

3.2. Neuroimaging individual differences in lucid dreaming

Several studies have taken an individual differences approach to neuroimaging
of lucid dreaming. While most people spontaneously experience lucid dreams
infrequently, there is substantial variation in lucid dream frequency, ranging, by
current estimates, from never (approximately 40-50%) to monthly
(approximately 20%) to a small percentage of people that report lucid dreams
several times per week or in some cases every night (Mota-Rolim et al., 2013;
Saunders, Roe, Smith and Clegg, 2016; Snyder and Gackenbach, 1988). This
variation invites the question of whether individuals who experience frequent

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 17/61
18/7/2021 The cognitive neuroscience of lucid dreaming

lucid dreams show differences in anatomical or functional properties of the

brain. Studies addressing this question can provide complementary evidence on
the neurobiology of lucid dreaming.

In the first neuroimaging study to evaluate the relationship between lucid

dream frequency and brain anatomy, Filevich, Dresler, Brick and Kuhn (2015)
measured whole-brain gray matter volume using voxel-based morphometry in
individuals with higher (“high lucidity”) vs. lower (“low lucidity”) scores on a
scale assessing the frequency of lucid dreams and/or dream content
hypothesized to be related to lucidity. Consistent with the hypothesized
connection between the metacognitive functions of aPFC and lucid dreaming
discussed above, the study found increased gray matter volume in two regions
of the frontal pole (BA9/10), as well as the right anterior cingulate cortex, left
supplementary motor area and bilateral hippocampus in the high lucidity
group. Additionally, the two identified frontopolar regions showed higher
BOLD signal in the monitoring component of a metacognitive thought-
monitoring task performed while awake.

A limitation of the study by Filevich et al. (2015) is that participants were not
frequent lucid dreamers per se, but rather subjects from a database who scored
higher relative to other participants on the scale. Lucid dream frequency for the
two groups was not reported in the study, thus it remains unclear to what extent
the “high lucidity” group experienced frequent lucid dreams in absolute terms.
Furthermore, the composite measure of dreaming used to distinguish the two
groups measured not only frequency of lucid dreams but also different
dimensions of dream content. While several of these content dimensions have
been found to be higher in lucid dreams (Voss, Schermelleh-Engel, Windt,
Frenzel and Hobson, 2013), it is likely that several of these dimensions also co-
vary more generally with dream recall and/or cognitive content in dreams
unrelated to lucidity. As a consequence, as the authors note, some of the results
could have been partly influenced by differences in dreaming “styles”, content
or dream recall.

More recently, Baird, Castelnovo, Gosseries and Tononi (2018a) evaluated a

sample of high-frequency lucid dreamers who reported lucid dreams in the
range of three to four times per week to multiple times per night compared to a
control group who reported lucid dreams once per year or less. The frequent
lucid dream group and control group were case-control matched on age,
gender, and dream recall frequency. Based on the previous research reviewed
above, the primary aim of the study was to investigate whether individuals who
have frequent lucid dreams would show increased gray matter density and/or
resting-state functional connectivity of aPFC. Consistent with this, compared to
the control group, individuals who reported frequent lucid dreams showed
increased resting-state functional connectivity between the left aPFC and the

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 18/61
18/7/2021 The cognitive neuroscience of lucid dreaming

bilateral angular gyrus, bilateral middle temporal gyrus and right inferior
frontal gyrus (Figure 2b). The frequent lucid dream group also showed
decreased functional connectivity between left aPFC and bilateral insula.
Whole-brain graph-theoretic analysis revealed that left aPFC had increased
node degree and strength in the frequent lucid dream group compared to the
control group. However, in contrast to the findings of Filevich et al. (2015), no
significant differences in gray matter density were observed between groups in
either a whole-brain analysis or an aPFC region-of-interest analysis.

Given the link to metacognition, it has also been suggested that lucid dreaming
may be linked to large-scale networks that regulate executive control processes,
in particular the frontoparietal control network (Dresler et al., 2015;
Spoormaker et al., 2010). To address this question, Baird et al. (2018a)
additionally evaluated the association between frequent lucid dreaming and
connectivity within established large-scale brain networks, including the
frontoparietal control network. Consistent with a link between the
frontoparietal control network and lucid dreaming, Baird and colleagues found
that frequent lucid dreamers had increased functional connectivity between
aPFC and a network of regions that showed the greatest overlap with a
frontoparietal control sub-network (Dixon et al., 2018; Yeo et al., 2011).
However, neither connectivity within the frontoparietal control network
broadly defined through meta-analysis (or within or between any other large-
scale networks), nor connectivity within frontoparietal control sub-networks, as
defined through parcellation of resting-state networks, showed significant
differences between the lucid dream group and the control group. The authors
speculate that this could be attributed to both the partial overlap of the regions
that showed increased aPFC connectivity in lucid dreamers with the
frontoparietal control network. However, it is important to keep in mind that
while this study did not find a significant difference in resting-state
connectivity within the frontoparietal network in frequent lucid dreamers, it
remains an open question whether lucid REM sleep dreams show increased
connectivity within the frontoparietal control network compared to non-lucid
REM sleep dreams.

Overall, the resting-state connectivity results of Baird et al. (2018a) converge

with the fMRI case study of lucid REM sleep dreaming described above
(Dresler et al., 2012), which found that an overlapping network of brain areas
increased fMRI BOLD signal during lucid compared to baseline REM sleep,
including bilateral aPFC, bilateral inferior parietal lobule (including the angular
gyrus), and bilateral middle temporal gyrus (Figure 2). Together, these results
suggest that increased intrinsic functional connectivity between aPFC and the
angular gyrus/middle temporal gyrus—regions that, as reviewed above, show
reduced activity in REM sleep (Nir and Tononi, 2010) and increased activity
during lucid REM sleep (Dresler et al., 2012)—is associated with the tendency
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 19/61
18/7/2021 The cognitive neuroscience of lucid dreaming

to have frequent lucid dreams. However, while the convergence between these
two preliminary studies is encouraging, the paucity of neuroimaging data on
this question limits strong conclusions at the current time.

3.3. Future directions for neuroimaging of lucid dreaming

Neuroimaging studies of lucid REM sleep using larger samples sizes are
needed. In particular, a group-level fMRI study of lucid REM sleep dreaming
using a no-task, within-state paradigm is perhaps the most important next step
in this line of research. In addition to evaluating activation and deactivation as
revealed by changes in BOLD signal, it would also be informative to evaluate
differences in functional connectivity in such a study. For example, as noted,
one question that arises from the above neuroimaging findings is whether there
could be increased connectivity within the network of regions identified in
Dresler et al. (2012) and Baird et al. (2018a) during lucid contrasted with non-
lucid REM sleep dreaming. Furthermore, building on the individual differences
results, in future work it would also be interesting to evaluate whether high
frequency lucid dreamers show increased functional connectivity and/or higher
BOLD signal in these brain areas during baseline REM sleep. If so, this could
suggest that it may be possible to bias the brain toward increased metacognitive
awareness of dreaming during REM sleep, for example, as discussed in the
next sections on induction of lucid dreams, through techniques to increase
activation of these regions.

In line with these remarks, it has been suggested that not only regional
activation of frontoparietal brain areas but also connectivity between these
regions could be important for lucidity to emerge during REM sleep
(Spoormaker et al., 2010). Indeed, while activation in these frontal and parietal
regions has been linked to key functions associated with lucid dreaming,
including metacognition, as discussed above, regional activations and
metabolic increases in these regions have also been observed during states of
global unconsciousness and subliminal information processing. For instance,
subliminally presented no-go stimuli during a response inhibition task activate
frontoparietal cortices in the absence of awareness (van Gaal, Ridderinkhof,
Scholte and Lamme, 2010). Moreover, loss of consciousness during the tonic
phase of generalized tonic-clonic seizures is associated with a transient
increase rather than decrease in metabolism in frontoparietal cortex
(Blumenfeld, 2008; Engel, Kuhl and Phelps, 1982).

Recent findings have suggested that a potentially more sensitive marker of

unconscious states may be reduced connectivity between frontoparietal areas,
particularly from frontal to parietal regions. For example, several neuroimaging
studies of patients in a persistent vegetative state or under different categories
of general anesthetics have shown a specific impairment of the backward

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 20/61
18/7/2021 The cognitive neuroscience of lucid dreaming

connectivity from frontal to parietal regions (Boly et al., 2011; Boly et al.,
2012; Lee et al., 2013). These findings converge with theoretical work and
computational modeling (Tononi, 2011), which has suggested a link between
consciousness and effective connectivity within a neural architecture, or the
capacity of a set of neural elements to exert causal influence over other neural
groups in a system. At present, it is unclear whether this reduction of top-down
frontoparietal connectivity is linked to changes in global brain activity,
alterations in primary consciousness (i.e., subjective, phenomenal states of
seeing, hearing or feeling), or whether it could relate to self-awareness (i.e.,
explicit conscious awareness of oneself and one’s state). A common
interpretation of these results is that top-down frontoparietal connectivity is a
marker of global loss of consciousness, including primary consciousness (e.g.,
Mashour, 2014). However, given that the reduction in top-down connectivity
has also been observed under ketamine (Lee et al., 2013), during which patients
often report vivid dream-like experiences, it is plausible that the reduction of
frontoparietal connectivity could instead indicate loss of self-awareness.

Cognitive neuroscience studies of lucid dreaming are uniquely placed to

contribute to this question because the comparison of lucid REM sleep to non-
lucid REM sleep is perhaps the only contrast that allows for a direct
comparison between the global loss and recovery of reflective consciousness
independently of global shifts in primary consciousness, arousal or vigilance
state. Thus, the question of whether lucid REM sleep is associated with altered
connectivity between frontal and parietal cortices has implications for several
broad questions in the cognitive neuroscience of consciousness. Future studies
evaluating changes in effective connectivity during lucid REM sleep dreaming,
and in particular changes in top-down frontoparietal connectivity, would be
valuable.

4. Brain lesions and lucid dreaming

In the neurological literature, to our knowledge only one paper has reported
changes in lucid dreaming as a result of neurological insult or brain lesions
(Sagnier et al., 2015). The paper describes two case reports of young patients
who reported lucid dreams following unilateral ischemic stroke to the left
mediodorsal thalamus. The first patient was a 26-year-old female with a left
anterior and mediodorsal thalamic stroke in an area supplied by the
premamillary artery, as revealed by MRI scans. She reported frequent lucid
dreams in the early morning hours, along with increased nightmares and
nocturnal awakenings. She also reported that her lucid dreams mostly involved
the hospital and medical staff that she encountered during her hospitalization,
and included catastrophic events such as helicopter crashes and hyper-
aggressive behaviors. The second patient was a 36-year-old male with a left
mediodorsal thalamic stroke in the area supplied by the paramedian artery as
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 21/61
18/7/2021 The cognitive neuroscience of lucid dreaming

revealed by MRI scans. He reported frequent lucid dreams following the

stroke, which also tended to occur in the early morning hours, along with
increased nocturnal awakenings, but without an increase in nightmares. Lucid
dreams subsided after one month for both patients.

Lucid dreams have not previously been reported following either unilateral or
bilateral thalamic stroke. However, loss of neurons in the anterior and
dorsomedian thalamic nuclei that occurs in familial fatal insomnia is associated
with loss of nocturnal sleep as well as oneiric ‘intrusions’ during wakefulness
(Montagna, 2005; Raggi, Cosentino, Lanuzza and Ferri, 2010). Furthermore,
hypersomnia and irregular sleep are frequently reported following paramedian
thalamic stroke (Hermann et al., 2008; Luigetti et al., 2011). These clinical
features could be manifestations of disruption of the intralaminar and midline
thalamic nuclei located in the mediodorsal thalamus, which are part of the
brain’s arousal network (Van der Werf, Witter and Groenewegen, 2002). Thus,
one possibility is that lucid dreams in these patients could have partly resulted
from increased or abnormal functioning of the brain’s arousal systems during
sleep, which is consistent with the reported increase in nocturnal awakenings.
Both patients also reported that their dreams contained highly anxious and
emotional content, which could reflect abnormal connectivity between these
thalamic nuclei and limbic structures with which they are densely connected
(Van der Werf et al., 2002). The highly emotional or disturbing content may
have also contributed to lucid dreaming, as these types of experiences could
induce individuals to question whether the explanation for such surprising or
frightening experiences is that they are dreaming (LaBerge and Rheingold,
1990).

A systematic study of the incidence of lucid dreams following thalamic strokes

is lacking. Particularly given that the lucid dreams subsided after a relatively
short duration (one month) for both patients, it is possible that lucid dreaming
as a consequence of thalamic strokes has been under-reported and/or
overlooked. More generally, a large-scale study of the occurrence of lucid
dreaming in neuropsychological cases has not been undertaken and would be a
welcome addition to the literature. The converse case, of a brain lesion causing
loss of lucid dreaming in an individual who regularly experiences lucid dreams
has also to our knowledge not been reported. Such a case would likely be very
unusual, particularly considering the small percentage of individuals who
experience lucid dreams spontaneously with high frequency. However, if such
a case were identified it could be informative to the neurobiology of lucid
dreaming.

5. Pharmacological induction of lucid dreaming

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 22/61
18/7/2021 The cognitive neuroscience of lucid dreaming

A main target of research is to develop methods to make the lucid dream state
more accessible. Indeed, reliable techniques to induce lucid dreams are needed
for it to be effectively used in both clinical and scientific applications.
Evidence suggests that lucid dreaming is a learnable skill (LaBerge, 1980a)
that can be developed by training with various induction strategies (LaBerge
and Rheingold, 1990; Price and Cohen, 1988; Stumbrys, Erlacher, Schadlich
and Schredl, 2012). These include training in prospective memory techniques
(LaBerge and Rheingold, 1990), which can be further aided by application of
external sensory cues (LaBerge and Levitan, 1995; LaBerge, Levitan, Rich and
Dement, 1988; LaBerge, Owens, Nagel and Dement, 1981b) and/or
interrupting sleep with short periods of wakefulness (Aspy, Delfabbro, Proeve
and Mohr, 2017; LaBerge, 1980a; LaBerge, Phillips and Levitan, 1994;
Stumbrys et al., 2012). Within cognitive neuroscience, studies have evaluated
pharmacological as well as non-invasive brain stimulation approaches to lucid
dream induction. In this section, we review studies that have taken a
pharmacological approach to lucid dream induction and in the next section we
review electrical brain stimulation studies.

5.1. Effects of Acetylcholinesterase inhibitors (AChEIs) on lucid

dreaming
As discussed above, lucid dreaming is associated with increased cortical
activation (LaBerge et al., 1981a), which reaches its peak during phasic REM
sleep. Given the relationship between phasic REM sleep and lucid dreaming, as
well as the role of Acetylcholine (ACh) in REM sleep regulation (e.g.,
Amatruda, Black, McKenna, McCarley and Hobson, 1975; Velazquez-
Moctezuma, Shalauta, Gillin and Shiromani, 1991), agents acting on the
cholinergic system have received particular interest. In an initial pilot study,
LaBerge (2001) evaluated the effect of donepezil (Aricept), an
Acetylcholinesterase inhibitor (AChEI), on lucid dreaming in a small group of
participants (N=10) who reported prior experience with lucid dreaming. On
each night, participants received either 0 mg (placebo), 5 mg, or 10 mg of
donepezil, with the dose order counterbalanced across the three nights of the
experiment. Nine of the ten participants (90%) reported at least one lucid
dream on donepezil, while only one participant reported a lucid dream on the
placebo dose.

Following on these results and additional pilot research, LaBerge, LaMarca and
Baird (2018b) conducted a double blind, placebo-controlled study in a large
group of participants (N=121) with high dream recall and an interest in lucid
dreaming. The first goal of the study was to quantify the size and reliability of
the effect of AChEI on lucid dreaming. The second goal was to test the
effectiveness of an integrated lucid dream induction protocol that combined
cholinergic stimulation with other methods, including sleep interruption and
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 23/61
18/7/2021 The cognitive neuroscience of lucid dreaming

the Mnemonic Induction of Lucid Dreams (MILD) technique, which trains

participants to use prospective memory to induce lucid dreams (LaBerge,
1980a; LaBerge and Rheingold, 1990). Participants were randomly assigned
counterbalanced orders of three doses of galantamine (0 mg=placebo, 4 mg,
and 8 mg), an AChEI that is readily accessible, fast acting and has a mild side
effect profile. On three consecutive nights, participants awoke approximately
4.5 hours after lights out (after approximately the 3rd REM cycle), recalled a
dream, ingested the capsules and stayed awake for at least 30 minutes.
Participants then returned to sleep practicing the MILD technique. After each
subsequent awakening, participants rated their dreams on a range of variables
including lucidity, recall, vividness, bizarreness, complexity, affect, cognitive
clarity, metacognition and control. Full reports of lucid dreams were also
collected.

Galantamine was found to significantly increase the frequency of lucid

dreaming in a dose-related manner. Increased incidence of lucid dreaming was
observed for both 4 mg (27% of participants) and 8 mg (42% of participants)
doses compared to 14% of participants for the active placebo procedure (which
included sleep interruption and MILD). Galantamine was also found to be
associated with significantly increased sensory vividness and environmental
complexity, which might be expected given the general intensification of REM
sleep, and associated dreaming, triggered by cholinergic stimulation (Riemann,
Gann, Dressing, Muller and Aldenhoff, 1994).

Another recent double blind, placebo-controlled study conducted by Sparrow,

Hurd, Carlson and Molina, 2018) also tested the effect of galantamine on lucid
dreaming. 35 participants completed an eight-night study that tested the effect
of 8 mg of galantamine paired with 40 minutes of sleep interruption (termed
“Wake-Back-to-Bed” (WBTB) in the study). The study additionally tested
combining galantamine with middle-of-the-night meditation and the imaginary
reliving of a distressing dream (termed meditation and dream reliving or MDR;
Sparrow, Thurston and Carlson, 2013). The study included pre- and post-
baseline nights and six conditions: 1) WBTB; 2) WBTB + placebo; 3) WBTB
+ galantamine; 4) MDR; 5) MDR + placebo; and 6) MDR + galantamine.
MDR conditions matched the 40 minutes of sleep interruption in the WBTB
conditions. Lucid dreams were measured with self-reports on the dream
lucidity scale (DLS; Sparrow et al., 2013), which in this study included three
categories: 0=non-lucid, l=pre-lucid (which included either “questioning things
in the dream without actually concluding that you were dreaming” or “doing
things that are ordinarily impossible to do”), or 2=lucid.

Both galantamine conditions (WBTB + galantamine; MDR + galantamine)

significantly increased self-ratings of lucidity on the DLS compared to the
other conditions. However, no significant difference was observed between

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 24/61
18/7/2021 The cognitive neuroscience of lucid dreaming

WBTB + galantamine and MDR + galantamine. The number of participants

who had a lucid dream in each condition was not reported, only the conditional
means for the DLS, which reflects the effect collapsed across both pre-lucid
and lucid dreams. We therefore contacted the authors for this information in
order to compare the results of this study to the study by LaBerge et al.
(2018b). 9% of participants reported a lucid dream in the WBTB + placebo
condition and 11% in the MDR + placebo, whereas 40% of participants
reported a lucid dream in the WBTB + galantamine and 34% in the MDR +
galanatamine (S. Sparrow, personal communication, December 17, 2018).
Overall, therefore, these results are comparable to the effect of 8 mg
galantamine observed by LaBerge and colleagues.

5.2. Effects of L-alpha glycerylphosphorylcholine (α-GPC) lucid

dreaming
In contrast to the positive findings for AChEIs, a double blind randomized
placebo-controlled study found no significant effect of 1200 mg of the ACh
precursor L-alpha glycerylphosphorylcholine (α-GPC) on the frequency of
lucid dreams in 33 participants with varying degrees of lucid dreaming
experience (Kern, Appel, Schredl and Pipa, 2017). One interpretation of this
result is that, in contrast to AChEIs, α-GPC is not effective for inducing lucid
dreams, perhaps due to differences in the neurobiological effects of choline—
an ACh precursor—and AChEIs. However, participants in this study appear to
have received no training in mental set, such as recalling and attending to
dreams in an effort to become lucid. Thus, an alternative, not mutually
exclusive, interpretation is that training in at least the minimal mental set for
lucid dream induction is needed for pharmacological (and other) interventions
to effectively increase the frequency of lucid dreams.

5.3. General discussion of pharmacological induction of lucid

dreaming
Overall, these data provide strong initial evidence that cholinergic
enhancement with AChEls, and galantamine in particular, facilitates a state of
the brain favorable to lucid dreams. However, a limitation of all
pharmacological studies on lucid dreaming performed to date is that they were
not conducted in a sleep laboratory and there was therefore no validation of
lucid dreams with eye-signaling methods. It will be important to follow up
these results with sleep laboratory studies to objectively validate lucid dreams
with polysomnographic recording. Such studies would also be valuable to
investigate the physiological effects of galantamine on the brain during REM
sleep, and which effects are predictive of lucidity. Given the high success rate
of lucid dreams in the combined induction protocol with cholinergic
stimulation reported by LaBerge, LaMarca and Baird (2018) and Sparrow et al.

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 25/61
18/7/2021 The cognitive neuroscience of lucid dreaming

(2018), studies of galantamine have the potential to enable efficient collection

of large sample sizes in electrophysiological and neuroimaging studies of lucid
dreaming.

The mechanism by which AChEls facilitate lucid dreams remains unclear.

There are several, not mutually exclusive, possibilities, including increasing
REM sleep intensity/phasic activation, influencing the brain regions/networks
associated with lucid dreaming, and influencing cognitive processes associated
with becoming lucid. In general, it is known that AChEls inhibit the metabolic
inactivation of ACh by inhibiting the enzyme acetylcholinesterase (AChE),
leading to accumulation of ACh at synapses. Furthermore, ACh and its
agonists as well as AChE and its antagonists are involved in the generation of
REM sleep (Amatruda et al., 1975; Gillin et al., 1985; Velazquez-Moctezuma
et al., 1991). For example, evidence suggests that REM sleep is controlled by
cholinergic neurons in the brainstem (Baghdoyan, 1997; Hernandez-Peon,
Chavez-Ibarra, Morgane and Timo-Iaria, 1963), and studies have observed that
microinjection of the ACh agonist carbachol in the pontine area of the
brainstem results in REM sleep in both humans and animals (Amatruda et al.,
1975; Baghdoyan, 1997). Administration of galantamine has been associated
with increased phasic activity and shortened REM latency (Riemann et al.,
1994). The increased frequency of lucid dreams associated with AChEls could
therefore plausibly be related to its effects on cholinergic receptors during
REM sleep, leading to longer, intensified REM periods with increased phasic
activity, which, as noted above, has been found to be associated with lucid
dreams (LaBerge et al., 1981a).

Beyond intensification of REM sleep/phasic activation, AChEls might also

directly act on cognitive processes associated with lucidity and their neural
underpinnings. One key question is whether AChEIs could facilitate lucid
dreaming through increasing activation within the network of frontopolar-
temporo-parietal areas observed in the neuroimaging studies of Dresler et al.
(2012) and Baird et al. (2018a). The relationship between cholinergic
modulation and frontoparietal activation is complex and depends on the task
context and population under study (see Bentley, Driver and Dolan, 2011 for a
review). However, pro-cholinergic drugs in general tend to increase
frontoparietal activity in conditions in which these areas show low baseline
activation, which is thought to reflect increased attentional-executive functions
(Bentley et al., 2011). Given that frontoparietal activity is typically suppressed
during REM sleep (Braun et al., 1997; Maquet et al., 1996), it is plausible that
AChEIs could increase activation within this network during REM sleep
dreaming.

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 26/61
18/7/2021 The cognitive neuroscience of lucid dreaming

Notably, AChEls are also prescribed to manage the cognitive symptoms of

Alzheimer’s disease (Koontz and Baskys, 2005). Theoretically, another way
that AChEls could facilitate lucid dreams is therefore through their effect on
memory. For example, AChEIs could enhance the ability to remember to
recognize that one is dreaming (a form of prospective memory), which is the
core of the MILD technique for lucid dream induction that participants engaged
in during the study by LaBerge, LaMarca and Baird (2018b). However,
evidence for cognition enhancing effects of AChEls in healthy subjects,
particularly for single doses, is sparse (Dresler et al., 2018), rendering the
theoretical possibility of a memory-mediated effect on dream lucidity unlikely.
Overall, it remains unclear whether galantamine also exerts a direct influence
on cognitive processes associated with lucidity, and the MILD technique in
particular, or whether it merely optimizes the physiological conditions for such
techniques.

One last possibility is that AChEIs could influence lucidity indirectly by

affecting other neuromodulators. For example, evidence suggests that AChEls
also increase systemic norepinephrine and dopamine (Cuadra, Summers and
Giacobini, 1994; Giacobini, Zhu, Williams and Sherman, 1996). It is therefore
possible that the increase in lucid dreams associated with AChEI might instead
be directly linked to aminergic modulation that occurs as a result of the
increases in ACh. Additional research will be needed to understand how the
neuromodulatory changes caused by AChEIs stimulate lucid REM sleep
dreaming. Studies using Positron Tomography (PET) or pharmaco-fMRI would
be valuable to address this issue.

Several other pharmacological substances have been suggested to increase the

frequency of lucid dreams, including various types of supplements and drugs
(e.g., Yuschak, 2006). For instance, recreational drugs such as alcohol, cocaine
and cannabis have been reported to be associated with lucid dreaming. These
substances suppress REM sleep (Roehrs and Roth, 2001; Schierenbeck,
Riemann, Berger and Hornyak, 2008), which leads to a phenomenon referred
to as REM rebound, in which longer REM sleep periods occur following REM
sleep suppression (Vogel, 1975). Intensified, prolonged REM sleep as a result
of REM rebound could potentially increase lucid dream frequency, particularly
in individuals predisposed to have lucid dreams or with prior experience in
lucid dreaming. Another example is LSD, since there is some evidence that it
can prolong REM sleep periods at some doses (Muzio, Roffwarg and Kaufman,
1966), which could potentially be favorable to lucid dreaming. To our
knowledge, however, no studies have systematically evaluated whether these
substances, or other substances not reviewed here, increase the incidence of
lucid dreams. Furthermore, it is prudent to remain cautious about such claims

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 27/61
18/7/2021 The cognitive neuroscience of lucid dreaming

given the placebo effect. Placebo-controlled studies will be essential to

substantiate any purported effects of pharmacological substances on lucid
dreaming.

6. Induction of lucid dreams with transcranial electrical

brain stimulation
Two studies have attempted to induce lucid dreams through transcranial
electrical stimulation of the frontal cortex during REM sleep. Stumbrys,
Erlacher and Schredl (2013b) tested direct current stimulation and Voss et al.
(2014) tested alternating current stimulation. We review each of these studies
in turn.

6.1. Effects of frontal transcranial direct current stimulation on

lucid dreaming
In an investigation of the effect of transcranial direct current stimulation
(tDCS) on lucid dreaming, Stumbrys et al. (2013b) applied either tDCS or
sham stimulation (counterbalanced across nights) over a frontolateral scalp
region in 19 participants. Stimulation was delivered through two pairs of
electrodes with anodes at positions F3 and F4, respectively, and cathodes at the
supraclavicular area of the same side. Stimulation was applied during all REM
sleep periods except the first for two consecutive nights in the sleep laboratory.
In total, 109 stimulations were performed, after which participants were
awakened to complete a dream report.

Compared to sham stimulation, tDCS resulted in a small numerical increase in

self-ratings of the unreality of dream objects as assessed by the Dream Lucidity
Questionnaire (DLQ; Stumbrys et al., 2013b). Post-hoc analyses revealed that
this effect was seen only in subjects with a high baseline frequency of lucid
dreams, but not in participants with little or no lucid dreaming experience.
However, tDCS did not significantly increase the number of dreams rated by
judges to have a clear indication of lucidity: seven dreams in total, three from
sham stimulation and four from tDCS stimulation. Furthermore, only one lucid
dream in total was confirmed by eye signaling, which was in the stimulation
condition. Given a difference of only one lucid dream between stimulation and
sham conditions for either of these two assessment criteria, overall frontal
stimulation with tDCS as tested in this study does not appear to be a reliable
method for inducing lucid dreams.

6.2. Effects of frontal transcranial alternating current stimulation

on lucid dreaming

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 28/61
18/7/2021 The cognitive neuroscience of lucid dreaming

A study by Voss et al. (2014) reported a more pronounced increase in lucid

dreaming by applying transcranial alternating current stimulation (tACS) in the
gamma frequency band over the frontal cortex. The study tested 27 participants
for up to four nights in the sleep laboratory. tACS was applied for 30 seconds
after two minutes of uninterrupted REM sleep to frontolateral scalp regions at
several different frequencies (2, 6, 12, 25, 40, 70 or 100 Hz or sham
stimulation). Stimulation was delivered through two pairs electrodes with
anodes at positions F3 and F4, respectively, and cathodes over the mastoids
close to TP9 and TP10, respectively. Participants were then awakened and
completed a dream report and the Lucidity and Consciousness in Dreams
(LuCiD) scale (Voss et al., 2013). The LuCiD scale measures dream content on
several different factor-analytically derived dimensions, including insight,
control, thought, realism, memory, dissociation and affect.

The authors reported they were able to induce lucid dreams with a success rate
of 58% with 25 Hz stimulation and 77% with 40 Hz stimulation. However, it is
important to note how lucid dreams were classified in this study: instead of
assessment of lucid dreams with eye signaling, self-report, or through statistical
analysis of judges’ ratings of dream reports, as in Stumbrys et al. (2013b),
dreams were assumed to be lucid if subjects reported “elevated ratings (>mean
+ 2 s.e.) on either or both of the LuCiD scale factors insight and dissociation”.
While dissociation scores (i.e., “seeing oneself from the outside” or a “3rd
person perspective”) have been found to be increased in lucid dreams before
(Voss et al., 2013), dissociation in the sense of adopting a 3rd person
perspective has never been considered a defining feature of lucid dreams per se
(e.g., DeGracia and LaBerge, 2000; Gackenbach and LaBerge, 1988; Green,
1968; LaBerge, 1985, 1990). It is therefore controversial to classify dreams as
lucid based solely on higher ratings of dissociation.

The insight subscale corresponds more closely to the standard definition of

lucid dreams adopted by other researchers as well as the general public. Mean
ratings in the insight subscale increased from approximately 0.1-0.2 in the
sham stimulation to 0.5-0.6 in the 25 Hz or 40 Hz stimulation conditions,
similar to the effects in the dissociation subscale, which was approximately
0.9-1.2. However, the scale anchors ranged from 0 (strongly disagree) to 5
(strongly agree), indicating that, on average, in both the 25 Hz and 40 Hz
stimulation conditions, participants disagreed that their dreams had increased
insight. Moreover, in the original validation of the LuCiD scale, non-lucid
dreams scored on average at 0.3 or 0.8 on the insight scale (depending on
whether the assessment was laboratory or survey based), whereas lucid dreams
scored at 3.2 or 3.5 (Voss et al., 2013). Thus, though significantly stronger in
relation to sham simulation, mean responses of 0.5-0.6 in the 25 and 40 Hz
stimulation conditions were much lower than the values reported for lucid
dreams in the validation study, and still on the non-lucid (disagree that the
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 29/61
18/7/2021 The cognitive neuroscience of lucid dreaming

dream contains insight) end of the scale spectrum in absolute values. Overall,
therefore, the results of this study appear to be comparable to the tDCS finding
of Stumbrys et al. (2013b) in that prefrontal tACS gamma band stimulation
induced numerical increases in some measures of dream content, but does not
appear to have lead to increases in the number of lucid dreams when defined in
the traditional sense of being aware of dreaming while dreaming.

6.3. General discussion of induction of lucid dreaming with

electrical brain stimulation
In summary, studies examining induction of lucid dreams with electrical brain
stimulation (tDCS and tACS) have thus far observed intriguing effects on
dream cognition, but a method for reliably inducing lucid dreams by electrical
stimulation of the brain is still yet to be identified. We think this is a
particularly interesting direction for upcoming work. Future studies might
consider stimulating a wider number of brain areas and different types of
stimulation. For example, transcranial magnetic stimulation (TMS) is another
method of noninvasive brain stimulation that could be used to attempt to
induce lucid dreams that has not yet been examined (Noreika, Windt,
Lenggenhager and Karim, 2010; Mota-Rolim et al., 2010). In contrast to tACS
or tDCS, high-frequency repetitive TMS (rTMS) stimulation sequences can be
used to increase neuronal excitability in focal areas of the cortex (e.g., Hallett,
2007). Several practical challenges with application of TMS during sleep
include the auditory artifacts produced by the TMS coil as well as tactile
sensations on the scalp during stimulation, which may lead to awakenings.
However, noise masking has been used to prevent subjects from hearing the
clicks associated with TMS pulses (e.g., Nieminen et al., 2016), and scalp
sensations could be decreased, for example, by reducing stimulation intensity
or potentially by application of a topical anesthetic cream.

Studies of electrical brain stimulation have also thus far only tested a small part
of the parameter space and there are many other stimulation protocols that
appear to be worth evaluating. For example, given the neuroimaging results
reviewed above, synchronous frontoparietal tACS—in which synchrony is
increased between frontal and parietal regions by simultaneous stimulation of
these regions (e.g., Violante et al., 2017)—is another stimulation method that
would be interesting to examine. Finally, as noted above, these methods are
likely to maximize their effect when participants are trained in at least the
minimal mental set for lucid dream induction, which was not done in either the
study by Voss et al. (2014) or Stumbrys et al. (2013b).

7. Lucid dreaming as a methodology for the cognitive

neuroscience of consciousness

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 30/61
18/7/2021 The cognitive neuroscience of lucid dreaming

Psychophysiological studies of non-lucid dreams have been used to study

neural correlates of conscious experiences during sleep (Perogamvros et al.,
2017; Siclari et al., 2017). However, there are significant limitations to this
approach. Specifically, while methods such as “serial awakenings” are useful
for contrasting the global presence vs. absence of dream experience during
sleep (Siclari et al., 2017), it is an inefficient method to collect data on specific
conscious contents during sleep. For instance, given that non-lucid dreamers
usually have no control over their dream content, these studies typically
employ a shot-in-the-dark approach, in which large numbers of sleep
recordings are made and small subsets of data in which the content of interest
appears by chance are extracted. Additionally, and perhaps most importantly,
establishing temporally precise correlations between retrospective dream
reports and physiological measurements is a substantial challenge. Lucid
dreaming provides ways to overcome several of these challenges. For example,
as mentioned above, lucid dreamers can conduct specific tasks within REM
sleep dreams, enabling experimental control over dream content. Furthermore,
as noted, participants can be trained to time-stamp the onset and offset of
particular content or actions with eye movement signals, which provides a way
to obtain more precise correlations between conscious experiences and
physiological measurements during sleep (Dresler et al., 2011; LaBerge, 1990;
LaBerge, Greenleaf and Kedzierski, 1983). In this section we briefly
summarize several recent studies that illustrate how lucid dreaming can be used
as a methodology in the cognitive neuroscience of consciousness.

7.1. Activation of sensorimotor cortex during dreamed movement

in REM sleep
Dresler et al. (2011) used lucid dreaming to test whether a motor task
performed during dreaming elicits neuronal activation in the sensorimotor
cortex. Participants made a series of dreamed left and right hand clenches in
their lucid dreams and marked the start and end of the sequences of clenches
with LRLR eye movements. Specifically, participants clenched their left hand
in the dream ten times, then signaled LRLR, then clenched their right hand in
the dream ten times, then signaled LRLR, and continued repeating this
sequence for as long as possible until awakening. Additionally, participants
performed an executed hand-clenching task as well as imagined hand-
clenching task during wakefulness for comparison. Six participants with prior
experience in lucid dreaming participated in the study. Of these, two
participants succeeded in performing the task during lucid REM sleep: one
under simultaneous EEG-fMRI (in two different signal-verified lucid dreams)
and one under combined EEG-near-infrared spectroscopy (NIRS) recording
(again in two different signal-verified lucid dreams).

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 31/61
18/7/2021 The cognitive neuroscience of lucid dreaming

Contrasting left vs. right fist clenches, increased BOLD signal in the
contralateral sensorimotor cortex was observed in both lucid dreams of the
fMRI experiment, as well as in waking and imagination conditions. Compared
to executed hand clenches during wakefulness, however, BOLD signal
increases during dreaming in contralateral sensorimotor cortex were more
localized, which could indicate either weaker activation or more focal
activation of hand areas only. BOLD signal fluctuations during dreaming were
approximately 50% of those observed for executed hand clenches during
wakefulness. Correspondingly, the NIRS data showed increased oxygenated
hemoglobin and decreased deoxygenated hemoglobin in the contralateral
sensorimotor cortex during dreamed hand clenching. This hemodynamic
response was also observed in the supplementary motor area, which is involved
in the timing, monitoring and preparation of movements (Goldberg, 1985).
This differed with the fMRI data in which no significant differences in the
supplementary motor area were found. Interestingly, during dreamed hand
clenching, hemodynamic responses were smaller in the sensorimotor cortex but
of similar amplitude in the supplementary motor area when compared to overt
motor performance during wakefulness.

Overall, these data suggest that the pattern of brain activation observed during
dreamed motor execution overlaps with motor execution during wakefulness.
However, given the different patterns of activation, the data may also suggest
that the interactions between the supplementary motor area, somatosensory and
sensorimotor cortex differs between REM sleep dreaming and waking. The
authors suggest that the reduced activation in sensorimotor cortex could be due
in part to the lack of sensory feedback as a result of REM sleep atonia.
However, given that this study consisted of two case reports—one for each
imaging modality—the data should be interpreted cautiously. Clarification of
the neural correlates of dreamed motor activity, as well as clarification of any
differences in this network compared to overt motor performance, awaits
larger-scale group-level studies. Nevertheless, this experiment provides a
proof-of-concept that neuroimaging of specific dream content can be
accomplished using lucid dreaming as a methodology.

7.2. Voluntary control of central apneas during REM sleep

dreaming
A similar type of experiment was recently undertaken by Oudiette et al. (2018)
to examine respiratory behavior during REM sleep dreaming. Specifically, the
researchers used lucid dreaming to investigate whether irregular breathing
during REM sleep has a cortical origin and whether such breathing patterns can
reflect the mental content of dreams. This research follows up on a study from
LaBerge and Dement (1982) which observed tachypnea during volitional rapid
breathing and apnea during voluntary breath holding during lucid REM sleep
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 32/61
18/7/2021 The cognitive neuroscience of lucid dreaming

dreaming. Polysomnography and respiration were recorded during early

morning naps from 21 patients with narcolepsy who reported frequent lucid
dreams. Participants were instructed to modify their dream scenario so that it
involved vocalizations or an apnea (e.g., diving under water)—two respiratory
behaviors that purportedly require a cortical control of respiration (McKay,
Adams, Frackowiak and Corfield, 2008). Participants signaled the onset of
lucidity as well as the start and end of the respiration tasks with LRLR eye
movement signals. Participants also performed the task during waking by
actually executing the respiratory task as well as during waking imagination. In
total, 32 lucid REM sleep naps were included in the analysis. Physiological
data was scored for the presence of central apneas, which were defined as
“cessation of nasal flow for more than 10 s in the absence of cyclic thoracic
and abdominal movements” as well as preparatory breaths preceding the
central apnea.

In 16 out of the 32 signal-verified lucid dreams, the physiological data showed

the expected respiratory behavior (e.g., a central apnea, in some cases including
preparatory breaths), which was appropriately marked by LRLR signals and
confirmed by dream reports of becoming lucid and executing the task. In the
remainder of cases, participants either failed to control the dream (N=2) or
appropriately execute the LRLR signals (N=2), or there was incongruence
between the report and the data (participants either did not recall performing
the task (N=8) or there was no physiological evidence of the task despite a
report of completing the task (N=4)). As the authors discuss, the incongruences
between reports and physiological data may in part have been attributable to
the fact that reports were obtained at the end of the 30-minute nap sessions
rather than awakening subjects directly after completing the task. Thus, in
some cases this resulted in a long delay between the dream task and the report.
Despite the presence of these ambiguous cases, overall the data show that
voluntarily control of central apneas during REM sleep occurred in a majority
of participants.

As the authors discuss, the pons is hypothesized to regulate cessation of

breathing, which assimilates input from supra-brainstem structures and inhibits
medullary respiratory neurons (McKay et al., 2008). Thus, they conclude that
the fact that voluntary control of central apneas is possible during REM sleep
suggests that this cortico-pontine drive is preserved during REM sleep.
However, it remains unclear from this study to what extent non-lucid dreams
containing this type of mental content (for example, diving under water), would
result in central apneas. Indeed, as the authors note, some participants reported
that they voluntarily held their breath when diving under water in the dream
even though they did not feel that they had to. In general, it remains unclear
whether central apneas as observed in the study are linked to the voluntary
control of respiration enabled during lucid dreams in particular or whether they
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 33/61
18/7/2021 The cognitive neuroscience of lucid dreaming

systematically occur in dreams with this type of content/scenario. In either

case, however, the data support the conclusion that voluntarily control of
central apneas is possible during REM sleep.

7.3. Smooth pursuit eye movements during visual tracking in REM

sleep dreaming
One last recent example of the use of lucid dreaming as methodology in
cognitive neuroscience is provided by LaBerge, Baird and Zimbardo (2018a),
who addressed the question of whether smooth pursuit eye movements
(SPEMs) occur during tracking of a slowly moving visual target during lucid
REM sleep dreaming. Seven participants with high reported dream recall and
frequency of lucid dreams participated in the study. Participants marked the
moment of lucidity as well as the initiation and completion of the tracking
tasks with LRLR eye movement signals. After making the LRLR signal,
participants performed one of two eye-tracking tasks: circle tracking or one-
dimensional movement tracking on the horizontal meridian. For each tracking
task, participants followed the tip of their thumb with their gaze as they traced
the pattern. Participants performed the tracking tasks in three conditions: 1)
lucid REM sleep dreaming (“dreaming”), 2) awake with eyes open
(“perception”) and 3) tracking the imagined movement while awake with eyes
closed (“imagination”). Eye movements were recorded with direct current
EOG and subjected to a validated algorithm that classifies saccades, fixations
and smooth pursuit eye movements (Komogortsev and Karpov, 2013).

The results revealed that intentional slow tracking of visual motion (of both
circles and lines) during lucid REM sleep dreams results in SPEMs. Pursuit eye
movements in REM sleep dreams did not significantly differ from pursuit
during waking perception, and both were characterized by high pursuit ratios
and low saccade rates. In contrast, tracking in imagination was characterized by
low pursuit with frequent saccadic intrusions. A Bayesian classification model
that included pursuit ratio and saccade rate discriminated both REM sleep
dreaming and perception from imagination with greater than 98% accuracy.

Together, these findings help to address several broad questions within

cognitive neuroscience and sleep research. First, the data provide empirical
evidence for a difficult to test question that has been asked at least since
Aristotle: “Are dreams more like perception or imagination?” (Nir and Tononi,
2010). Based on the smooth tracking behavior, the findings of this study
suggest that, at least in this respect, the visual quality of REM sleep dream
imagery is more similar to waking perception than imagination. Second, the
findings help to address a longstanding question in the psychophysiology of
sleep since the discovery of REM in the 1950’s: whether the eye movements of
REM sleep track the gaze of the dreamer—the so-called “scanning hypothesis”

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 34/61
18/7/2021 The cognitive neuroscience of lucid dreaming

(for a review, see Arnulf, 2011). By demonstrating that individuals can trace
circles and lines with their gaze while in EEG-verified REM sleep, which can
be recorded with EOG, the data provide unique evidence that shifts in the
perceived gaze direction in dreams give rise to the appropriate corresponding
eye movements. This is consistent with the view that a subset of eye
movements during REM sleep are linked to the direction of subjective gaze
during dreams. Lastly, the results also provide a novel source of data for a
central research question on the topic of smooth pursuit in humans and non-
human primates that dates back at least forty years. Specifically, an enduring
question has been whether a physical stimulus and/or retinal image motion is
necessary to drive the neural circuitry of smooth pursuit (Spering and
Montagnini, 2011). By demonstrating that sustained SPEMs can be elicited in
the absence of visual input to the cortex, as is the case during REM sleep, the
findings provide strong evidence that neither a physical motion stimulus nor
readout of retinal image motion are necessary for SPEMs.

7.4. General discussion of lucid dreaming as experimental

methodology
Altogether, these studies illustrate the potential of lucid dreaming as an
experimental methodology for the study of consciousness in general and REM
sleep dreaming in particular. The fact that lucid dreamers can exercise
volitional control over their actions while dreaming and conduct experiments
from within EEG-verified REM sleep dreams opens up the ability to perform
experiments that would otherwise be difficult or impossible to conduct. This
methodology also has the potential to more efficiently target specific research
questions. As discussed above, lucid dreaming enables both experimental
control over the content of dreams as well as a way to establish precise
psychophysiological correlations between the contents of consciousness during
sleep and physiological measures in a way that is not possible in studies of
non-lucid dreaming. In sum, lucid dreaming provides a methodology that
allows for new ways of studying the relationship between consciousness and
neurophysiological processes, and, as the above studies highlight, shows
emerging potential for research on consciousness in sleep science.

8. Clinical cognitive neuroscience of lucid dreaming

Research on lucid dreaming is not only relevant to the neuroscience of
consciousness but could also have clinical implications. While a detailed
treatment of the clinical applications of lucid dreaming is beyond the scope of
this review (see e.g., Garfield, Fellows, Halliday and Malamud, 1988), here we
briefly note several interesting applications and future directions with particular
relevance for cognitive neuroscience.

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 35/61
18/7/2021 The cognitive neuroscience of lucid dreaming

8.1. Lucid dreaming in the treatment of persistent nightmares

The most researched application of lucid dreaming is to treat recurring
nightmares (Abramovitch, 1995; Holzinger, Klösch and Saletu, 2015;
Spoormaker and Van Den Bout, 2006; Tanner, 2004; Zadra and Pihl, 1997).
Lucid dreaming was included by the American Academy of Sleep Medicine in
their therapy suggestions for nightmare disorder (Morgenthaler et al., 2018).
Conceptually, the idea is that becoming lucid during a nightmare should allow
the dreamer to realize the content of the nightmare is not real and thus has no
reason to be afraid, and to be able to exert control over the dream and/or work
with the psychological content of the nightmare (LaBerge and Rheingold,
1990; Mota-Rolim and Araujo, 2013). Neurocognitive models of nightmare
generation suggest a hyper-responsivity of the amygdala coupled with a failure
of prefrontal regions to dampen this activation (Levin and Nielsen, 2007).
Studying the influence of lucidity on nightmare resolution could therefore
provide an interesting opportunity to study top-down regulation of amygdala
activation, perhaps through reactivation of prefrontal regions (Dresler et al.,
2012).

A case study (Zadra and Pihl, 1997), and one small, controlled pilot-study
(Spoormaker and Van Den Bout, 2006) have found that lucid dreaming therapy
was effective in reducing nightmare frequency. Also a study of 32 patients who
suffer from frequent nightmares found a slight advantage of lucid dreaming as
add-on to Gestalt therapy compared to the latter alone (Holzinger et al., 2015).
In contrast, a larger online study did not find any additional effect of lucid
dreaming therapy as an add-on to other cognitive-behavioral techniques, such
as imagery rehearsal therapy (Lancee, Van Den Bout and Spoormaker, 2010),
although low power and high dropout rates (>70%) limited the scope of the
conclusions. Controlled experiments with larger sample sizes are needed to
further evaluate the potential usefulness of lucid dreaming for the treatment of
recurring nightmares and related disorders, as well as to examine the neural
mechanisms of these interactions.

8.2. Lucid dreaming and narcolepsy

Consistent with a potential beneficial role of lucid dreaming in recurring
nightmares, patients with narcolepsy report that becoming lucid provides
psychological relief (Rak et al., 2015). Generally, narcolepsy patients
experience longer, more complex, and more vivid dreams and more frequent
nightmares than healthy subjects (Mazzetti et al., 2010). Moreover, patients
with narcolepsy report higher reflective consciousness within dreams (Fosse,
2000) and accordingly a considerably increased lucid dreaming frequency
(Dodet et al., 2014; Rak et al., 2015). The mechanisms for this increased lucid
dreaming frequency are not entirely understood yet: nightmares often lead to

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 36/61
18/7/2021 The cognitive neuroscience of lucid dreaming

the insight into the current dream state, however it is currently unclear if an
increased nightmare frequency causes an increased lucid dreaming frequency
in narcolepsy, or if the strongly increased frequency of REM sleep in
narcolepsy affects nightmares and lucid dreaming independently. In particular
sleep onset REM (SOREM) episodes appear to prompt lucid dreams (Dodet et
al., 2014), which is in line with the dream lucidity-enhancing effects of the
early morning “Wake-Back-to-Bed” procedure in healthy subjects. Of note,
patients with narcolepsy make a clear distinction between their experiences of
lucid dreaming and sleep paralysis (Dodet et al., 2014), and the increased lucid
dreaming frequency in this patient group does not appear to be associated with
medication use (Rak et al., 2014). It has been speculated whether, potentially as
a result of a considerably increased lucid dreaming experience, narcoleptic
patients might exhibit different neurophysiological correlates of lucid dreaming
(Dodet et al., 2014).

8.3. Lucid dreaming as a model of insight in psychiatric conditions

Another area in which research on lucid dreaming might be applied is in
psychiatric disorders in which patients suffer from lack of insight into their
state. Indeed, there is considerable overlap between preliminary findings of
brain regions related to insight into the dream state and brain regions impaired
in psychotic patients with disturbed insight into their pathological state (Dresler
et al., 2015; Mota, Resende, Mota-Rolim, Copelli and Ribeiro, 2016). The
concept of insight is becoming an increasingly important area in schizophrenia
research (e.g., Baier, 2010), for example, where between 50 and 80% of
patients diagnosed with schizophrenia have poor insight into the presence of
their disorder (Lincoln, Lullmann and Rief, 2007). Evidence suggests that poor
insight in turn leads to more relapses, re-hospitalizations and poorer therapy
success (Mintz, Dobson and Romney, 2003). With regard to dreaming, lack of
insight into the current state characterizes almost all dream experiences, with
the exception of lucid dreaming. Thus, lucid dreaming could potentially be
used as a model for at least some cognitive dimensions of insight (David,
1990). In this context it is interesting to note that historical approaches to
psychosis used the term lucid to denote the awareness of the patient into his or
her illness (Berrios and Markova, 1998). At the current time, these ideas
remain highly speculative, but this appears to us to be an area worthy of
additional research.

8.4. Using lucid dreaming to establish brain activity markers of

self-awareness
Another potential clinical application of research on lucid dreaming is in the
development of neuroimaging-based diagnostic markers of awareness. Such
measures have the potential to improve the diagnosis and monitoring of

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 37/61
18/7/2021 The cognitive neuroscience of lucid dreaming

patients who are unresponsive due to traumatic injury, aphasia, motor

impairment, or other physical limitations. Neurobiological studies of lucid
dreaming could provide information relevant to development of these brain
activity markers since, in addition to assessing a patient’s capacity for primary
consciousness (i.e., if a patient can see, hear or experience pain), an important
clinical goal is to assess whether patients, who may nevertheless be
unresponsive via behavioral assessment, are aware of themselves and their state
(Laureys, Perrin and Bredart, 2007). This information is critical to making
appropriate therapeutic choices and determining prognosis (Laureys et al.,
2007). Research indicates that the bedside behavioral assessment of such
patients is challenging and has a high rate of misdiagnosis (over 40% according
to some studies) (Laureys, Owen and Schiff, 2004; Schnakers et al., 2009).
Accordingly, identification of a reliable brain activity marker of a patients’
capacity for self-awareness—which could be informed by studying the changes
in brain activity between lucid and non-lucid REM sleep dreaming—is an
important goal. Research on lucid dreaming has the potential to contribute a
valuable source of data to this question since, as noted above, the contrast
between lucid and non-lucid REM sleep is perhaps the only one currently
known in which a global loss and recovery of self-awareness can be contrasted
within the same vigilance state in healthy individuals.

9. The measurement of lucid dreaming in cognitive

neuroscience research
In this last section, we review methodological issues and strategies in the
measurement of lucid dreaming in cognitive neuroscience research. We review
the validation of lucid dreaming both physiologically and with questionnaires,
and discuss best-practice procedures to investigate lucid dreaming in the sleep
laboratory.

9.1. Eye signaling methodology

The eye signaling methodology is the gold standard in lucid dreaming research,
as it allows for objective confirmation of lucid dreams through the execution of
pre-agreed upon sequences of eye movements recorded with the EOG during
EEG-verified REM sleep (Figure 1). While there are some types of research
studies (e.g., field studies) where eye signaling is not possible or not
applicable, we recommend considering this method as the standard practice for
laboratory-based studies of lucid dreaming. In general, most recent studies
have adhered to this convention; however, there is some confusion about how
to properly instruct participants in executing the eye movements, which has
resulted in studies implementing several different variations of the method. For

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 38/61
18/7/2021 The cognitive neuroscience of lucid dreaming

instance, while some experimenters instruct participants to move their eyes left
and right (e.g., Dresler et al., 2012), in other cases participants have been
instructed to “scan the horizon” from left to right (Dodet et al., 2014).

Differences in eye signaling instructions could partly account for the varying
degrees of effectiveness in objectively identifying the eye signals across
studies. For example, Dodet et al. (2014) reported that while three control
participants and twelve narcoleptic patients reported making the eye signal in
overnight EEG recordings, none of these could be objectively identified, and
only about half of reported signals could be unambiguously identified from nap
recordings. While it is possible that some of these instances represent cases
where participants misremembered or misreported a lucid dream, it is likely
that this high rate of ambiguous eye movement signals is partly attributable to
the specific instructions that were given. Similarly, while the exact instructions
provided to participants was not described, Voss et al. (2009) stated that they
were unable to obtain reliable eye signals using the standard signaling method
and therefore attempted to develop a novel signaling method employing two
sets of eye-signals separated by a pause. Again, suboptimal results could
plausibly be due to the instructions provided and the way the eye signals were
executed by participants in the study.

One reason for the confusion and diverse instructions given for the eye
signaling methodology is that a standardized set of instructions for making the
signals has never been published. Here we report a simple set of instructions
adapted from LaBerge et al. (2018a) that has been reported to yield nearly
100% correspondence between subjective reports of eye signals and objective
EOG recordings. The instruction is as follows:

When making an eye movement signal, we would like you to look all the
way to the left then all the way to the right two times consecutively, as if
you are looking at each of your ears. Specifically, we would like you to
look at your left ear, then your right ear, then your left ear, then your right
ear, and then finally back to center. Make the eye movements without
moving your head, and make the full left-right-left-right-center motion as
one rapid continuous movement without pausing.

Looking at the ears is one of the critical aspects of the instruction, as it

encourages full-scale eye movements without corresponding head movements.
These extreme and rapid consecutive eye movements make the signals easy to
discern in the horizontal EOG time series. The signals are of higher amplitude
than typical REMs, and have a distinctive shape (Figure 1) which can be
identified with template matching (LaBerge et al., 2018a). To optimize
execution of the eye signals, participants are given the opportunity to practice
the signals in the laboratory while awake and connected to the EOG, with an
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 39/61
18/7/2021 The cognitive neuroscience of lucid dreaming

opportunity to view the signals and receive feedback from the experimenter.
Additionally, participants practice making the eye signals in any lucid dreams
they have at home in the weeks leading up to the sleep laboratory visit, in order
to gain experience with executing the signals.

9.2. Questionnaire assessment of lucid dreaming

A related issue concerns how the phenomenology of lucid dreaming should
optimally be assessed in cognitive neuroscience research. Several
questionnaires have been developed to assess changes in conscious experience
during dreaming. For instance, the Metacognitive, Affective, Cognitive
Experience questionnaire (MACE; Kahan, LaBerge, Levitan and Zimbardo,
1997; Kahan and Sullivan, 2012) was designed to assesses the monitoring and
regulation of both cognitive and affective experience during both wakefulness
and sleep. In its latest form, it consists of ten items, including four self-
monitoring questions, three questions on self-reflective consciousness and
three questions that target self-regulatory behaviors. Another measure, the
Dream Lucidity Questionnaire (DLQ; Stumbrys et al., 2013b), is designed to
assess different aspects of lucidity within dreams. It consists of ten items,
scored on a 5-point scale: 0 – not at all, 1 – just a little, 2 – moderately, 3 –
pretty much, 4 – very much. The DLQ evaluates different types of awareness
(awareness of dreaming, awareness that the physical body is asleep, awareness
that dream characters and objects are not real, awareness of different
possibilities) and control (deliberately choosing an action, changing dream
events, dream characters, dream scenes, breaking physical laws). In a similar
manner, the Lucidity and Consciousness in Dreams scale (LuCiD, Voss et al.,
2013) includes eight subscales, derived from factor analysis of a sample of
lucid and non-lucid dream reports, which assess various dimensions of
dreaming experience and cognition: 1) Insight, 2) Control, 3) Thought, 4)
Realism, 5) Memory, 6) Dissociation, 7) Negative emotion, and 8) Positive
emotion.

All three questionnaires provide measures for evaluating how some content
dimensions might differ across lucid and non-lucid dreams. However, as
mentioned, questionnaires such as these are not sufficient to objectively
establish whether a participant had a lucid dream. It is worth noting that only
the DLQ in its first question (“I was aware that I was dreaming”) directly
queries whether the dreamer was lucid, and the MACE was never intended for
this purpose. Most studies using the DLQ and LuCiD questionnaires have
collected a dream report from participants in addition to the questionnaire
responses. We would like to emphasize the importance of this point: Instead of
relying on the inference of lucidity solely from questionnaire measures of
dream content, accurate assessment of lucidity can be facilitated by, in addition
to using the eye signaling method, collecting a full dream report from
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 40/61
18/7/2021 The cognitive neuroscience of lucid dreaming

participants. In making the dream report, participants are typically asked to

describe in as much detail as possible the narrative of the dream, including the
sequence of events and any thoughts, feelings or sensations that they
experienced. In dream reports for lucid dreams, the participant is also asked to
include a specific description of how they became lucid in the dream (for
example, by noticing an oddity of an event, action or person in the dream,
which is also known as “dream sign”) and also to explicitly note any eye
signals made at the appropriate instances in the dream narrative.

Following the collection of a full open-ended dream report, further

confirmation of lucidity and eye signaling can be accomplished with simple
follow-up questions, including, for example: 1) “Were you aware of the fact
that you were dreaming while you were dreaming?” (YES/NO), If YES: 2)
“How confident are you that you became lucid?” (0-4 scale), 3) “Did you have
a wake-initiated lucid dream (WILD) or a dream initiated lucid dream
(DILD)?” (DILD/WILD), 4) “Did you make the eye movement signal to
indicate that you became lucid?” (YES/NO), 5) “Please briefly describe how
you became lucid.” These example questions are not meant to be exhaustive,
but they illustrate the types of questions that in our view are useful to obtaining
an accurate and thorough assessment of lucid dreams following collection of a
full dream report.

9.3. Measurement of individual differences in lucid dreaming

Another related question facing researchers is how to measure individual
differences in lucid dream frequency, which has been done in inconsistent
ways, and could be improved in future research. A method used in several
studies consists of an 8-point scale that asks participants to self-rate the
frequency with which they experience lucid dreams, ranging from “never” to
“several times per week” (Schredl and Erlacher, 2004; Mota-Rolim et al.,
2013). While this method provides a straightforward coarse assessment of an
individual’s estimated frequency of lucid dreams that has shown high test-retest
reliability (Stumbrys, Erlacher and Schredl, 2013a), a limitation is that it does
not measure lucid dream frequency greater than several times per week. The
scale could be improved by including additional categories on the higher end of
the measure, including, for example, “Every night” and “Multiple times per
night.” While individuals who experience lucid dreams on a nightly basis
represent a very small percentage of respondents (according to Baird et al.
(2018a) approximately one in one thousand), optimally this kind of instrument
would enable a researcher to distinguish respondents that have lucid dreams
once or several times a week from those that have them every night or multiple
times per night. Indeed, these “virtuoso” lucid dreamers represent perhaps one
of the most interesting populations for cognitive neuroscience studies of
individual differences in lucid dreaming (Baird et al., 2018a).
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 41/61
18/7/2021 The cognitive neuroscience of lucid dreaming

A related method is to query the number of lucid dreams reported in a given

period of time (i.e., the last 6 months), which has the advantage of asking
participants to report a specific number rather than a coarse estimate. In
principle, this method has the potential to be more accurate and to capture
increased variance. However, some participants, particularly those with high
lucid dream rates, may not be able to recall all instances of their lucid dreams
within the requested time interval, and may therefore resort to heuristics when
answering the question, making it akin to simply asking participants to report
frequency using a multiple-choice scale. Furthermore, this method may not
accurately assess lucid dream frequency over longer periods of time – i.e., an
individual may normally experience lucid dreams frequently, but has not
experienced them as frequently during the last queried interval of time. If using
this approach, it is therefore advisable to also collect additional estimates of
frequency, including the most lucid dream episodes experienced in any 6-
month period (e.g., LaBerge et al., 2018b).

A limitation of the above methods is that they do not measure variation in the
length or degree of lucid dreams. Indeed, lucid dreams can range from a mere
fleeting thought about the fact that one is dreaming followed by an immediate
loss of lucidity or awakening, to extended lucid dreams in which an individual
is able to engage in sequences of actions (e.g., LaBerge and Rheingold, 1990).
Distinguishing between these different “levels” or subtypes of lucid dreams
will likely be valuable to understanding observed differences (or lack of
differences) in brain structural or functional measures associated with lucid
dream frequency. Along these lines, several recent questionnaires have taken
first steps to measure individual differences in specific characteristics of lucid
dreaming. For example, the Lucid Dreaming Skills Questionnaire (LUSK)
measures participants’ frequency of several different but inter-related aspects
of awareness and control in lucid dreams (Schredl, Rieger and Göritz, 2018).
Another questionnaire, the Frequency and Intensity Lucid Dreaming
Questionnaire (FILD) queries participants regarding the duration of their lucid
dreams and various aspects of dream control, as well as the frequency with
which they deliberately attempt to induce lucid dreams (Aviram and Soffer-
Dudek, 2018). In addition to providing data for individual differences studies,
such questionnaires could also potentially be useful in selecting participants for
sleep laboratory experiments of lucid dreaming, for example by selecting
participants who report high levels of dream control in addition to frequent
lucid dreams (in order to select participants who are more likely to be able to
effectively make the eye signals or engage in experimental tasks during lucid
dreams).

For all the above methods, important steps need to be taken to minimize
measurement error, particularly to ensure that participants have a clear
understanding of the meaning of lucid dreaming (Snyder and Gackenbach,
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 42/61
18/7/2021 The cognitive neuroscience of lucid dreaming

1988). These include providing participants with a written definition of lucid

dreaming, asking participants to provide written examples of their own lucid
dreams to ensure clear understanding, as well as additional vetting through
participant interviews (Baird et al., 2018a). Ultimately, however, basing the
measurement of individual differences in lucid dreaming solely on self-report
is not optimal. One way to further validate participant questionnaire responses
would be to attempt to physiologically validate at least one lucid dream in the
sleep laboratory for each participant. While additional validations such as this
could potentially be valuable to incorporate in future studies, it is important to
note that the estimated frequency of lucid dreaming would still depend on
questionnaire assessment. Thus, approaches such as this do not obviate the
reliance on questionnaire assessment.

An intriguing, though ambitious, method for deriving a measure of lucid dream

frequency not dependent on questionnaire assessment would be to utilize
home-based EEG recording systems to collect longitudinal sleep
polysomnography data, from which estimates of lucid dreaming frequency
could be derived from the frequency of signal-verified lucid dreams collected
over many nights. However, this approach would only measure the frequency
of signal-verified lucid dreams, and instances in which participants achieved
lucidity but did not make the eye signal due to factors such as awakening,
forgetting the intention, or lack of dream control would be missed by this
procedure. There are many more points that could be addressed on the topic of
questionnaire assessment of lucid dreaming frequency, but an extended
analysis of this issue is beyond the scope of the present review.

9.6. General discussion of the measurement of lucid dreaming in

cognitive neuroscience
In summary, cognitive neuroscience studies of lucid dreaming have at their
disposal a unique set of rigorous methodological tools, including in particular
the eye movement signaling method, which allows for the objective validation
of lucid dreaming as well as precise time-stamping of physiological data.
However, refinement of the instructions given to participants, as described
above, could help further increase the reliability of the technique. Accurate
phenomenological assessment of lucidity has been more mixed. In sleep
laboratory studies using the eye signaling method, phenomenological reports
are important but less critical due to the presence of an objective marker of
lucidity. In contrast, in studies without eye signaling, accurate
phenomenological assessment of whether an individual was lucid becomes
essential, and inadequate or ambiguous measurement of lucidity can undermine
the interpretability of the results. Questionnaire measures such as the DLQ
(Stumbrys et al., 2013b) or LuCiD scale (Voss et al., 2013) by themselves do
not provide an unambiguous assessment of whether an individual had a lucid
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 43/61
18/7/2021 The cognitive neuroscience of lucid dreaming

dream. Cognitive neuroscience research on lucid dreaming would greatly

benefit from the further development of improved questionnaire measures for
the validation of lucidity and the cognitive and experiential changes that
accompany it, as well as further development of standardized measures for
quantifying both the frequency and degree of lucidity. Overall, this brief
discussion highlights the need for a set of standard operating procedures for
both the phenomenological and objective sleep laboratory assessment of lucid
dreaming.

10. Conclusion
Despite having been physiologically validated for approximately four decades,
the neurobiology of lucid dreaming is still incompletely characterized. Most
studies conducted to date have relied on small sample sizes, which limits the
generalizability of the findings. Not surprisingly, the results of such
underpowered studies are not consistent: almost every EEG study reports
changes in spectral power in a different frequency band or brain area.
Neuroimaging data on lucid dreaming is even sparser. Currently, there is only
one fMRI study contrasting lucid and non-lucid REM sleep and it is a case
study. Nevertheless, the results of this study converge with MRI studies that
have evaluated individual differences in lucid dreaming frequency. Together,
this preliminary evidence suggests that regions of anterior prefrontal, parietal
and temporal cortex are involved in lucid dreaming. The involvement of these
brain regions in metacognitive processes during the waking state is also in line
with these findings.

A primary goal is to develop reliable strategies for making lucid dreaming

more accessible. As reviewed above, several studies have explored methods for
non-invasive electrical stimulation of the brain as well as pharmacological
approaches to lucid dream induction. Electrical stimulation of prefrontal brain
areas has resulted in statistically significant but weak increases of dream
“insight” ratings, but so far it has not resulted in significant increases in the
frequency of lucid dreams. Currently it remains too early to tell how effective
(if at all) electrical stimulation of the frontal cortex, or other brain areas, could
be for lucid dream induction. Pharmacological induction with agents acting on
the cholinergic system, in particular the AChEI galantamine, has shown
promising results; however, these findings need to be replicated systematically,
and lucid dreams objectively confirmed with polysomnography. Other
approaches to lucid dream induction not discussed in the current review, and
that do not directly target neural mechanisms, such as cognitive/psychological
approaches, also appear promising (Stumbrys et al., 2012). For example,
advances in the research of targeted memory reactivation via olfactory or
acoustic stimuli during sleep (e.g., Oudiette, Antony, Creery and Paller, 2013)

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 44/61
18/7/2021 The cognitive neuroscience of lucid dreaming

might lead to new strategies for lucid dream induction, together with continued
research on stimulating lucid dreams with visual or auditory cues (LaBerge and
Levitan, 1995; LaBerge et al., 1988; LaBerge et al., 1981b).

In conclusion, additional studies with larger sample sizes, for example large-
scale group-level high-density EEG, MEG, and concurrent EEG/fMRI studies,
will be important next steps toward characterizing the neural functional
changes associated with lucid dreaming. For now, a more detailed
understanding of the neurobiological basis of lucid dreaming remains an open
question for ongoing research. Lucid dreaming shows promise as a useful
methodology for psychophysiological studies of REM sleep, with potential
applications in both clinical and basic research domains. Perhaps the largest
potential of research on lucid dreaming is that it provides a unique method to
investigate the neurobiology of consciousness, which remains one of the largest
lacunas in scientific knowledge.

Highlights

EEG studies of lucid dreaming are mostly underpowered and show

mixed results

Preliminary neuroimaging data implicates frontoparietal cortices in

lucid dreaming

Cholinergic stimulation with mental set shows promise for inducing

lucid dreams

We present best-practice procedures to investigate lucid dreaming in

the laboratory

Acknowledgements
We thank Stephen LaBerge for helpful discussion.

Funding

BB was supported by the National Institutes of Health (NIH) under Ruth L.

Kirschstein National Research Service Award F32NS089348 from the NINDS.
SAM-R was supported by the Coordena9ao de Aperfei9oamento de Pessoal de
Nivel Superior (CAPES), Conselho Nacional de Desenvolvimento Científico e
Tecnológico (CNPq), Financiadora de Estudos e Projetos do Ministério da
Ciência e Tecnologia (FINEP), and Fundação de Apoio à Pesquisa do Estado
do Rio Grande do Norte (FAPERN). MD was supported by the Netherlands
Organisation for Scientific Research (NWO) through a Vidi fellowship
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 45/61
18/7/2021 The cognitive neuroscience of lucid dreaming

(016.Vidi.185.142). The content is solely the responsibility of the authors and

does not necessarily represent the official views of the NIH, CAPES, CNPq,
FINEP, FAPERN or NWO.

Footnotes
Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been
accepted for publication. As a service to our customers we are providing this early
version of the manuscript. The manuscript will undergo copyediting, typesetting, and
review of the resulting proof before it is published in its final citable form. Please note
that during the production process errors may be discovered which could affect the
content, and all legal disclaimers that apply to the journal pertain.

Competing interests

The authors declare no competing interests.

References

1. Abramovitch H, 1995. The nightmare of returning home: A case of acute

onset nightmare disorder treated by lucid dreaming. Israel journal of
psychiatry and related sciences
32, 140–145. [PubMed] [Google Scholar]
2. Amatruda TT, Black DA, McKenna TM, McCarley RW, Hobson JA,
1975. Sleep cycle control and cholinergic mechanisms: Differential effects
of carbachol injections at pontine brain stem sites. Brain Res. 98, 501–
515. [PubMed] [Google Scholar]
3. Antrobus JS, Antrobus JS, 1967. Discrimination of two sleep stages by
human subjects. Psychophysiology
4, 48–55. [PubMed] [Google Scholar]
4. Aristotle, 1941. On Dreams, in: McKeon R (Ed.), The basic works of
Aristotle. Random House, New York, NY, pp. 618–625. [Google Scholar]
5. Arnulf I, 2011. The’scanning hypothesis’ of rapid eye movements during
REM sleep: A review of the evidence. Arch. Ital. Biol
149, 367–382.
[PubMed] [Google Scholar]
6. Aspy DJ, Delfabbro P, Proeve M, Mohr P, 2017. Reality testing and the
Mnemonic Induction of Lucid Dreams: Findings from the national
Australian lucid dream induction study. Dreaming
27, 206–231.
[Google Scholar]
7. Aviram L, Soffer-Dudek N, 2018. Lucid dreaming: Intensity, but not
frequency, is inversely related to psychopathology. Front. Psychol
9, 384.
[PMC free article] [PubMed] [Google Scholar]
8. Baghdoyan HA, 1997. Cholinergic mechanisms regulating REM sleep, in:
Schwartz W (Ed.), Sleep science: Integrating basic research and clinical
practice. Karger, Basel, pp. 88–116. [Google Scholar]
9. Baier M, 2010. Insight in schizophrenia: A review. Curr. Psychiatry Rep
12, 356–361. [PubMed] [Google Scholar]
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 46/61
18/7/2021 The cognitive neuroscience of lucid dreaming

10. Baird B, Castelnovo A, Gosseries O, Tononi G, 2018a. Frequent lucid

dreaming associated with increased functional connectivity between
frontopolar cortex and temporoparietal association areas. Sci. Rep
[PMC free article] [PubMed] [Google Scholar]
11. Baird B, Castelnovo A, Riedner BA, Lutz A, Ferrarelli F, Boly M,
Davidson RJ, Tononi G, 2018b. Human rapid eye movement sleep shows
local increases in low-frequency oscillations and global decreases in high-
frequency oscillations compared to resting wakefulness. eNeuro
5.
[PMC free article] [PubMed] [Google Scholar]
12. Baird B, Riedner BA, Boly M, Davidson RJ, Tononi G, 2018c. Increased
lucid dream frequency in long-term meditators but not following
mindfulness-based stress reduction training. Psychology of
Consciousness: Theory, Research and Practice. [Google Scholar]
13. Baird B, Smallwood J, Gorgolewski KJ, Margulies DS, 2013. Medial and
lateral networks in anterior prefrontal cortex support metacognitive ability
for memory and perception. J. Neurosci
33, 16657–16665.
[PMC free article] [PubMed] [Google Scholar]
14. Bentley P, Driver J, Dolan RJ, 2011. Cholinergic modulation of cognition:
Insights from human pharmacological functional neuroimaging. Prog.
Neurobiol
94, 360–388. [PMC free article] [PubMed] [Google Scholar]
15. Berrios GE, Markova IS, 1998. Insight in the psychoses: A conceptual
history, in: Amador X, David A (Eds.), Insight and psychosis. Oxford
University Press, New York, NY, pp. 33–46. [Google Scholar]
16. Berryhill ME, Phuong L, Picasso L, Cabeza R, Olson IR, 2007. Parietal
lobe and episodic memory: Bilateral damage causes impaired free recall
of autobiographical memory. J. Neurosci
27, 14415–14423.
[PMC free article] [PubMed] [Google Scholar]
17. Blumenfeld H, 2008. Epilepsy and consciousness, in: Laureys S (Ed.),
The neurology of consciousness. Elsevier Academic Press, Oxford, pp.
247–260. [Google Scholar]
18. Boly M, Garrido MI, Gosseries O, Bruno M-A, Boveroux P, Schnakers C,
Massimini M, Litvak V, Laureys S, Friston K, 2011. Preserved
feedforward but impaired top-down processes in the vegetative state.
Science
332, 858–862. [PubMed] [Google Scholar]
19. Boly M, Moran R, Murphy M, Boveroux P, Bruno M-A, Noirhomme Q,
Ledoux D, Bonhomme V, Brichant J-F, Tononi G, 2012. Connectivity
changes underlying spectral EEG changes during propofol-induced loss of
consciousness. J. Neurosci
32, 7082–7090. [PMC free article] [PubMed]
[Google Scholar]
20. Braun A, Balkin T, Wesenten N, Carson R, Varga M, Baldwin P, Selbie S,
Belenky G, Herscovitch P, 1997. Regional cerebral blood flow throughout
the sleep-wake cycle. An H2 (15) O PET study. Brain
120, 1173–1197.
[PubMed] [Google Scholar]
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 47/61
18/7/2021 The cognitive neuroscience of lucid dreaming

21. Braun AR, Balkin TJ, Wesensten NJ, Gwadry F, Carson RE, Varga M,
Baldwin P, Belenky G, Herscovitch P, 1998. Dissociated pattern of
activity in visual cortices and their projections during human rapid eye
movement sleep. Science
279, 91–95. [PubMed] [Google Scholar]
22. Brylowski A, Levitan L, LaBerge S, 1989. H-reflex suppression and
autonomic activation during lucid REM sleep: A case study. Sleep
12,
374–378. [PubMed] [Google Scholar]
23. Cavallero C, Cicogna P, Natale V, Occhionero M, Zito A, 1992. Slow
wave sleep dreaming. Sleep
15, 562–566. [PubMed] [Google Scholar]
24. Cavanna AE, Trimble MR, 2006. The precuneus: A review of its
functional anatomy and behavioural correlates. Brain
129, 564–583.
[PubMed] [Google Scholar]
25. Christoff K, Ream JM, Geddes L, Gabrieli JD, 2003. Evaluating self-
generated information: Anterior prefrontal contributions to human
cognition. Behav. Neurosci
117, 1161–1168. [PubMed] [Google Scholar]
26. Cuadra G, Summers K, Giacobini E, 1994. Cholinesterase inhibitor effects
on neurotransmitters in rat cortex in vivo. J. Pharmacol. Exp. Ther
270,
277–284. [PubMed] [Google Scholar]
27. Dane J, Van de Caslte R, 1984. A comparison of waking instruction and
posthypnotic suggestion for lucid dream induction. Lucidity Letter
3.
[Google Scholar]
28. David AS, 1990. Insight and psychosis. The British Journal of Psychiatry
156, 798–808. [PubMed] [Google Scholar]
29. DeGracia DJ, LaBerge S, 2000. Varieties of lucid dreaming experience,
in: Kunzendorf RG, Wallace B (Eds.), Individual differences in conscious
experience. John Benjamins, Amsterdam, pp. 269–307. [Google Scholar]
30. Dement W, Wolpert EA, 1958. The relation of eye movements, body
motility, and external stimuli to dream content. J. Exp. Psychol
55, 543–
552. [PubMed] [Google Scholar]
31. Dixon ML, De La Vega A, Mills C, Andrews-Hanna J, Spreng RN, Cole
MW, Christoff K, 2018. Heterogeneity within the frontoparietal control
network and its relationship to the default and dorsal attention networks.
Proc. Natl. Acad. Sci, E1598–E1607. [PMC free article] [PubMed]
[Google Scholar]
32. Dodet P, Chavez M, Leu-Semenescu S, Golmard J, Arnulf I, 2014. Lucid
dreaming in narcolepsy. Sleep
38, 487–497. [PMC free article] [PubMed]
[Google Scholar]
33. Donner TH, Siegel M, 2011. A framework for local cortical oscillation
patterns. Trends Cog. Sci
15, 191–199. [PubMed] [Google Scholar]
34. Dresler M, Eibl L, Fischer CF, Wehrle R, Spoormaker VI, Steiger A,
Czisch M, Pawlowski M, 2014. Volitional components of consciousness
vary across wakefulness, dreaming and lucid dreaming. Front. Psychol
4,
987. [PMC free article] [PubMed] [Google Scholar]
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 48/61
18/7/2021 The cognitive neuroscience of lucid dreaming

35. Dresler M, Koch SP, Wehrle R, Spoormaker VI, Holsboer F, Steiger A,

Sämann PG, Obrig H, Czisch M, 2011. Dreamed movement elicits
activation in the sensorimotor cortex. Curr. Biol
21, 1833–1837.
[PubMed] [Google Scholar]
36. Dresler M, Sandberg A, Bublitz C, Ohla K, Trenado C, Mroczko-
Wqsowicz A, Kühn S, Repantis D, 2018. Hacking the brain: Dimensions
of cognitive enhancement. ACS Chemical Neuroscience.
[PMC free article] [PubMed] [Google Scholar]
37. Dresler M, Wehrle R, Spoormaker VI, Koch SP, Holsboer F, Steiger A,
Obrig H, Sämann PG, Czisch M, 2012. Neural correlates of dream
lucidity obtained from contrasting lucid versus non-lucid REM sleep: A
combined EEG/fMRI case study. Sleep
35, 1017–1020. [PMC free article]
[PubMed] [Google Scholar]
38. Dresler M, Wehrle R, Spoormaker VI, Steiger A, Holsboer F, Czisch M,
Hobson JA, 2015. Neural correlates of insight in dreaming and psychosis.
Sleep Med. Rev
20, 92–99. [PubMed] [Google Scholar]
39. Engel AK, Fries P, 2010. Beta-band oscillations—signalling the status
quo?
Curr. Opin. Neurobiol
20, 156–165. [PubMed] [Google Scholar]
40. Engel J, Kuhl DE, Phelps ME, 1982. Patterns of human local cerebral
glucose metabolism during epileptic seizures. Science
218, 64–66.
[PubMed] [Google Scholar]
41. Erlacher D, Schredl M, LaBerge S, 2003. Motor area activation during
dreamed hand clenching: A pilot study on EEG alpha band. Sleep
Hypnosis
5, 182–187. [Google Scholar]
42. Filevich E, Dresler M, Brick TR, Kühn S, 2015. Metacognitive
mechanisms underlying lucid dreaming. J. Neurosci
35, 1082–1088.
[PMC free article] [PubMed] [Google Scholar]
43. Fleming SM, Weil RS, Nagy Z, Dolan RJ, Rees G, 2010. Relating
introspective accuracy to individual differences in brain structure. Science
329, 1541–1543. [PMC free article] [PubMed] [Google Scholar]
44. Fosse R, 2000. REM mentation in narcoleptics and normals: An empirical
test of two neurocognitive theories. Conscious. Cogn
9, 488–509.
[PubMed] [Google Scholar]
45. Funk CM, Honjoh S, Rodriguez AV, Cirelli C, Tononi G, 2016. Local
slow waves in superficial layers of primary cortical areas during REM
sleep. Curr. Biol
26, 396–403. [PMC free article] [PubMed]
[Google Scholar]
46. Gackenbach J, Cranson R, Alexander C, 1986. Lucid dreaming,
witnessing dreaming, and the transcendental meditation technique: A
developmental relationship. Lucidity Letter
5, 34–40. [Google Scholar]
47. Gackenbach J, LaBerge S, 1988. Conscious mind, sleeping brain:
Perspectives on lucid dreaming. Plenum Press, New York, NY.
[Google Scholar]
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 49/61
18/7/2021 The cognitive neuroscience of lucid dreaming

48. Garfield P, Fellows P, Halliday G, Malamud JR, 1988. Clinical

applications of lucid dreaming, in: Gackenbach J, LaBerge S (Eds.),
Conscious Mind, Sleeping Brain. Plenum Press, New York, NY, pp. 289–
319. [Google Scholar]
49. Giacobini E, Zhu X-D, Williams E, Sherman K, 1996. The effect of the
selective reversible acetylcholinesterase inhibitor E2020 on extracellular
acetylcholine and biogenic amine levels in rat cortex. Neuropharmacology
35, 205–211. [PubMed] [Google Scholar]
50. Gillin JC, Sitaram N, Janowsky D, Risch C, Huey L, Storch FI, 1985.
Cholinergic mechanisms in REM sleep, in: Wauquier A, Gail lard J, Monti
J, Radulovacki M (Eds.), Sleep: Neurotransmitters and neuromodulators.
Raven Press, New York, NY, pp. 29–42. [Google Scholar]
51. Goldberg G, 1985. Supplementary motor area structure and function:
Review and hypotheses. Behav. Brain. Sci
8, 567–588. [Google Scholar]
52. Gratton G, Coles MG, Donchin E, 1983. A new method for off-line
removal of ocular artifact. Electroencephalogr. Clin. Neurophysiol
55,
468–484. [PubMed] [Google Scholar]
53. Green CE, 1968. Lucid dreams. Hamilton, London. [Google Scholar]
54. Hallett M, 2007. Transcranial magnetic stimulation: A primer. Neuron
55,
187–199. [PubMed] [Google Scholar]
55. Hearne KM, 1978. Lucid dreams: An elecro-physiological and
psychological study (Unpublished doctoral dissertation). Liverpool
University, Liverpool, UK. [Google Scholar]
56. Hermann DM, Siccoli M, Brugger P, Wachter K, Mathis J, Achermann P,
Bassetti CL, 2008. Evolution of neurological, neuropsychological and
sleep-wake disturbances after paramedian thalamic stroke. Stroke
39, 62–
68. [PubMed] [Google Scholar]
57. Hernandez-Peon R, Chavez-lbarra G, Morgane P, Timo-Iaria C, 1963.
Limbic cholinergic pathways involved in sleep and emotional behavior.
Exp. Neurol
8, 93–111. [Google Scholar]
58. Hipp JF, Siegel M, 2013. Dissociating neuronal gamma-band activity
from cranial and ocular muscle activity in EEG. Front. Hum. Neurosci
7,
338. [PMC free article] [PubMed] [Google Scholar]
59. Hobson JA, Pace-Schott EF, 2002. The cognitive neuroscience of sleep:
Neuronal systems, consciousness and learning. Nat. Rev. Neurosci
3, 679–
693. [PubMed] [Google Scholar]
60. Hobson JA, Pace-Schott EF, Stickgold R, 2000. Dreaming and the brain:
Toward a cognitive neuroscience of conscious states. Behav. Brain. Sci
23,
793–842. [PubMed] [Google Scholar]
61. Hodes R, Dement WC, 1964. Depression of electrically induced reflexes
(“H-reflexes”) in man during low voltage EEG “sleep”.
Electroencephalogr. Clin. Neurophysiol
17, 617–629. [PubMed]
[Google Scholar]
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 50/61
18/7/2021 The cognitive neuroscience of lucid dreaming

62. Holzinger B, Klösch G, Saletu B, 2015. Studies with lucid dreaming as

add-on therapy to Gestalt therapy. Acta Neurol. Scand
131, 355–363.
[PubMed] [Google Scholar]
63. Holzinger B, LaBerge S, Levitan L, 2006. Psychophysiological correlates
of lucid dreaming. Dreaming
16, 88–95. [Google Scholar]
64. Joseph R, 1999. Frontal lobe psychopathology: Mania, depression,
confabulation, catatonia, perseveration, obsessive compulsions, and
schizophrenia. Psychiatry
62, 138–172. [PubMed] [Google Scholar]
65. Kahan TL, LaBerge S, Levitan L, Zimbardo P, 1997. Similarities and
differences between dreaming and waking cognition: An exploratory
study. Conscious. Cogn
6, 132–147. [PubMed] [Google Scholar]
66. Kahan TL, Sullivan KT, 2012. Assessing metacognitive skills in waking
and sleep: A psychometric analysis of the Metacognitive, Affective,
Cognitive Experience (MACE) questionnaire. Conscious. Cogn
21, 340–
352. [PubMed] [Google Scholar]
67. Keren AS, Yuval-Greenberg S, Deouell LY, 2010. Saccadic spike
potentials in gamma-band EEG: Characterization, detection and
suppression. Neuroimage
49, 2248–2263. [PubMed] [Google Scholar]
68. Kern S, Appel K, Schredl M, Pipa G, 2017. No effect of α-GPC on lucid
dream induction or dream content. Somnologie
21, 180–186.
[Google Scholar]
69. Kjaer TW, Nowak M, Lou HC, 2002. Reflective self-awareness and
conscious states: PET evidence for a common midline parietofrontal core.
Neuroimage
17, 1080–1086. [PubMed] [Google Scholar]
70. Komogortsev OV, Karpov A, 2013. Automated classification and scoring
of smooth pursuit eye movements in the presence of fixations and
saccades. Behav. Res. Methods
45, 203–215. [PubMed] [Google Scholar]
71. Koontz J, Baskys A, 2005. Effects of galantamine on working memory
and global functioning in patients with mild cognitive impairment: A
double-blind placebo-controlled study. Am. J. Alzheimer’s Dis. Other
Dementias
20, 295–302. [PubMed] [Google Scholar]
72. Koshino Y, Niedermeyer E, 1975. Enhancement of rolandic mu-rhythm by
pattern vision. Electroencephalogr. Clin. Neurophysiol
38, 535–538.
[PubMed] [Google Scholar]
73. LaBerge S, 1980a. Lucid dreaming as a learnable skill: A case study.
Percept. Motor Skills
51, 1039–1042. [Google Scholar]
74. LaBerge S, 1980b. Lucid dreaming: An exploratory study of
consciousness during sleep (Unpublished doctoral dissertation). Stanford
University, Stanford, CA. [Google Scholar]
75. LaBerge S, 1985. Lucid dreaming: The power of being awake and aware
in your dreams. Jeremy P. Tarcher, Los Angeles. [Google Scholar]

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 51/61
18/7/2021 The cognitive neuroscience of lucid dreaming

76. LaBerge S, 1988a. Lucid dreaming in western literature, in: LaBerge JGS
(Ed.), Conscious Mind, Sleeping Brain. Plenum Press, New York, NY, pp.
11–26. [Google Scholar]
77. LaBerge S, 1988b. The psychophysiology of lucid dreaming, in:
Gackenbach J, LaBerge S (Eds.), Conscious mind, sleeping brain:
Perspectives on lucid dreaming. Plenum Press, New York, NY, pp. 135–
153. [Google Scholar]
78. LaBerge S, 1990. Lucid dreaming: Psychophysiological studies of
consciousness during REM sleep, in: Bootzin RR, Kihlstrom JF, Schacter
DL (Eds.), Sleep and Cognition. American Psychological Association,
Washington DC, pp. 109–126. [Google Scholar]
79. LaBerge S, 2001. The paradox and promise of lucid dreaming
Research
update: Cholinergic stimulation of lucid dreaming; voluntary control of
auditory perception during REM lucid dreams, International Association
for the Study of Dreams, Berkeley. [Google Scholar]
80. LaBerge S, 2003. Lucid dreaming and the yoga of the dream state: A
psychophysiological perspective, in: Wallace BA (Ed.), Buddhism &
science: Breaking new ground. Columbia University Press, New York,
NY, pp. 233–258. [Google Scholar]
81. LaBerge S, 2010. Signal-verfied lucid dreaming proves that REM sleep
can support reflective consciousness. Int. J. Dream Res
3, 26–27.
[Google Scholar]
82. LaBerge S, 2015. Lucid dreaming: Metaconsciousness during paradoxical
sleep, in: Glucksman MKM (Ed.), Dream research: Contributions to
clinical practice. Routledge, New York, NY, pp. 198–214.
[Google Scholar]
83. LaBerge S, Baird B, Zimbardo PG, 2018a. Smooth tracking of visual
targets distinguishes lucid REM sleep dreaming and waking perception
from imagination. Nat. Comm
9, 3298. [PMC free article] [PubMed]
[Google Scholar]
84. LaBerge S, Dement WC, 1982. Voluntary control of respiration during
REM sleep. Sleep Res. 11, 107. [Google Scholar]
85. LaBerge S, Greenleaf W, Kedzierski B, 1983. Physiological responses to
dreamed sexual activity during lucid REM sleep. Psychophysiology, 454–
455. [Google Scholar]
86. LaBerge S, LaMarca K, Baird B, 2018b. Pre-sleep treatment with
galantamine stimulates lucid dreaming: A double-blind, placebo-
controlled, crossover study. PLoS ONE
13, e0201246. [PMC free article]
[PubMed] [Google Scholar]
87. LaBerge S, Levitan L, 1995. Validity established of DreamLight cues for
eliciting lucid dreaming. Dreaming
5, 159–168. [Google Scholar]

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 52/61
18/7/2021 The cognitive neuroscience of lucid dreaming

88. LaBerge S, Levitan L, Dement WC, 1986. Lucid dreaming: Physiological

correlates of consciousness during REM sleep. J. Mind Behav
7, 251–258.
[Google Scholar]
89. LaBerge S, Levitan L, Rich R, Dement WC, 1988. Induction of lucid
dreaming by light stimulation during REM sleep. Sleep Res. 17, 104.
[Google Scholar]
90. LaBerge S, Nagel L, Taylor W, Dement W, Zarcone V, 1981a.
Psychophysiological correlates of the initiation of lucid dreaming. Sleep
Res. 10, 149. [Google Scholar]
91. LaBerge S, Owens J, Nagel L, Dement WC, 1981b. “This is a dream”:
Induction of lucid dreams by verbal suggestion during REM sleep. Sleep
Res. 10, 150. [Google Scholar]
92. LaBerge S, Phillips L, Levitan L, 1994. An hour of wakefulness before
morning naps makes lucidity more likely. NightLight
6, 1–4.
[Google Scholar]
93. LaBerge S, Rheingold H, 1990. Exploring the world of lucid dreaming.
Ballantine Books; New York, NY. [Google Scholar]
94. LaBerge SP, Nagel LE, Dement WC, Zarcone VP, 1981c. Lucid dreaming
verified by volitional communication during REM sleep. Percept. Motor
Skills
52, 727–732. [PubMed] [Google Scholar]
95. Lachaux JP, Fonlupt P, Kahane P, Minotti L, Hoffmann D, Bertrand O,
Baciu M, 2007. Relationship between task-related gamma oscillations and
BOLD signal: New insights from combined fMRI and intracranial EEG.
Hum. Brain Mapp
28, 1368–1375. [PMC free article] [PubMed]
[Google Scholar]
96. Lancee J, Van Den Bout J, Spoormaker VI, 2010. Expanding self-help
imagery rehearsal therapy for nightmares with sleep hygiene and lucid
dreaming: A waiting-list controlled trial. Int. J. Dream Res
3, 111–120.
[Google Scholar]
97. Laureys S, Owen AM, Schiff ND, 2004. Brain function in coma,
vegetative state, and related disorders. Lancet Neurol. 3, 537–546.
[PubMed] [Google Scholar]
98. Laureys S, Perrin F, Brédart S, 2007. Self-consciousness in non-
communicative patients. Conscious. Cogn
16, 722–741. [PubMed]
[Google Scholar]
99. Lee U, Ku S, Noh G, Baek S, Choi B, Mashour GA, 2013. Disruption of
frontal-parietal communication by ketamine, propofol, and sevoflurane.
Anesthesiology
118, 1264–1275. [PMC free article] [PubMed]
[Google Scholar]
100. Levin R, Nielsen TA, 2007. Disturbed dreaming, posttraumatic stress
disorder, and affect distress: A review and neurocognitive model. Psychol.
Bull
133, 482. [PubMed] [Google Scholar]

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 53/61
18/7/2021 The cognitive neuroscience of lucid dreaming

101. Lincoln TM, Lüllmann E, Rief W, 2007. Correlates and long-term

consequences of poor insight in patients with schizophrenia. A systematic
review. Schizophrenia Bulletin
33, 1324–1342. [PMC free article]
[PubMed] [Google Scholar]
102. Lou HC, Luber B, Crupain M, Keenan JP, Nowak M, Kjaer TW, Sackeim
HA, Lisanby SH, 2004. Parietal cortex and representation of the mental
self. Proc. Natl. Acad. Sci
101, 6827–6832. [PMC free article] [PubMed]
[Google Scholar]
103. Luigetti M, Di Lazzaro V, Broccolini A, Vollono C, Dittoni S, Frisullo G,
Pilato F, Profice P, Losurdo A, Morosetti R, 2011. Bilateral thalamic
stroke transiently reduces arousals and NREM sleep instability. J. Neurol.
Sci
300, 151–154. [PubMed] [Google Scholar]
104. Malcolm N, 1959. Dreaming. Routledge, London, England.
[Google Scholar]
105. Maquet P, Péters J-M, Aerts J, Delfiore G, Degueldre C, Luxen A, Franck
G, 1996. Functional neuroanatomy of human rapid-eye-movement sleep
and dreaming. Nature
383, 163–166. [PubMed] [Google Scholar]
106. Mashour GA, 2014. Top-down mechanisms of anesthetic-induced
unconsciousness. Front. Sys. Neurosci
8, 115. [PMC free article]
[PubMed] [Google Scholar]
107. Mason LI, Orme-Johnson DW, 2010. Transcendental consciousness wakes
up in dreaming and deep sleep. Int. J. Dream Res
3, 28–32.
[Google Scholar]
108. Mazzetti M, Bellucci C, Mattarozzi K, Plazzi G, Tuozzi G, Cipolli C,
2010. REM-dreams recall in patients with narcolepsy-cataplexy. Brain
Res. Bull
81, 133–140. [PubMed] [Google Scholar]
109. McCaig RG, Dixon M, Keramatian K, Liu I, Christoff K, 2011. Improved
modulation of rostrolateral prefrontal cortex using real-time fMRI training
and meta-cognitive awareness. NeuroImage
55, 1298–1305. [PubMed]
[Google Scholar]
110. McKay LC, Adams L, Frackowiak RS, Corfield DR, 2008. A bilateral
cortico-bulbar network associated with breath holding in humans,
determined by functional magnetic resonance imaging. NeuroImage
40,
1824–1832. [PubMed] [Google Scholar]
111. Mintz AR, Dobson KS, Romney DM, 2003. Insight in schizophrenia: A
meta-analysis. Schizophrenia Research
61, 75–88. [PubMed]
[Google Scholar]
112. Montagna P, 2005. Fatal familial insomnia: A model disease in sleep
physiopathology. Sleep Med. Rev
9, 339–353. [PubMed] [Google Scholar]
113. Morgenthaler TI, Auerbach S, Casey KR, Kristo D, Maganti R, Ramar K,
Zak R, Kartje R, 2018. Position paper for the treatment of nightmare
disorder in adults: An American Academy of Sleep Medicine position

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 54/61
18/7/2021 The cognitive neuroscience of lucid dreaming

paper. Journal of Clinical Sleep Medicine

14, 1041–1055.
[PMC free article] [PubMed] [Google Scholar]
114. Mota NB, Resende A, Mota-Rolim SA, Copelli M, Ribeiro S, 2016.
Psychosis and the control of lucid dreaming. Front. Psychol
7, 294.
[PMC free article] [PubMed] [Google Scholar]
115. Mota-Rolim S, Pantoja A, Pinheiro R, Camilo A, Barbosa T, Hazboun I,
Araujo J, Ribeiro S, 2008. Lucid dream: Sleep electroencephalographic
features and behavioral induction methods, First Congress IBRO/LARC of
Neurosciences for Latin America, Caribbean and Iberian Peninsula.
Bdzios, Brazil. [Google Scholar]
116. Mota-Rolim SA, Araujo JF, 2013. Neurobiology and clinical implications
of lucid dreaming. Medical hypotheses
81, 751–756. [PubMed]
[Google Scholar]
117. Mota-Rolim SA, Brandão DS, Andrade KC, de Queiroz CMT, Araujo JF,
de Araujo DB, Ribeiro S, 2015. Neurophysiological features of lucid
dreaming during N1 and N2 sleep stages: Two case reports. Sleep Sci. 4,
215. [Google Scholar]
118. Mota-Rolim SA, Erlacher D, Tort AB, Araujo JF, Ribeiro S, 2010.
Different kinds of subjective experience during lucid dreaming may have
different neural sub-strates. Int. J. Dream Res
25, 550–557.
[Google Scholar]
119. Mota-Rolim SA, Targino ZH, Souza BC, Blanco W, Araujo JF, Ribeiro S,
2013. Dream characteristics in a Brazilian sample: An online survey
focusing on lucid dreaming. Front. Hum. Neurosci
7, 836.
[PMC free article] [PubMed] [Google Scholar]
120. Muzio JN, Roffwarg HP, Kaufman E, 1966. Alterations in the nocturnal
sleep cycle resulting from LSD. Clin. Neurophysiol
21, 313–324.
[PubMed] [Google Scholar]
121. Nieminen JO, Gosseries O, Massimini M, Saad E, Sheldon AD, Boly M,
Siclari F, Postle BR, Tononi G, 2016. Consciousness and cortical
responsiveness: A within-state study during non-rapid eye movement
sleep. Sci. Rep
6, 30932. [PMC free article] [PubMed] [Google Scholar]
122. Nir Y, Fisch L, Mukamel R, Gelbard-Sagiv H, Arieli A, Fried I, Malach
R, 2007. Coupling between neuronal firing rate, gamma LFP, and BOLD
fMRI is related to interneuronal correlations. Curr. Biol
17, 1275–1285.
[PubMed] [Google Scholar]
123. Nir Y, Tononi G, 2010. Dreaming and the brain: From phenomenology to
neurophysiology. Trends Cog. Sci
14, 88–100. [PMC free article]
[PubMed] [Google Scholar]
124. Norbu N, Katz M, 1992. Dream yoga and the practice of natural light.
Snow Lion Publications, Ithaca, NY. [Google Scholar]

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 55/61
18/7/2021 The cognitive neuroscience of lucid dreaming

125. Noreika V, Windt JM, Lenggenhager B, Karim AA, 2010. New

perspectives for the study of lucid dreaming: From brain stimulation to
philosophical theories of self-consciousness. Int. J. Dream Res
3, 36–45.
[Google Scholar]
126. Ogilvie R, Hunt H, Kushniruk A, Newman J, 1983. Lucid dreams and the
arousal continuum. Lucidity Letter
2. [Google Scholar]
127. Ogilvie R, Hunt H, Sawicki C, McGowan K, 1978. Searching for lucid
dreams. Sleep Res. 7, 165. [Google Scholar]
128. Ogilvie R, Vieira K, Small R, 1991. EEG activity during lucid dreaming.
Lucidity Letter
10. [Google Scholar]
129. Ogilvie RD, Hunt HT, Tyson PD, Lucescu ML, Jeakins DB, 1982. Lucid
dreaming and alpha activity: A preliminary report. Percept. Motor Skills
55, 795–808. [PubMed] [Google Scholar]
130. Oudiette D, Antony JW, Creery JD, Paller KA, 2013. The role of memory
reactivation during wakefulness and sleep in determining which memories
endure. J. Neurosci
33, 6672–6678. [PMC free article] [PubMed]
[Google Scholar]
131. Oudiette D, Dodet P, Ledard N, Artru E, Rachidi I, Similowski T, Arnulf
I, 2018. REM sleep respiratory behaviours mental content in narcoleptic
lucid dreamers. Sci. Rep
8, 2636. [PMC free article] [PubMed]
[Google Scholar]
132. Padmasambhava, 1998. Natural liberation: Padmasambhava’s teachings
on the six bardos. Wisdom, Boston, MA. [Google Scholar]
133. Perogamvros L, Baird B, Seibold M, Riedner B, Boly M, Tononi G, 2017.
The phenomenal contents and neural correlates of spontaneous thoughts
across wakefulness, NREM sleep, and REM sleep. J. Cogn. Neurosci
29,
1766–1777. [PMC free article] [PubMed] [Google Scholar]
134. Pfurtscheller G, Stancak A, Neuper C, 1996. Post-movement beta
synchronization. A correlate of an idling motor area?
Electroencephalogr.
Clin. Neurophysiol
98, 281–293. [PubMed] [Google Scholar]
135. Pigorini A, Sarasso S, Proserpio P, Szymanski C, Arnulfo G, Casarotto S,
Fecchio M, Rosanova M, Mariotti M, Russo GL, 2015. Bistability breaks-
off deterministic responses to intracortical stimulation during non-REM
sleep. Neuroimage
112, 105–113. [PubMed] [Google Scholar]
136. Price RF, Cohen DB, 1988. Lucid dream induction: An empirical
evaluation. Conscious mind, sleeping brain: Perspectives on lucid
dreaming, 105–134. [Google Scholar]
137. Purdon PL, Pierce ET, Mukamel EA, Prerau MJ, Walsh JL, Wong KFK,
Salazar-Gomez AF, Harrell PG, Sampson AL, Cimenser A, 2013.
Electroencephalogram signatures of loss and recovery of consciousness
from propofol. Proc. Natl. Acad. Sci
110, E1142–E1151.
[PMC free article] [PubMed] [Google Scholar]

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 56/61
18/7/2021 The cognitive neuroscience of lucid dreaming

138. Raggi A, Cosentino FI, Lanuzza B, Ferri R, 2010. Behavioural and

neurophysiologic features of state dissociation: A brief review of the
literature and three descriptive case studies. Behavioural neurology
22,
91–99. [PMC free article] [PubMed] [Google Scholar]
139. Rak M, Beitinger P, Steiger A, Schredl M, Dresler M, 2015. Increased
lucid dreaming frequency in narcolepsy. Sleep
38, 787–792.
[PMC free article] [PubMed] [Google Scholar]
140. Rechtschaffen A, Kales A, 1968. A manual of standardized terminology,
techniques and scoring system for sleep stages of human subjects.
Government Printing Office National Institutes of Health, Washington,
DC. [PubMed] [Google Scholar]
141. Rees G, Wojciulik E, Clarke K, Husain M, Frith C, Driver J, 2002. Neural
correlates of conscious and unconscious vision in parietal extinction.
Neurocase
8, 387–393. [PubMed] [Google Scholar]
142. Riemann D, Gann H, Dressing H, Müller WE, Aldenhoff JB, 1994.
Influence of the cholinesterase inhibitor galanthamine hydrobromide on
normal sleep. Psychiatry Res. 51, 253–267. [PubMed] [Google Scholar]
143. Roehrs T, Roth T, 2001. Sleep, sleepiness, sleep disorders and alcohol use
and abuse. Sleep Med. Rev
5, 287–297. [PubMed] [Google Scholar]
144. Sagnier S, Coulon P, Chaufton C, Poll M, Debruxelles S, Renou P,
Rouanet F, Olindo S, Sibon I, 2015. Lucid dreams, an atypical sleep
disturbance in anterior and mediodorsal thalamic strokes. Revue
neurologique
171, 768–772. [PubMed] [Google Scholar]
145. Saunders DT, Roe CA, Smith G, Clegg H, 2016. Lucid dreaming
incidence: A quality effects meta-analysis of 50 years of research.
Conscious. Cogn
43, 197–215. [PubMed] [Google Scholar]
146. Schierenbeck T, Riemann D, Berger M, Hornyak M, 2008. Effect of illicit
recreational drugs upon sleep: Cocaine, ecstasy and marijuana. Sleep Med.
Rev
12, 381–389. [PubMed] [Google Scholar]
147. Schmitz TW, Rowley HA, Kawahara TN, Johnson SC, 2006. Neural
correlates of self-evaluative accuracy after traumatic brain injury.
Neuropsychologia
44, 762–773. [PubMed] [Google Scholar]
148. Schnakers C, Vanhaudenhuyse A, Giacino J, Ventura M, Boly M, Majerus
S, Moonen G, Laureys S, 2009. Diagnostic accuracy of the vegetative and
minimally conscious state: Clinical consensus versus standardized
neurobehavioral assessment. BMC Neurol. 9, 35. [PMC free article]
[PubMed] [Google Scholar]
149. Schooler JW, 2002. Re-representing consciousness: Dissociations between
experience and meta-consciousness. Trends Cog. Sci
6, 339–344.
[PubMed] [Google Scholar]
150. Schredl M, Erlacher D, 2004. Lucid dreaming frequency and personality.
Pers. Individ. Dif
37, 1463–1473. [Google Scholar]

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 57/61
18/7/2021 The cognitive neuroscience of lucid dreaming

151. Schredl M, Rieger J, Göritz AS, 2018. Measuring lucid dreaming skills: A
new questionnaire (LUSK). Int. J. Dream Res [Google Scholar]
152. Siclari F, Baird B, Perogamvros L, Bernardi G, LaRocque JJ, Riedner B,
Boly M, Postle BR, Tononi G, 2017. The neural correlates of dreaming.
Nat. Neurosci
20, 872–878. [PMC free article] [PubMed]
[Google Scholar]
153. Siclari F, LaRocque JJ, Postle BR, Tononi G, 2013. Assessing sleep
consciousness within subjects using a serial awakening paradigm. Front.
Psychol
4. [PMC free article] [PubMed] [Google Scholar]
154. Snyder TJ, Gackenbach J, 1988. Individual differences associated with
lucid dreaming, in: LaBerge S, Gackenbach J (Eds.), Conscious mind,
sleeping brain. Plenum, New York, NY, pp. 221–259. [Google Scholar]
155. Sparrow G, Hurd R, Carlson R, Molina A, 2018. Exploring the effects of
galantamine paired with meditation and dream reliving on recalled
dreams: Toward an integrated protocol for lucid dream induction and
nightmare resolution. Conscious. Cogn
63, 74–88. [PubMed]
[Google Scholar]
156. Sparrow GS, Thurston M, Carlson R, 2013. Dream reliving and
meditation as a way to enhance reflectiveness and constructive
engagement in dreams. Int. J. Dream Res
6, 84–93. [Google Scholar]
157. Spering M, Montagnini A, 2011. Do we track what we see? Common
versus independent processing for motion perception and smooth pursuit
eye movements: A review. Vision Res. 51, 836–852. [PubMed]
[Google Scholar]
158. Spoormaker VI, Czisch M, Dresler M, 2010. Lucid and non-lucid
dreaming: Thinking in networks. Int. J. Dream Res
3, 49–51.
[Google Scholar]
159. Spoormaker VI, Van Den Bout J, 2006. Lucid dreaming treatment for
nightmares: A pilot study. Psychother. Psychosom
75, 389–394. [PubMed]
[Google Scholar]
160. Steriade M, Timofeev I, Grenier F, 2001. Natural waking and sleep states:
A view from inside neocortical neurons. J. Neurophysiol
85, 1969–1985.
[PubMed] [Google Scholar]
161. Stickgold R, Malia A, Fosse R, Hobson JA, 2001. Brain-mind states: I.
Longitudinal field study of sleep/wake factors influencing mentation
report length. Sleep
24, 171–179. [PubMed] [Google Scholar]
162. Stumbrys T, Erlacher D, 2012. Lucid dreaming during NREM sleep: Two
case reports. Int. J. Dream Res
5, 151–155. [Google Scholar]
163. Stumbrys T, Erlacher D, Malinowski P, 2015. Meta-awareness during day
and night: The relationship between mindfulness and lucid dreaming.
Imagin. Cogn. Pers
34, 415–433. [Google Scholar]

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 58/61
18/7/2021 The cognitive neuroscience of lucid dreaming

164. Stumbrys T, Erlacher D, Schadlich M, Schredl M, 2012. Induction of

lucid dreams: A systematic review of evidence. Conscious. Cogn
21,
1456–1475. [PubMed] [Google Scholar]
165. Stumbrys T, Erlacher D, Schredl M, 2013a. Reliability and stability of
lucid dream and nightmare frequency scales. Int. J. Dream Res
6, 123–
126. [Google Scholar]
166. Stumbrys T, Erlacher D, Schredl M, 2013b. Testing the involvement of the
prefrontal cortex in lucid dreaming: A tDCS study. Conscious. Cogn
22,
1214–1222. [PubMed] [Google Scholar]
167. Tanner BA, 2004. Multimodal behavioral treatment of nonrepetitive,
treatment-resistant nightmares: A case report. Percept. Motor Skills
99,
1139–1146. [PubMed] [Google Scholar]
168. Tononi G, 2011. Integrated information theory of consciousness: An
updated account. Arch. Ital. Biol
150, 56–90. [PubMed] [Google Scholar]
169. Tononi G, Boly M, Massimini M, Koch C, 2016. Integrated information
theory: From consciousness to its physical substrate. Nat. Rev. Neurosci
17, 450–461. [PubMed] [Google Scholar]
170. Tononi G, Massimini M, 2008. Why does consciousness fade in early
sleep?
Ann. N. Y. Acad. Sci
1129, 330–334. [PubMed] [Google Scholar]
171. Tyson PD, Ogilvie RD, Hunt HT, 1984. Lucid, prelucid, and nonlucid
dreams related to the amount of EEG alpha activity during REM sleep.
Psychophysiology
21, 442–451. [PubMed] [Google Scholar]
172. Van der Werf YD, Witter MP, Groenewegen HJ, 2002. The intralaminar
and midline nuclei of the thalamus. Anatomical and functional evidence
for participation in processes of arousal and awareness. Brain Res. Rev
39,
107–140. [PubMed] [Google Scholar]
173. Van Eeden F, 1913. A study of dreams, Proceedings of the Society for
Psychical Research, pp. 431–461. [Google Scholar]
174. van Gaal S, Ridderinkhof KR, Scholte HS, Lamme VA, 2010.
Unconscious activation of the prefrontal no-go network. J. Neurosci
30,
4143–4150. [PMC free article] [PubMed] [Google Scholar]
175. Vanni S, Portin K, Virsu V, Hari R, 1999. Mu rhythm modulation during
changes of visual percepts. Neuroscience
91, 21–31. [PubMed]
[Google Scholar]
176. Velazquez-Moctezuma J, Shalauta M, Gillin JC, Shiromani PJ, 1991.
Cholinergic antagonists and REM sleep generation. Brain Res. 543, 175–
179. [PubMed] [Google Scholar]
177. Violante IR, Li LM, Carmichael DW, Lorenz R, Leech R, Hampshire A,
Rothwell JC, Sharp DJ, 2017. Externally induced frontoparietal
synchronization modulates network dynamics and enhances working
memory performance. Elife
6, e22001. [PMC free article] [PubMed]
[Google Scholar]

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 59/61
18/7/2021 The cognitive neuroscience of lucid dreaming

178. Vogel GW, 1975. A review of REM sleep deprivation. Arch. Gen.
Psychiatry
32, 749–761. [PubMed] [Google Scholar]
179. Voss U, Holzmann R, Hobson A, Paulus W, Koppehele-Gossel J, Klimke
A, Nitsche MA, 2014. Induction of self awareness in dreams through
frontal low current stimulation of gamma activity. Nat. Neurosci
17, 810–
812. [PubMed] [Google Scholar]
180. Voss U, Holzmann R, Tuin I, Hobson JA, 2009. Lucid dreaming: A state
of consciousness with features of both waking and non-lucid dreaming.
Sleep
32, 1191–1200. [PMC free article] [PubMed] [Google Scholar]
181. Voss U, Schermelleh-Engel K, Windt J, Frenzel C, Hobson A, 2013.
Measuring consciousness in dreams: The lucidity and consciousness in
dreams scale. Conscious. Cogn
22, 8–21. [PubMed] [Google Scholar]
182. Wagner AD, Shannon BJ, Kahn I, Buckner RL, 2005. Parietal lobe
contributions to episodic memory retrieval. Trends Cog. Sci
9, 445–453.
[PubMed] [Google Scholar]
183. Wallace BA, 2013. Buddhism and science: Breaking new ground.
Columbia University Press. [Google Scholar]
184. Wallace BA, Hodel B, 2012. Dreaming yourself awake: Lucid dreaming
and Tibetan dream yoga for insight and transformation. Shambhala
Publications, Boston, MA. [Google Scholar]
185. Windt JM, 2010. The immersive spatiotemporal hallucination model of
dreaming. Phenomenol. Cogn. Sci
9, 295–316. [Google Scholar]
186. Windt JM, 2015. Dreaming: A conceptual framework for philosophy of
mind and empirical research. MIT Press, Cambridge, MA.
[Google Scholar]
187. Windt JM, Metzinger T, 2007. The philosophy of dreaming and self-
consciousness: What happens to the experiential subject during the dream
state?, in: Barrett D, McNamara P (Eds.), The new science of dreaming:
Cultural and theoretical perspectives. Praeger; , Westport, CT, pp. 193–
247. [Google Scholar]
188. Windt JM, Nielsen T, Thompson E, 2016. Does consciousness disappear
in dreamless sleep? Trends Cog. Sci
20, 871–882. [PubMed]
[Google Scholar]
189. Yeo B, Krienen FM, Sepulcre J, Sabuncu MR, Lashkari D, Hollinshead
M, Roffman JL, Smoller JW, Zöllei L, Polimeni JR, 2011. The
organization of the human cerebral cortex estimated by intrinsic functional
connectivity. J. Neurophysiol
106, 1125–1165. [PMC free article]
[PubMed] [Google Scholar]
190. Yuschak T, 2006. Advanced lucid dreaming: The power of supplements.
Lulu Enterprises, Raleigh, NC. [Google Scholar]
191. Yuval-Greenberg S, Deouell LY, 2009. The broadband-transient induced
gamma-band response in scalp EEG reflects the execution of saccades.
Brain Topogr. 22, 3–6. [PubMed] [Google Scholar]
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 60/61
18/7/2021 The cognitive neuroscience of lucid dreaming

192. Yuval-Greenberg S, Tomer O, Keren AS, Nelken I, Deouell LY, 2008.

Transient induced gamma-band response in EEG as a manifestation of
miniature saccades. Neuron
58, 429–441. [PubMed] [Google Scholar]
193. Zadra AL, Pihl RO, 1997. Lucid dreaming as a treatment for recurrent
nightmares. Psychother. Psychosom
66, 50–55. [PubMed]
[Google Scholar]

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451677/ 61/61