Accepted Manuscript

Beyond the neuropsychology of dreaming: insights into the neural basis of dreaming
with new techniques of sleep recording and analysis
Carlo Cipolli, Michele Ferrara, Luigi De Gennaro, Giuseppe Plazzi
PII:

S1087-0792(16)30067-3

DOI:

10.1016/j.smrv.2016.07.005

Reference:

YSMRV 983

To appear in:

Sleep Medicine Reviews

Received Date: 16 November 2015

Revised Date:

14 July 2016

Accepted Date: 14 July 2016

Please cite this article as: Cipolli C, Ferrara M, De Gennaro L, Plazzi G, Beyond the neuropsychology
of dreaming: insights into the neural basis of dreaming with new techniques of sleep recording and
analysis, Sleep Medicine Reviews (2016), doi: 10.1016/j.smrv.2016.07.005.
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 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.

ACCEPTED MANUSCRIPT
Title: Beyond the neuropsychology of dreaming: insights into the neural basis of dreaming
with new techniques of sleep recording and analysis.

Running Title: Beyond the neuropsychology of dreaming

RI
PT

Authors : Carlo Cipolli1, Michele Ferrara2, Luigi De Gennaro3, Giuseppe Plazzi4,5*

Affiliations:
1

Department of Specialty, Diagnostic and Experimental Medicine, University of Bologna, Bologna,

SC

Italy.
2

Department of Biotechnological and Applied Clinical Sciences, University of LAquila,

LAquila, Italy.

Department of Psychology, Sapienza University of Roma, Roma, Italy.

DIBINEM Department of Biomedical and Neuromotor Sciences, University of Bologna,

M
AN
U

Bologna, Italy.

IRCCS Istituto delle Scienze Neurologiche, AUSL di Bologna, Italy.

TE
D

Address correspondence to: *Giuseppe Plazzi, Department of Biomedical and Neuromotor

Sciences, University of Bologna, Via Altura 3, Bologna, Italy.

EP

Tel: +39 051 4966924;

Fax: : +39 051 4966098;

AC
C

E-mail address: giuseppe.plazzi@unibo.it

ACCEPTED MANUSCRIPT
Summary

Recent advances in electrophysiological [e.g., surface high-density electroencephalographic (hdEEG) and intracranial recordings], video-polysomnography (video-PSG), transcranial stimulation

RI
PT

and neuroimaging techniques allow more in-depth and more accurate investigation of the neural
correlates of dreaming in healthy individuals and in patients with brain-damage, neurodegenerative
diseases, sleep disorders or parasomnias. Convergent evidence provided by studies using these

SC

techniques on healthy subjects has led to a reformulation of several unresolved issues of dream
generation and recall [such as the inter- and intra-individual differences in dream recall and the

M
AN
U

predictivity of specific EEG rhythms, such as theta in rapid eye movement (REM) sleep, for dream
recall] within more comprehensive models of human consciousness and its variations across
sleep/wake states than the traditional models, which were largely based on the neurophysiology of
REM sleep in animals. These studies are casting new light on the neural bases (in particular, the

TE
D

activity of dorsal medial prefrontal cortex regions and hippocampus and amygdala areas) of the
inter- and intra-individual differences in dream recall, the temporal location of specific contents or
properties (e.g., lucidity) of dream experience and the processing of memories accessed during

EP

sleep and incorporated into dream content. Hd-EEG techniques, used on their own or in
combination with neuroimaging, appear able to provide further important insights into how the

AC
C

brain generates not only dreaming during sleep but also some dreamlike experiences in waking.

Keywords: Dreaming; dream recall; cognitive processes; REM sleep; EEG correlates;
neuroimaging techniques; intracranial EEG recordings; state-/trait-like differences; videopolysomnography.

ACCEPTED MANUSCRIPT
List of Abbreviations:
dl /l/ m/ vmPFC dorsolateral / lateral/ medial/ ventromedial prefrontal cortex
DTI diffusion tensor imaging
EEG electroencephalography

Hd-EEG high density EEG

HDR/LDR high/low dream recaller
Hz Hertz (cycles per second);
REM sleep rapid eye movement sleep
NREM sleep non rapid eye movement sleep

NIRS near-infrared spectroscopy

P300 P3 wave (event-related potential)
PET positron emission tomography
video-PSG video-polysomnography

TE
D

PTSD post-traumatic stress disorder

M
AN
U

MEG magnetoencephalography

SC

RI
PT

(f)MRI (functional) magnetic resonance imaging

PuM medial pulvinar nucleus

RBD REM sleep behavior disorder

SEEG stereo-EEG

EP

SOREM sleep onset REM sleep

SWS slow wave sleep

AC
C

tACS transcranial alternating current stimulation

tDCS transcranial direct current stimulation
TMS transcranial magnetic stimulation
TMR targeted memory reactivation
TP(O)J temporoparietal (occipital) junction
V1/ V4/ V5 visual area one/four/five

ACCEPTED MANUSCRIPT
1. INTRODUCTION

Dreaming (also termed sleep mentation, dream experience or mental activity during sleep) is
a state of consciousness occurring in a physiological condition different from that in which it

RI
PT

becomes available for investigation via its recall (and possibly report). Because of the asynchrony
between its generation during sleep and recall after awakening, dreaming has traditionally been
considered difficult to study through the conceptual apparatus applied to investigate the states of

SC

consciousness experienced in wakefulness (for review1,2). This (often implicit) assumption has
deeply influenced the experimental investigation of dreaming, first developed in the 1950s after the

M
AN
U

discovery of the cyclic architecture of sleep and the identification of rapid eye movement (REM)
sleep as a possible neurophysiological marker of dreaming. However, recent neuroimaging and
neurophysiological studies on resting state and mind wandering in wakefulness have shown a wide
overlap of phenomenological features and underlying brain mechanisms3,4 with dreaming. This has

TE
D

led to a conceptualization of dreaming as a natural extension of waking consciousness5, namely, a

state characterized by internally generated multisensorial (overall visual and auditory), motor
(sometimes dramatic), cognitive and emotional experiences, inserted as fairly coherent events into

EP

an imaginary story-like plot3,6-8.

In this review, we will examine the deepening of our knowledge of the neurobiological basis of

AC
C

dreaming made possible by recent advances in electrophysiological and neuroimaging methods of

sleep recording and analysis. To facilitate the understanding of the theoretical relevance of the
findings obtained through these methods, we will start from an updated characterization of
dreaming, as results from over 60 years of laboratory and clinical research.

2. FREQUENCY OF DREAM RECALL AND DREAM GENERATION PROCESSES

The collection of dream reports after provoked awakening in the laboratory has provided both
reliable estimates of the frequency of dream experience developed in the different sleep stages and
4

ACCEPTED MANUSCRIPT
useful insights into the underlying cognitive processes, while the clinical observation of sleep and
dream recall of patients with acute brain lesions has offered important evidence of the anatomical
correlates of dream alteration and dream loss.

RI
PT

2.1 Frequency of dream recall

Early laboratory studies using electropolygraphic recordings of sleep9-11 reported a much more
frequent association of fairly long, perceptually vivid and complex (dreamlike) mental

SC

experiences after awakening from periods of sleep with heightened and desynchronized cortical
activity (i.e., high-frequency/low-amplitude electroencephalographic [EEG] activity) accompanied

M
AN
U

by REMs, muscle atonia and increased variability in heart rate and respiratory activity, compared to
other non-REM (NREM) periods of sleep (for review, see7,8).

The originally postulated close (if not exclusive) association of REM sleep and dreaming, however,
was rapidly disproved by studies carried out using more complex designs and interview techniques

TE
D

(for review, see8,12), which yielded several crucial findings.

1) Dream recall is also fairly frequent (about 50%) after awakening from nighttime13-15 and daytime
(in particular, stage-2) NREM sleep13,16 relative to REM sleep (more than 80%).

EP

2) One or more dreamlike characteristics (such as perceptual vividness, bizarreness, emotional tone
and story-like organization) are enhanced in reports collected after late night NREM sleep (relative

AC
C

to the early night)15,17,18 and in the morning19,20, as well as after periods of total or partial sleep
deprivation21,22 , restriction23 or with multiple awakenings24.
3) Neither dreaming nor REM and NREM sleep are stable, homogeneous and distinct states
irrespective of terminology (for dreaming) and taxonomy (for sleep stages). Indeed, not only
perceptual, but also cognitive contents (such as planning, reasoning and thinking) are common, as
are emotional experiences (often intense and negatively toned25,26), in dream reports. Moreover,
whole reports can rarely be classified as dreams or thoughts, but are better described along a
continuum ranging from thought-like (overall in NREM sleep of early night15,18) to dreamlike
5

ACCEPTED MANUSCRIPT
content (overall in REM sleep of late night17,18,27 and under higher sleep pressure21). Finally, 5 to
10% of NREM reports after stage 228 and stages 3 and 429 cannot be distinguished from REM
reports solely on the basis of the perceptual and emotional features of their contents.
4) The stage- and cycle-related variations in recall frequency and in the perceptual, emotional,

RI
PT

motor and story-like features of dream reports are influenced by large differences not only between
(trait-like), but also within subjects (state-like). For example, there are opposite trends in the length
and complexity of reports according to whether the time-in-stage pertains to REM or NREM sleep15

SC

and whether it is in the first or second half of the night18,30.

5) The frequency and characteristics of dream reports (and, thus, their within-subject variability) are

concern

the

modalities

of

M
AN
U

influenced, in particular, by situational and individual factors (for reviews31,32). Situational factors
awakening

(abrupt/gradual33)

and

dream

reporting

(free

recall31/questionnaire32/affirmative probes34, guided recall35), and the presence/absence of

interfering tasks upon awakening36. Individual factors concern gender, age, personality traits

TE
D

(openness to experience, psychological boundaries and absorption37), the tendency to suppress

negative thoughts and emotions38 and the attitude toward dreams, motivation, emotional reactivity,
and cognitive styles39.

EP

6) Individuals with normal or high recall frequency (once or more per week32,40) usually fail to
report any dream after 530% of REM awakenings8, and some (so-called non-recallers) cannot even

AC
C

report any dream after REM awakenings31,41.

7) Dream recall can be modulated by dopamine agonists42,43, or even suppressed by brain lesions
(see below) located at the temporoparieto-occipital (TPO) junction and ventromedial prefrontal
cortex (vmPFC)44,45, without any appreciable effect on REM sleep frequency and duration or REM
density46.
The evidence that a more or less dreamlike mental activity is also developed during NREM sleep
prompted researchers to reconcile the observed differences not only by postulating a continuum
(ranging from purely thought-like to dreamlike features) of mental activities developed during all
6

ACCEPTED MANUSCRIPT
sleep stages7,8,23,24., but also by attempting to overcome the boundaries of the traditional
neuropsychology of dreaming, which was largely based on the neurophysiology of REM sleep in
animal models. Recent advances in electrophysiological and neuroimaging techniques allow more
in-depth (by monitoring the functioning of specific brain regions) and accurate (for segments of

RI
PT

sleep close to awakening or marked by motor behaviors) investigation of the neural correlates of
dreaming in healthy individuals and in patients with brain damage, neurodegenerative diseases,
sleep disorders or parasomnias (see below). The indications so gathered may both complement

SC

those provided by the traditional electropolygraphic and clinical approaches and point towards the
need to reformulate and test several unresolved issues of dream generation and recall within more

M
AN
U

comprehensive models of human consciousness and its variations across sleep/wake states.

2.2 Cognitive processes involved in dream generation and recall

Laboratory studies have consistently shown that dream contents result from the elaboration of

TE
D

several memory sources and not from a simple reactivation of previous events. An individuals
current concerns and everyday life events (so-called episodic memories) are seldom reproduced
mechanically as dream contents47,48 but, rather, are largely transformed in combination with

EP

fragments of recent and remote events and items of semantic information49,50. Moreover, items of
recent episodic information can be activated and processed not only over the following night (day

AC
C

residue effect51), but also up to 5-7 nights later (dream-lag effect51). Indeed, subsequent dreams
reported after multiple awakenings of the same night show both repeated incorporations of presleep stimuli52-56 or suggestions and high frequencies of semantically equivalent or similar (socalled interrelated57,58) contents, regardless of the number of awakenings59, sleep stage60 or delay
between awakenings. Both types of findings indicate that the activation of memories is not random,
but oriented by some concerns61,62 and/or relationships with previously accessed information63.
The fairly consistent findings on the dream-lag effect64-66 indicate that the cognitive processes
subserving the functions of memory consolidation and emotional adaptation attributed to dreaming
7

ACCEPTED MANUSCRIPT
are at work during both NREM and REM sleep (albeit with some differences65), also over a long
period, with a selective advantage during REM sleep for personally relevant information66. Further
investigating the dream-lag effect also seems important for the understanding of sleep-dependent
memory consolidation and emotional balance (i.e., the different fate of emotional memories in

RI
PT

normal subjects67,68 and in patients with post-traumatic stress disorder: PTSD69). Indeed, some
neuroimaging and neurophysiological studies on the activation, during sleep, of the systems
involved in (re)processing items of information that are emotionally and motivationally relevant

SC

(salient) to the individuals have suggested that their different functional outcomes may be
accounted for in terms of consolidation (in patients with PTSD70,71) or depotentiation (in normal

M
AN
U

subjects72) of the negative emotional valence of events (for review71). In particular, the triage
model73, which posits that salient information is tagged for consolidation by emotional arousal,
future relevance, and/or deliberate intention, stems from the evidence that the negative emotional
tone of items of autobiographical memory fades faster over time than positive one74. Accordingly,

emotional charge72,75.

TE
D

sleep should provide a sort of overnight therapy for conflictual waking events and their negative

A full understanding of the relationships between dream generation and brain activity during sleep

EP

requires considering not only the fact that dreaming occurs in all stages and cycles, but also that its
contents, which result from the processing (elaborative encoding76,77) of several memory sources,

AC
C

already reach some consolidation during sleep (obviously lower than in waking). Indeed, dreams
can be retrieved at delayed recall (the next morning) without substantial changes in the amount and
sequential order of contents35,78, compared with immediate recall (just after night awakening) and
with short films watched some hours before79. Moreover, dreams may also persist in memory when
retrieval fails, as shown by their successful recall when triggered by occasional real-life cues or
prompted by appropriate probes (such as a short title given at immediate recall35) in a laboratory
setting. Finally, when dream contents incorporate some parts of newly learned tasks (including their
verbal, emotional, motor, perceptual and spatial components80-82), they may be also be accompanied
8

ACCEPTED MANUSCRIPT
by higher consolidation of the tasks themselves at post-awakening retrieval. The latter finding
suggests that, although the incorporation of pre-sleep tasks and suggestions is not a necessary step
of their consolidation process (for review83), the elaborative encoding involved in dream generation
may provide a further consolidation gain. This hypothesis raises the entwined issues of a) the

RI
PT

possible cumulative consolidation effect of the repeated elaboration of recent information

incorporated into dream contents82,84; and b) the (at least partial) overlap of the brain mechanisms
responsible for the consolidation of recently acquired information and the elaborative encoding of

SC

dream contents during sleep. Both possibilities are intriguing given that, despite the wide
familiarity (which also pertains to declarative memory) of characters and setting of dreams,

M
AN
U

episodic information is rarely (2%) replicated as a whole in dreams47,48.

The items of evidence in favor of the hypothesis that recent individually salient or task-related
experiences are not only reactivated, but also further consolidated in the sleeping brain via
incorporation into dream content, are still scant and discordant (for a discussion85). For example,

TE
D

visuomotor skills were shown to improve more after nighttime sleep in low dream recallers (LDR)
compared with high dream recallers (HDR), although the latter had a higher rate of incorporation of
the new (Mirror Tracing) task into dream content and a better initial performance86. At the present

EP

state of our knowledge, it, thus, seems more cautious to argue that: a) dreaming is not simply a
function of the consolidation process of recent information, either replayed81 or associated with

AC
C

older memories during dreaming77; and b) only a part of the neural activity underlying dreaming,
which is distributed across several cortical and subcortical structures, is influenced by the brain
structures subserving different memory systems85.

2.3 Clinical studies of dreaming

The early indications on the neural basis of dreaming were provided in the nineteenth century by the
observation of the anatomical correlates of dream alteration or even cessation in patients with
naturally occurring brain lesions87. However, it was only after the discovery of REM sleep that
9

ACCEPTED MANUSCRIPT
clinical reports addressed the consequences of brainstem lesions and focal cortical damage to the
mechanisms assumed to be responsible for the perceptual, emotional and formal properties of dream
content88-89. The subsequent investigation of dreaming was based on the general hypothesis that
lesions to pontine brainstem areas (which control sleep/waking cyclic organization90) reduce or

RI
PT

suppress both REM sleep and dreaming91. Solms45 attempted to test this hypothesis by examining
all cases of patients with acute brainstem lesions that included information relating to dreaming. His
review showed that a drastic reduction of REM sleep was accompanied by complete dream loss (so-

SC

called Charcot-Wilbrand syndrome) in only one92 of the 26 reported cases, and in none of the 4
patients with large pontine lesions he examined himself44. However, as consciousness is usually not

M
AN
U

preserved when pontine lesions are severe enough to have a significant effect on REM sleep93-94, it
cannot be argued that dreaming persists regardless of REM sleep (as suggested by Solms45,95).
The theoretical interest of also ascertaining how other chronic subcortical lesions steadily modify
dreaming is apparent. For example, some patients with bilateral damage to the basal ganglia (which

TE
D

causes an auto-activation deficit, namely absence of any self-reported thought in waking) can report
very simple dreams after REM sleep96. This suggests that simple dream imagery is generated by
brainstem stimulation and sent to the sensory cortex, while full dreams require that these

EP

sensations be interpreted by the cortical areas subserving higher-order cognitive processes.

Several reviews on the outcomes of acute cortical lesions44,45,88,95,97,98 have addressed the role of the

AC
C

cerebral cortex in dreaming. These studies, which primarily attempted to test the hypothesis of the
laterality of dreaming, consistently indicated that unilateral or bilateral temporoparieto-occipital
(TPO) injuries are often (but not always) associated with a complete dream loss. The most
comprehensive review (on 361 patients44) disclosed that dream loss usually follows damage
localized in either of the following brain systems:
1) A posterior system, mostly unilateral (right), in or near the TPO junction. Lesions to this system
affect dreaming44 as well as waking visual imagery99, while lesions to more specific regions (like
V4 or V5) selectively affect dream representation of color45 or movement100. However, lesions to
10

ACCEPTED MANUSCRIPT
primary unimodal sensorimotor cortices do not affect dream imagery45. Since visual imagery in turn
shares approximately two-thirds of activated brain areas with visual perception, and especially
visual association cortices99,101, both these findings support the hypothesis that dream experience,
mental imagery and late stages of visual perception share some neural mechanisms. This is

RI
PT

consistent with the finding that total dream loss in REM sleep persisted after the normalization of
sleep architecture102 in a patient with bilateral occipital artery infarction (including the right inferior
lingual gyrus).

SC

2) An anterior system, mostly bilateral, underlying the ventromedial (vm)PFC and including the
white matter tracts surrounding the anterior horns of the lateral ventricles. Lesions to areas of this

M
AN
U

system are less frequently associated with dream cessation, which follows overall bilateral lesions
to the white matter tracts surrounding the anterior horns of the lateral ventricles, underlying vmPFC.
Many of these nerve fibers originate or terminate in the limbic system45,95. The ventromedial white
matter contains dopaminergic projections to the frontal lobe, which are severed by prefrontal

TE
D

leucotomy. As one would expect from these findings, most leucotomized patients also complain of
global cessation of dreaming45. Moreover, damage to the secondary visual areas of the medial
occipital lobe/lingual gyrus leads to cessation of visual dream imagery, but leaves dreaming

EP

otherwise intact. On the contrary, lesions to the medial (m)PFC, anterior cingulate cortex and basal
forebrain appear to be associated with increased frequency and vividness of dreams and with their

AC
C

intrusion into waking life44. In addition, lesions in the dorsolateral (dl)PFC, which cause waking
deficits of self-monitoring and decision-making, have no effect on dreaming45 and no major
changes in dreaming are associated with brain lesions, irrespective of their severity, in areas outside
these two systems.
Prospective studies on brain-damaged patients would be undoubtedly useful to better understand the
neural basis of dreaming, as about half of these patients recover the ability to recall dreams at 2-4
years follow-up103. Nevertheless, the relationships between sleep normalization (i.e., neuronal
reorganization associated with functional recovery after brain damage104) and changes in dream
11

ACCEPTED MANUSCRIPT
recall and/or perceptual properties of dream content (possibly related to a reduction of
visuoperceptive disorders) remain unexplored to a large extent in REM sleep and completely in
NREM sleep.
To sum up, a more or less dreamlike mental experience is developed during all sleep stages,

RI
PT

although time-of-night, modality of awakening and technique of recall influence the estimates of
dreaming and its content characteristics. Dream contents result from the re-elaboration of several
memory sources, the processing of which may also exert some influence on their level of

SC

consolidation. Clinical studies on brain-damaged patients have provided fairly accurate indications

3. NEUROIMAGING STUDIES

M
AN
U

on the structures of two main (anterior and posterior) brain systems subserving dream generation.

Since the late 1990s, the findings of neuroimaging studies during sleep and the discovery that a
default network of brain regions active during waking restful states is in part reactivated in REM

dreaming.

TE
D

sleep but de-activated in NREM sleep have advanced our knowledge of the neural correlates of

The advent of brain imaging techniques (in particular, positron emission tomography: PET; single-

EP

photon emission computed tomography: SPECT; structural and functional magnetic resonance
imaging: s/fMRI) promised to cast light more directly on the relationships between specific dream

AC
C

features (as disclosed by report analysis) and brain activity during sleep. Indeed, the first (and only)
PET and EEG study controlling the presence/absence of dream recall showed an activation during
REM sleep in the pontine tegmentum, left thalamus, both amygdaloid complexes, anterior cingulate
cortex and right parietal operculum, and a (bilateral) deactivation in a vast area of the dlPFC,
parietal cortex (supramarginal gyrus), posterior cingulate cortex and precuneus105,106. These findings
were fully compatible with the clinical observation that lesions in these areas do not affect
dreaming. Two contemporary studies (without dream reporting107,108) disclosed a strong activation
of the high-order occipitotemporal visual cortex (consistent with the vividness of many dreams) and
12

ACCEPTED MANUSCRIPT
a concomitant decreased activation of the primary visual cortex during REM sleep. This
dissociation is suggestive of a high-order visual processing during sleep, without external visual
input and with a decreased activity of V1.
The majority of subsequent neuroimaging studies (for reviews109,110) have shown substantial

RI
PT

differences in brain activity during REM compared with NREM sleep, in which activation
diminishes from waking levels107,111. In particular, REM sleep is characterized by an increased
activity in the pons and midbrain, thalamus, basal ganglia, hypothalamus, ventral striatum and

SC

visual association cortices, and midline limbic and paralimbic areas, as well as in orbitofrontal and
paracingulate cortices and in part of the medial prefrontal cortex (mPFC)105,107, whereas the

M
AN
U

dorsolateral prefrontal cortex (dlPFC) remains deactivated after the transition from NREM to REM
sleep105,107,108,112. These indications prompt a reformulation of how the variations in brain activity
and dreaming are actually associated, which may lead to the development of a new and more
accurate neurophysiological model, enabling the testing of its predictions in studies on the trait- and

TE
D

state-like individual differences of dream generation and recall113.

The indications on the neural correlates of dreaming have been strengthened by the comparison of
neuroimaging data of brain functioning concomitant with mental activities during sleep and resting

EP

wakefulness (such as daydreaming and mind-wandering). Indeed, some dreamlike features (such as
visual imagery and bizarreness) had long been observed not only during stage-2 NREM at sleep

AC
C

onset14, in the late night15,17 and early morning19, but also in relaxed wakefulness114. However, the
theoretical relevance of the latter finding only became apparent after the observation that the
dmPFC is more active during mind-wandering compared with goal-directed intentional thinking115.
This evidence complemented the indications provided by early PET studies, showing that some
structures (anterior default network areas, vmPFC and portions of dmPFC, hippocampal and
parahippocampal areas) are partially reactivated during REM sleep, while others (posterior parietal
default network areas, especially the lateral inferior parietal and posterior cingulate cortex) remain
deactivated105-108,111. With specific regard to the default mode network (DMN), both increased116
13

ACCEPTED MANUSCRIPT
and decreased117connectivity between its nodes has been observed118 and distinct functions in dream
generation have been hypothesized for its two subsystems. These are centered on the hippocampal
formation (the medial temporal lobe subsystem, also called the simulation subsystem) and the
dorsal medial PFC (the dorsal medial PFC subsystem, also called the self referential subsystem),

RI
PT

respectively. The hippocampal formation might support dreaming, as it is more active in REM than
NREM110,119,120, while the dorsal medial PFC (which shows incomplete connectivity during REM
sleep117) might be responsible for the lack of insight into the current mental state, namely, the

SC

delusional acceptance of dreaming compared with waking internally-cued cognition120.

In general terms, many indications provided by lesional and neuroimaging studies have been

M
AN
U

combined to sketch models of the neurobiological bases of dreaming7,110,121. These models converge
to suggest which brain networks may be responsible for modulating the most distinctive
characteristics of dreams and dreamlike mental activities109,110,122: (1) activation of the amygdala
complex, anterior cingulate cortex and orbitofrontal cortex could be related to the emotional

TE
D

features of dreams; (2) increased activation of the occipitotemporal visual cortex could be
associated with visual dream imagery; (3) relative hypoactivation of the dlPFC could be associated
with alterations in logical reasoning, working memory, episodic memory and executive functions,

EP

which frequently occur in REM sleep dreams; (4) activation of mesiotemporal areas, and
specifically the hippocampus, could account for the episodic (recent and remote) memories

AC
C

commonly recognizable in specific dream contents.

Notably, the involvement of the first two networks is consistent with the results of brain-lesion
studies, while the role of mesiotemporal areas is supported by recent electrophysiological123,124 and
morpho-anatomical findings125,126. Conversely, the neural bases of mind-wandering seem to involve
more than just default network activity127, and several perceptual and emotional features of
daydreaming seem to differ from those of REM and NREM daytime naps128. These partially
discrepant findings clearly do not invalidate the models but, rather, prompt the elaboration of more
specific hypotheses, which may be tested by applying complementary bottom-up (from lesional and
14

ACCEPTED MANUSCRIPT
neuroimaging data to cognitive features of mental experiences129) and top-down research strategies
(from dream phenomenology to brain maps121), and by using refined psychometric indicators to
establish how the functioning of specific cognitive processes involved in dreaming (for example,
working memory130) varies during NREM and REM sleep relative to wakefulness. Establishing

RI
PT

how the variations in the activity of given brain areas are associated with specific features of dream
content would also cast light on such crucial issue as the trait- and state-like individual differences
of dream generation and recall113.

SC

The significant implications of the evidence from neuroimaging studies are not limited to cortical
regions but also extend to subcortical nuclei. In particular, evidence for the metabolic decline of

M
AN
U

brainstem and thalamus during NREM sleep7 (both involved in generating cortical slow waves106)
and for the increased activation in limbic and paralimbic structures during REM sleep105 suggests
that the hippocampus and amygdala play important and complementary roles in dream generation
and recall. This hypothesis is supported by evidence that: a) retrieving cues of fear-conditioning

TE
D

stimuli delivered before sleep affects the emotional tonality of dreams in REM and NREM sleep131;
b) in waking, gamma-band coherence between rhinal cortex and hippocampus increases when a
stimulus is successfully encoded132, while gamma activity increases in the entorhinal cortex layers

EP

projecting to the hippocampus when the stimulus is retrieved133. Consistently, a study on epileptic
patients with PSG and fMRI recordings has shown that an increased rhinalhippocampal coherence

AC
C

during REM sleep is predictive of dream recall and, thus, indicative of some consolidation of dream
content134.

Moreover, the activity of the amygdala, which is involved in the encoding and retrieval of
emotional memories and in the physical expression of emotions during wakefulness135, is higher
during REM sleep compared to wakefulness105. The hypothesis that the emotional load in dreams is
also related to amygdala activation121 has received some support from two MRI studies evaluating
the differences in the brain tissue of the hippocampus-amygdala complex. The volume of gray
matter and its microstructural alterations were measured by means of microstructural analyses of
15

ACCEPTED MANUSCRIPT
brain MRI and diffusion tensor imaging (DTI) analysis. The first study, on normal subjects, showed
that inter-individual differences in the emotional tone and bizarreness of dream contents reported in
the morning are closely related with the differences in the brain tissue of the hippocampusamygdala complex125. The second study, on Parkinsons patients, showed significant relationships

RI
PT

between the visual vividness of dream reports and the volume of amygdala, thickness of the medial
prefrontal cortex and hypodopaminergic activity, pointing to a specific role for the mesolimbic
dopaminergic system in qualitative (but not quantitative) aspects of dream recall126.

SC

In summary, neuroimaging studies have identified several networks of brain structures involved in
specific aspects of dreaming, whose functions have been ascertained in wakefulness. These

M
AN
U

observations have prompted studies on the role played by both cortical and subcortical nuclei in
dream generation and their stage-related variations.

4. ELECTROPHYSYOLOGICAL CORRELATES OF DREAM RECALL

TE
D

Recent advances in sleep recording (such as multi-electrodes in healthy subjects and intracranial
electrodes in epileptic patients) and in brain stimulation during sleep have led to new strategies to
identify the relationships between specific dream features and the activity of their putative

EP

underlying brain structures.

4.1 Cortical recordings

AC
C

The traditional approach to the neural basis of dreaming, based on the cortical electrophysiology of
sleep, has also been revitalized by the advent of multi-electrode recording techniques and
quantitative analysis of EEG signals, which provide a good temporal resolution and an acceptable
level of spatial resolution. Studies using these techniques have identified both the spatiotemporal
characteristics of sleep and its underlying neuronal networks111,136, and suggested a plausible
functional role of the fast- (25 Hz) and slow-frequency (1-4 Hz) oscillations during sleep
compared to waking. In particular, fast oscillations, which, in waking, are associated with attention
to stimuli and active cognition, during REM sleep are associated with the temporal binding of
16

ACCEPTED MANUSCRIPT
imagery137, memory and perceptual processes involved in dreaming138,139. Moreover, the decline in
phase synchrony (coherence) of EEG rhythms between distinct brain regions during sleep reflects a
functional disconnection, possibly responsible for the lack of executive control and bizarreness of
dream content110.

RI
PT

Consistent with the above indications, the analysis of EEG power during sleep onset REM
(SOREM) periods disclosed that increased alpha activity (at 11-13 Hz) is associated with the
absence of SOREM dreams and the appearance of NREM dreams140. This finding has been, in part,

SC

confirmed by a study where, after awakenings from stage 2 NREM and REM sleep, dream recall
was associated with a reduction in alpha power (of lower magnitude in REM sleep), mainly in the

M
AN
U

temporoparietal area141. The involvement of alpha activity in dreaming (overall in the right temporal
area, but only during stage 2 NREM) was also observed in a study where frontal theta oscillations
(5-7 Hz) were found to be positively related to dream recall after REM sleep142. This relationship
was also found in REM sleep of early afternoon naps, in which dream recall proved to be positively

TE
D

associated with higher frontal theta activity and theta oscillations at 6.06 Hz compared with a norecall condition143. Taken together, these findings provide some support for the "state-like
hypothesis" (for review113), according to which the variations in dream recall frequency after

EP

awakening from the same sleep stage may primarily depend on the contingent physiological state
preceding the awakening.

AC
C

The apparent parallelism between the above findings and the close association of theta and alpha
oscillations with memory encoding and retrieval while awake suggests that similar
neurophysiological mechanisms may be responsible for the encoding and recall of episodic
memories, both in wakefulness and during sleep. Indeed, a more efficient encoding of words and
faces correlates with a lower alpha activity (10-12 Hz) in the right temporoparietal cortical
region144, whereas an increased alpha power correlates with decreased memory performance145.
Moreover, scalp recordings have shown that successful encoding and retrieval of declarative
information are associated with increased theta power146. Finally, studies with intracerebral
17

ACCEPTED MANUSCRIPT
recordings in waking have also shown that an increase in frontal theta oscillations at encoding is
predictive of successful recall147, and mediates the interaction between PFC and medial temporal
lobe148.
Seemingly discrepant findings have been obtained using a 40-h multiple nap protocol (with 10

RI
PT

sleep-wake cycles of 75-150 min each) 149. However, the observed association of dream recall with
lower delta and sigma EEG activity in frontal and centroparietal derivations during NREM sleep,
and with higher alpha and beta activity in the occipital cortex during REM sleep, may depend on the

SC

repeated offset and re-onset of sleep, which altered the ultradian and circadian rhythms that interact
in modulating dream experience64, and, hence, the EEG predictors of dream recall.

M
AN
U

These findings raise the question of whether the association between EEG oscillations during sleep
and successful dream recall reflects stable characteristics of sleep EEG in some subjects rather than
temporary relationships. Pertinent evidence for the existence of trait-like inter-individual
differences has been obtained by comparing the brain reactivity of HDR and LDR subjects to

TE
D

auditory stimuli delivered during wakefulness and different sleep stages. Both intra-sleep
wakefulness and brain reactivity, measured by attention-orienting brain response (P300) and late
parietal response to first names (presented among pure tones while subjects were watching a silent

EP

movie or sleeping) ave been shown to be higher in HDR than in LDR subjects123,124. These findings
were in keeping with the "arousal-retrieval" model of dream recall, which posits that dream

AC
C

encoding depends on intra-sleep periods of wakefulness150. Regional cerebral blood flow has also
been found to be higher in HDR compared with LDR subjects in the temporoparietal (TP) junction
during REM sleep, stage 3 NREM and wakefulness, and in the mPFC during REM sleep and
wakefulness123. The latter finding supports the notion that the TP junction has a key role in the
production of mental imagery and the memory encoding of dream content, as its increased activity
may facilitate orienting attention toward external stimuli and prompt intra-sleep wakefulness.
Finally, by using a passive auditory oddball paradigm, a decrease in parietal alpha power (8-12 Hz)
has been demonstrated when names, compared with tones, are presented in waking, and an increase
18

ACCEPTED MANUSCRIPT
in parietal alpha power when they are presented during REM sleep123. The different effects of
complex sounds on alpha power during wakefulness (decrease) and REM sleep (increase) suggest
that the increased alpha power during REM sleep corresponds to either a short and transient
increase in arousal or a cortical inhibition associated with sleep protection.

RI
PT

The existence of some stable differences in the brain reactivity of HDR and LDR subjects during
both sleep and wakefulness suggests that the ability to recall dream content may be associated with
a particular cerebral functional organization, regardless of the state of vigilance, subserving the

M
AN
U

4.2 Intracranial EEG recordings

SC

functioning of some memory mechanisms involved in dream generation and/or recall.

Convergent indications have been provided by studies on patients with pharmacoresistant epilepsy,
using techniques of sleep recordings with higher spatial resolution [i.e., Hd-EEG and intracranial
stereo-EEG (SEEG)] to assess the spatiotemporal dynamics of peculiar EEG features. In keeping

TE
D

with the local sleep theory, which posits that the quantitative EEG features of each sleep stage are
regionally and temporally modulated151,152, the regional differences in EEG activity at cortical and
subcortical level may be indicative of specific functions in dream generation and recall. The activity

EP

of the mediotemporal lobe, thought to be involved in dream encoding and recall, has been studied
using intracranial SEEG134, under the assumption that the encoding of such episodic information as

AC
C

dream contents during sleep could share some electrophysiological mechanisms with the encoding
of other episodic information in wakefulness. Since a phase synchronization of rhinalhippocampal
EEG activity in the gamma range and an increased EEG coherence in the theta range had proved to
be predictive of successful memory formation132, the indices of rhinalhippocampal and
intrahippocampal EEG connectivity were compared in REM and NREM sleep of patients139 who
were or were not successful in recalling dreams after awakening. EEG coherence was higher for all
the frequency bands investigated (from 1 to 44 Hz) in patients with successful dream recall
compared with those with no recall, with a significant difference for all the states (waking, NREM
19

ACCEPTED MANUSCRIPT
and REM sleep). Moreover, the higher connectivity was more apparent in the low frequency theta
range, consistent with data on memory formation in wakefulness132,139. All these findings support
the hypothesis that the consolidation of dream content and the formation of episodic memories are
associated with increased mediotemporal connectivity in both REM and NREM sleep.

RI
PT

Other SEEG studies have provided useful suggestions on the neurophysiological mechanisms
underlying dream recall. Deactivation of the thalamic medial pulvinar nucleus (PuM) during REM
sleep (indicated by the abundant EEG delta activity153), which is at odds with the general

SC

thalamocortical cholinergic activation, suggests the presence of deactivated cortical areas (directly
connected with PuM) among other activated areas (connected with other thalamic nuclei). This

M
AN
U

dissociation could explain the reduced spatiotemporal cortical connectivity of REM sleep compared
to waking154 and, albeit indirectly, the high frequency of bizarre contents of REM dreams as a
consequence of the inactivation of specific cortical areas (such as posterior cingulate, dorsolateral

TE
D

prefrontal and parietal cortices) connected with PuM153.

4.3 Brain stimulation techniques during sleep

Transcranial stimulation techniques are able to disclose causal links between targeted brain areas

EP

and specific cognitive or emotional responses. In particular, transcranial direct current stimulation
(tDCS) can modulate cortical excitability over frontocortical areas during slow wave sleep (SWS)

AC
C

without awakening subjects, and enhances declarative memory consolidation155. When applied to
dream investigation, tDCS has shown that cathodal-frontal and anodal-parietal stimulation increases
reports of visual dream imagery during stage 2-NREM156, but not during SWS157, and the
stimulation of PFC induces dream lucidity during REM sleep158 in lucid dreamers (see below).
The demonstrated effectiveness of tDCS in activating PFC is theoretically relevant, as dream
lucidity is accompanied by a shift in EEG power, especially in the 40 Hz range of frontal brain
regions159. This is consistent with the finding that transcranial alternating current stimulation
(tACS) in the lower gamma band during REM sleep influences the ongoing frontal brain activity
20

ACCEPTED MANUSCRIPT
and induces self-reflective awareness in dreams160. Moreover, synchronous oscillations around 40
Hz of frontal regions are also present in lucid SOREMP dreams of narcoleptic patients161. Finally,
tDCS also influences the neural substrates of mind-wandering: the propensity to mind-wander of
subjects performing a monotonous task with a periodical sampling of their thoughts is enhanced by

RI
PT

stimulation through an anode electrode on the left dlPFC and a cathode electrode on the right
supraorbital area162.

Brain stimulation techniques may also cast light on the cognitive processes involved in dreamlike

SC

experiences. Indeed, an interhemispheric paired pulse transcranial magnetic stimulation (TMS)

study showed a lower interhemispheric connectivity associated with REM sleep, suggesting a

M
AN
U

possible explanation for dream features like the lack of insight, time distortion, and amnesia163.
Other techniques, such as magnetoencephalography (MEG), which allow a better localization of the
regions where the signals originate164, could also be applied to identify the variations in the activity
of specific brain regions subserving given dream features.

TE
D

In summary, multi-channel and intracranial recordings of brain activity have made possible more
refined analyses of EEG signals, identifying specific patterns predictive of dream recall after
awakening from REM and NREM sleep, the functioning of cortical and subcortical nuclei involved

AC
C

sleep stages.

EP

in memory processing, and the role played by specific brain structures stimulated during distinct

5. TOWARD AN INTEGRATIVE APPROACH TO DREAMING AND ITS NEURAL BASIS

The neurophysiological signatures provided by the new methods of sleep recording and analysis
allow accurate correspondences to be established between the characteristics of pre-awakening
sleep and dream recall (and perhaps specific dream contents), thus overcoming some traditional
methodological constraints of dream investigation, such as the much more tentative temporal
location of dreaming (and thus the correspondence of its contents with PSG indicators) compared
with goal-directed mental experiences in wakefulness.
21

ACCEPTED MANUSCRIPT
Closer temporal proximities of physiological markers and dream contents may now be established
by combining one or more of the new methods and the traditional paradigms of dream research. In
particular, two poorly explored dimensions of dream contents, namely their voluntary control and
behavioral enactment, promise important insights into the neural basis and the cognitive processes

RI
PT

of dreaming. Indeed, previously agreed contents may be inserted by lucid dreamers into the ongoing
dream experience in REM sleep159,160,165, and dream contents may be enacted during episodes of
REM sleep behavior disorder (RBD) in patients with this parasomnia166,167.

SC

The finding that there is a greater level of reactivation of the cerebral regions involved in learning a
new task in trained subjects than in controls during REM sleep112 and SWS168 suggests that such

M
AN
U

cerebral reactivation should also be accompanied by that of the task-related information. Pertinent
evidence may be gathered by investigating lucid dreamers159,160,165, as they are aware of the ongoing
dreaming state and capable of both performing predefined actions while all standard PSG criteria
of REM sleep are fulfilled and sending previously agreed eye signals as temporal markers of their

TE
D

lucid state. Indeed, neuronal activation of the sensorimotor cortex during lucid REM dreaming
(measured by fMRI and NIRS) appears comparable to that of a given movement (hand clenching),
both imagined and performed in waking, by the same subjects159,160,169. This finding is important

EP

because EEG analyses have revealed increased gamma band activity over frontal and frontolateral
areas in REM sleep, when the dream is lucid compared with when it is nonlucid159.

AC
C

Interestingly, lucidity is a dimension of dreaming that can be learnt159 or prompted by frontal low
tACS in the lower gamma band160. A similar increase in gamma activity over frontal and
frontolateral areas has also been observed in SOREMP of daytime naps in narcolepsy patients170,
who often report being able to maintain or recover lucidity while dreaming and modify unpleasant
or frightening dream contents161,170.
It would also be of interest to establish whether the same cerebral areas are activated during
different sleep stages, as well as in waking, when the incorporation of target information into dream
content is triggered by an external stimulus previously associated with it (this paradigm being called
22

ACCEPTED MANUSCRIPT
cuing or targeted memory reactivation: TMR171). This issue has been raised by some (indirect)
evidence provided by TMR studies, showing that specific patterns of brain activity in the
hippocampus and neocortex during wakefulness are reactivated during SWS and drive the
consolidation of previously acquired information, for example, paired object-location associations

RI
PT

(learnt while smelling a rose fragrance)172. An entwined crucial issue to be clarified is determining
the capacity of the different sleep stages for memory replay, which is limited for such material as
phrases of an artificial language173. Important insights may be expected from investigating whether:

SC

a) the effectiveness of cues for reactivation varies with respect to their perceptual modality
(olfactory vs auditory172,174), in interaction with their associated information relevance (low/high

M
AN
U

value), and with respect to sleep as a whole, compared with wakefulness, where cues are always
effective172, or to sleep stage; and b) the responsiveness of the brain structures activated by TMR
differs in relation to the cues (for example, the modulation of the activity and connectivity of the
parahippocampal cortex for spatial associations175).

TE
D

The possibility of identifying when specific visual contents are experienced has also been recently
explored, in keeping with the assumptions of the so-called brain reading approach. This refers to
the decoding of perceptual or mental conscious states by brain activity alone, using non-invasive

EP

techniques (for example, multivariate pattern analysis176) capable of decoding mental states with
high accuracy and reasonable temporal resolution. By provoking repeated awakenings just after

AC
C

sleep onset and asking subjects to recall what they had seen, it has been found that fMRI patterns
can be reliably linked, on a probabilistic basis, to the visual information (i.e., categories of objects
such as cars, men or women) in dream reports177. It is apparent that, given the multimodal nature of
dream contents (visual, auditory, tactile, etc.), much more complex pattern-recognition algorithms
are required to decode information from different simultaneous modalities before attempting to
extend brain reading to all dream features (that is, identifying the occurrence of contents with
different perceptual features and their correlates in the activity of specific brain regions). However,
the possibility of brain reading is also supported, in principle, by data collected with intracranial
23

ACCEPTED MANUSCRIPT
EEG recordings across the medial temporal lobe and neocortex during sleep and wakefulness, and
during visual stimulation with fixation178. Single neurons exhibit reduced firing rates before REMs
and increasing rates immediately after REMs, similarly to the activity pattern upon image
presentation during fixation in wakefulness. Furthermore, theta oscillations similarly reset following

RI
PT

eye movements in sleep and wakefulness, as well as after visual stimulation.

The interpretative hypothesis that REMs during sleep rearrange discrete epochs of visual-like
processing, as during wakefulness, is compatible with the findings of a study where the directions

SC

of REMs in RBD patients during dream enactment were matched with the description of dream
content reported after awakening179. Moreover, the activity pattern of the motor cortex during

M
AN
U

phasic REM appears similar to that preceding a movement during wakefulness compared to tonic
REM of the same motor cortex, and to the EEG activity pattern of dlPFC during both phasic and
tonic REM sleep180.

A close correspondence between one or more PSG markers and specific contents of dream reports

TE
D

can also be established by observing video-PSG recordings of patients with RBD disorder. Indeed,
external raters blindly analyzing video-PSG and dream reports181 can establish reliably whether
dream contents, such as movements and vocalizations enacted during RBD episodes, correspond to

EP

those reported after awakening166. This means that some observed motor behaviors can be
considered markers of the concomitant elaboration of specific REM dream contents, which thus

AC
C

become predictable before reporting. The observation of enacted contents also confirms that
dreaming is actually developed by RBD patients who always fail to recall dreams after
awakening182.

Moreover, the possibility that two or more RBD episodes may occur in the same period of REM
sleep of patients with narcolepsy allows the tentative temporal localization not only of the enacted,
but also of the intermediate contents, which reflect REM-sleep/wakefulness dissociative phenomena
(for example, awareness of dream-state, volitional control of contents or out-of-body
experiences)183. This, albeit limited, reconstruction of the time course of dreaming might, in turn,
24

ACCEPTED MANUSCRIPT
facilitate the identification of specific EEG correlates of dissociative phenomena (such as prefrontal
gamma activity for the awareness of dreaming-state159,161).
To sum up, the use of multiple techniques of sleep recording allows an accurate operational
approach to such complex issues as the temporal location of given contents (as made possible by

RI
PT

comparing video-PSG recordings with verbal reports in the case of dream enactment in RBD
episodes), as well as of episodes of lucid dreaming, and the replay of pre-sleep acquired information

SC

for incorporation into dream content.

6. CONCLUSION

M
AN
U

Taken together, the findings reviewed clearly indicate that the development of new PSG, videorecording and neuroimaging techniques has been an important step in the process of identifying the
neural basis of dreaming. Indeed, their development has led to a more accurate assessment of the
temporal location of dreaming during sleep and, possibly, to a clarification of the time course of

TE
D

specific contents, as well as of the factors responsible for the intra- and inter-individual variability
in dream generation and recall. Moreover, the construction of general models of mental experience
as a consciousness phenomenon of sleep and waking has generated more specific hypotheses on the

EP

neural basis of dreaming and guided the collection of reliable data for both mental activity and
regional cerebral activity during PSG-defined sleep stages. Even if PSG and neuroimaging have

AC
C

seldom been combined to date, technical advances will lead to more accurate and pertinent
questions as to the neural correlates of dreaming and its features.
Finally, the use of neuroimaging techniques may strengthen the reliability of dream reports against
some persistent skepticism1. Indeed, fMRI measurements have disclosed important differences in
the activation of specific brain areas (right inferior frontal gyrus, right superior and middle temporal
gyrus) when an actually experienced dream is recalled compared with one listened to or read in
wakefulness or with a daytime mental activity184. The observation of these differences provides a
strong argument supporting the reliability of dream reports and, overall, suggests a further strategy
25

ACCEPTED MANUSCRIPT
for the investigation of both the inter-individual (HDR vs LDR) and intra-individual (success vs
failure) differences in dream recall.
There seems to be no doubt that the new techniques of sleep recordings, used on their own or
combined with those of neuroimaging analysis of brain functioning, are yielding important new

RI
PT

insights into how the brain generates dreams during sleep, as well as dreamlike experiences in
waking. These insights converge to indicate that the continuity between the mental experiences
elaborated in waking and sleep primarily manifests itself in terms of similarity in the functioning of

SC

the cognitive processes involved in their processing, rather than in the types or amount of memories

M
AN
U

transformed into dream contents2,5.

PRACTICE POINTS

A more or less dreamlike mental experience is reported after over 80% of awakenings from REM

TE
D

sleep and about 50% of awakenings from NREM sleep.

There is a large inter-individual (high/low recallers) and intra-individual variability (between stages
and nights) in dream recall frequency and in perceptual and formal characteristics of dream

EP

experience.

Clinical studies on the success/failure of dream recall and on perceptual and formal characteristics
of dream experience in patients with acute brain damage have documented that, overall, the

AC
C

temporoparieto-occipital junction and the ventromedial prefrontal cortex are involved in dreaming.

Neuroimaging studies have substantially confirmed clinical indications on the neural bases of
dreaming and disclosed a certain parallelism between the functioning of specific brain structures in
dreaming during sleep and daydreaming, mind-wandering and resting states in wakefulness.

Intracranial sleep recordings and high-density electroencephalography have provided new insights
into dreaming during various sleep stages and off-line mental experiences in waking.

26

ACCEPTED MANUSCRIPT
The new techniques of sleep recording and quantitative analysis of sleep have led to the
development of new research strategies and the revitalization of traditional paradigms.

RESEARCH AGENDA

RI
PT

The functioning of specific cognitive processes (e.g., activation of episodic and semantic
information, access to associative networks, working memory) during various sleep stages and
cycles compared to their functioning in wake should be established in detail.

SC

Investigation into the relations between dream generation and recall and EEG features of prior sleep
should benefit from the evaluation of intracranial cortical and subcortical recordings.

M
AN
U

Trait-like (high/low recallers) and state-like (sleep stages/cycles) differences in dream recall should
be further investigated using hd-EEG (and fMRI) techniques.

Comparison of the activation of frontal and temporal brain structures during the recall of actual
dreams and listened to or read dreams and imagined events may elucidate the different recall

TE
D

strategies in high and low recallers.

Assessing the predictive power of theta EEG oscillations in frontal regions for dream generation
and memory encoding during REM sleep of distinct cycles should be established to identify

EP

circadian variations in the frequency and characteristics of dream experience.

The correspondence of specific (motor or verbal) dream contents and their enactment in RBD

AC
C

episodes may allow the identification of both the temporal location during REM sleep of dissociated
REM-sleep/wakefulness phenomena and facilitate the detection of EEG markers (such as gamma
activity for dream lucidity).

The role of dreaming in the reprocessing and consolidation of memories should be investigated by
combining SEEG techniques and targeted memory reactivation (i.e., cuing) during distinct sleep
stages and cycles.

Conflict of interest
All authors report no conflict of interest.
27

ACCEPTED MANUSCRIPT
Acknowledgments
This work was supported by grants from the Fondazione del Monte di Bologna e Ravenna to Carlo
Cipolli (RF: 2012-2407) and from the Italian Ministry of Health (RF:2009-1528677) to Luigi De

RI
PT

Gennaro. The authors are indebted to Cristina Marzano and Fabio Moroni for their comments on a
preliminary version, to Alessandra Laffi for secretarial assistance and to an anonymous reviewer for

AC
C

EP

TE
D

M
AN
U

SC

many thorough comments and helpful suggestions.

28

ACCEPTED MANUSCRIPT
References
1. Windt JM. Reporting dream experience: Why (not) to be skeptical about dream reports. Front
Hum Neurosci 2013;7:708.
*2. Wamsley EJ. Dreaming, waking conscious experience, and the resting brain: report of
subjective experience as a tool in the cognitive neurosciences. Front Psychol 2013;4:637.

RI
PT

3. Fox KCR, Nijeboer S, Solomonova E, Domhoff GW, Christoff K. Dreaming as mind wandering:
evidence from functional neuroimaging and first-person content reports. Front Hum Neurosci
2013;7:412.

SC

4. De Gennaro L, Marzano C, Cipolli C, Ferrara M. How we remember the stuff that dreams are
made of: neurobiological approaches to the brain mechanisms of dream recall. Behav Brain Res
2012;226:5926.

M
AN
U

5. Graveline YM, Wamsley EJ. Dreaming and waking cognition. Transl. Issues Psychol. Sci.
2015;1:97105.
6. Pace-Schott EF. Dreaming as a story-telling instinct. Front Psychol 2013;4:159.
*7. Hobson JA, Pace-Schott EF, Stickgold R. Dreaming and the brain: toward a cognitive
neuroscience of conscious states. Behav Brain Sci 2000;23:793842.
*8. Nielsen TA. A review of mentation in REM and NREM sleep: covert REM sleep as a
possible reconciliation of two opposing models. Behav Brain Sci 2000;23:85166.

TE
D

9. Aserinsky E, Kleitman N. Regularly occurring periods of eye motility, and concomitant

phenomena, during sleep. Science 1953;118:2734.

EP

10. Dement W, Kleitman N. The relation of eye movements during sleep to dream activity: an
objective method for the study of dreaming. J Exp Psychol 1957;53:33946.
11. Dement W, Kleitman N. Cyclic variations in EEG during sleep and their relation to eye
movements, body motility, and dreaming. Electroencephalogr Clin Neurophysiol 1957;9:67390.

AC
C

12. Antrobus JS, Fein G, Jordan L, Ellman SJ, Arkin AM. Measurement and design in research on
sleep reports. In: Ellman SJ, Antrobus JS, (eds) The mind in sleep: psychology and physiology.
New York, NY: John Wiley & Sons, Inc;1991.
13. Foulkes WD. Dream reports from different stages of sleep. J Abnorm Soc Psychol 1962;65:14
25.
14. Foulkes D, Vogel G. Mental activity at sleep onset. J Abnorm Psychol 1965;70:23143.
15. Pivik T, Foulkes D. NREM mentation: relation to personality, orientation time, and time of
night. J Consult Clin Psychol 1968;32:14451.
16. Taub JM. Dreams recalled spontaneously following afternoon naps and nocturnal sleep. J
Abnorm Psychol 1971;78:22931.
29

ACCEPTED MANUSCRIPT
17. Snyder, F. The phenomenology of dreaming. In: L.Meadow and L.Snow (eds) The
Psychodynamic Implications of the Physiological Studies on Dreams. Springfield, Illinois: Thomas,
1970:124151.
18. Foulkes D, Schmidt M. Temporal sequence and unit composition in dream reports from
different stages of sleep. Sleep 1983;6:26580.

RI
PT

19. Antrobus J, Kondo T, Reinsel R, Fein G. Dreaming in the late morning: summation of REM and
diurnal cortical activation. Conscious Cogn 1995;4:27599.
20. Wamsley EJ, Hirota Y, Tucker MA, Smith MR, Antrobus JS. Circadian and ultradian influences
on dreaming: a dual rhythm model. Brain Res Bull 2007;71:34754.

SC

21. De Gennaro L, Marzano C, Moroni F, Curcio G, Ferrara M, Cipolli C. Recovery sleep after
sleep deprivation almost completely abolishes dream recall. Behav Brain Res 2010;206:2938.

M
AN
U

22. Nielsen T, Stenstrom P, Takeuchi T, Saucier S, Lara-Carrasco J, Solomonova E, et al. Partial

REM-sleep deprivation increases the dream-like quality of mentation from REM sleep and sleep
onset. Sleep 2005;28:10839.
*23. Oudiette D, Dealberto M-J, Uguccioni G, Golmard J-L, Merino-Andreu M, Tafti M, et al.
Dreaming without REM sleep. Conscious Cogn 2012;21:112940.
24. Siclari F, Larocque JJ, Postle BR, Tononi G. Assessing sleep consciousness within subjects
using a serial awakening paradigm. Front Psychol 2013;4:542.

TE
D

25. Desseilles M, Dang-Vu TT, Sterpenich V, Schwartz S. Cognitive and emotional processes
during dreaming: a neuroimaging view. Conscious Cogn 2011;20:9981008.
26. Hefez A, Metz L, Lavie P. Long-term effects of extreme situational stress on sleep and
dreaming. Am J Psychiatry 1987;144:3447.

EP

27. Stickgold R, Malia A, Fosse R, Propper R, Hobson JA. Brain-mind states: I. Longitudinal field
study of sleep/wake factors influencing mentation report length. Sleep 2001;24:1719.

AC
C

28. Monroe LJ, Rechtschaffen A, Foulkes D, Jensen J. Discriminability of REM and NREM
reports. J Pers Soc Psychol 1965;2:45660.
29. Cavallero C, Cicogna P, Natale V, Occhionero M, Zito A. Slow wave sleep dreaming. Sleep
1992;15:5626.
30. Cipolli C, Guazzelli M, Bellucci C, Mazzetti M, Palagini L, Rosenlicht N, et al. Time-of-night
variations in the story-like organization of dream experience developed during rapid eye movement
sleep. J Sleep Res 2015;24:23440.
31. Cohen DB. Sleep and Dreaming: Origins, Nature and Functions. Oxford, OX: Pergamon Press;
1979.
32. Schredl M, Wittmann L, Ciric P, Gtz S. Factors of home dream recall: a structural equation
model. J Sleep Res 2003;12:13341.
30

ACCEPTED MANUSCRIPT
33. Goodenough DR, Lewis HB, Shapiro A, Jaret L, Sleser I. Dream reporting following abrupt and
gradual awakenings from different types of sleep. J Pers Soc Psychol 1965;2:1709.
34. Kahn D, Stickgold R, Pace-Schott EF, Hobson JA. Dreaming and waking consciousness: a
character recognition study. J Sleep Res 2000;9:31725.

RI
PT

35. Cipolli C, Fagioli I, Baroncini P, Fumai A, Marchi B, Sancini M, et al. Recall of mental sleep
experience with or without prior verbalization. Am J Psychol 1992;105:385407.
36. Cohen DB, Wolfe G. Dream recall and repression: evidence for an anternative hypothesis. J
Consult Clin Psychol 1973;41:34955.

SC

37. Beaulieu-Prvost D, Zadra A. Absorption, psychological boundaries and attitude towards

dreams as correlates of dream recall: two decades of research seen through a meta-analysis. J Sleep
Res 2007;16:519.

M
AN
U

38. Malinowski JE. Dreaming and personality: Wake-dream continuity, thought suppression, and
the Big Five Inventory. Conscious Cogn 2015;38:915..
39. Zadra A, Robert G. Dream recall frequency: impact of prospective measures and motivational
factors. Conscious Cogn 2012;21:1695702.
40. Schredl M, Reinhard I. Gender differences in dream recall: a meta-analysis. J Sleep Res
2008;17:12531.
41. Pagel JF. Non-dreamers. Sleep Med 2003;4:23541.

TE
D

42. Sharf B, Moskovitz C, Lupton MD, Klawans HL. Dream phenomena induced by chronic
levodopa therapy. J Neural Transm 1978;43:14351.

EP

43. Nausieda PA, Weiner WJ, Kaplan LR, Weber S, Klawans HL. Sleep disruption in the course of
chronic levodopa therapy: an early feature of the levodopa psychosis. Clin Neuropharmacol
1982;5:18394.

AC
C

44. Solms M. The neuropsychology of dreaming: A clinico-anatomical study. Mahwah, NJ:

Lawrence Erlbaum Associates;1997.
*45. Solms M. Dreaming and REM sleep are controlled by different brain mechanisms. Behav
Brain Sci 2000;23:84350.
46 Hartmann E, Russ D, Oldfield M, Falke R, Skoff B. Dream content: effects of l-DOPA. Sleep
Res 1980;9:153.
47. Fosse MJ, Fosse R, Hobson JA, Stickgold RJ. Dreaming and episodic memory: a functional
dissociation? J Cogn Neurosci 2003;15:19.
48. Malinowski JE, Horton CL. Memory sources of dreams: the incorporation of autobiographical
rather than episodic experiences. J Sleep Res 2014;23:4417.
49. Baylor GW, Cavallero C. Memory sources associated with REM and NREM dream reports
throughout the night: a new look at the data. Sleep 2001;24:16570.
31

ACCEPTED MANUSCRIPT
50. Nielsen TA, Stenstrom P. What are the memory sources of dreaming? Nature 2005;437:12869.
51. Nielsen TA, Kuiken D, Alain G, Stenstrom P, Powell RA. Immediate and delayed
incorporations of events into dreams: further replication and implications for dream function. J
Sleep Res 2004;13:32736.

RI
PT

52. Foulkes D, Rechtschaffen A. Presleep determinants of dream content: effect of two films.
Percept Mot Skills 1964;19:9831005.
53. Burton SA, Harsh JR, Badia P. Cognitive activity in sleep and responsiveness to external
stimuli. Sleep 1988;11:618.

SC

54. Badia P, Wesensten N, Lammers W, Culpepper J, Harsh J. Responsiveness to olfactory stimuli

presented in sleep. Physiol Behav 1990;48:8790.

M
AN
U

55. Cipolli C, Fagioli I, Maccolini S, Salzarulo P. Associative relationships between pre-sleep

sentence stimuli and reports of mental sleep experience. Percept Mot Skills 1983;56:22334.
56. Stickgold R, Malia A, Maguire D, Roddenberry D, OConnor M. Replaying the game:
hypnagogic images in normals and amnesics. Science 2000;290:3503.
57. Rechtschaffen A, Vogel G, Shaikun G. Interrelatedness of mental activity during sleep. Arch
Gen Psychiatry 1963;9:53647.

TE
D

58. Kramer M, Whitman RM, Baldridge BJ, Lansky LM. Patterns of dreaming: the interrelationship
of the dreams of a night. J Nerv Ment Dis 1964;139:42639.
59. Cipolli C, Fagioli I, Baroncini P, Fumai A, Marchi B, Sancini M. The thematic continuity of
mental experiences in REM and NREM sleep. Int J Psychophysiol 1988;6:30713.

EP

60. Fagioli I, Cipolli C, Tuozzi G. Accessing previous mental sleep experience in REM and NREM
sleep. Biol Psychol 1989;29:2738.

AC
C

61. Hoelscher TJ, Klinger E, Barta SG. Incorporation of concern- and nonconcern-related verbal
stimuli into dream content. J Abnorm Psychol. 1981;90: 8891.
62. Cartwright R, Agargun MY, Kirkby J, Friedman JK. Relation of dreams to waking concerns.
Psychiatry Res 2006;141:26170.
63. Horton CL, Malinowski JE. Autobiographical memory and hyperassociativity in the dreaming
brain: implications for memory consolidation in sleep. Front Psychol 2015;6:874.
*64. Nielsen TA. Chronobiological features of dream production. Sleep Med Rev 2004;8:40324.
65. Blagrove M, Fouquet NC, Henley-Einion JA, Pace-Schott EF, Davies AC, Neuschaffer JL, et
al. Assessing the dream-lag effect for REM and NREM stage 2 dreams. PLoS ONE 2011;6:e26708.
66. van Rijn E, Eichenlaub J-B, Lewis PA, Walker MP, Gaskell MG, Malinowski JE, et al. The
dream-lag effect: Selective processing of personally significant events during Rapid Eye Movement
sleep, but not during Slow Wave Sleep. Neurobiol Learn Mem 2015;122:98109.
32

ACCEPTED MANUSCRIPT
67. Gujar N, McDonald SA, Nishida M, Walker MP. A role for REM sleep in recalibrating the
sensitivity of the human brain to specific emotions. Cereb Cortex 2011;21:11523.
68. Pace-Schott EF, Germain A, Milad MR. Effects of sleep on memory for conditioned fear and
fear extinction. Psychol Bull 2015;141:83557.

RI
PT

69. Germain A. Sleep disturbances as the hallmark of PTSD: where are we now? Am J Psychiatry
2013;170:37282.
70. Levin R, Nielsen TA. Disturbed dreaming, posttraumatic stress disorder, and affect distress: a
review and neurocognitive model. Psychol Bull 2007;133:482528.

SC

71. Nielsen T, Levin R. Nightmares: a new neurocognitive model. Sleep Med Rev 2007;11:295
310.

M
AN
U

72. van der Helm E, Yao J, Dutt S, Rao V, Saletin JM, Walker MP. REM sleep depotentiates
amygdala activity to previous emotional experiences. Curr Biol 2011;21:202932.
73. Stickgold R, Walker MP. Sleep-dependent memory triage: evolving generalization through
selective processing. Nat Neurosci 2013;16:13945.
74. Ritchie TD, Skowronski J. Perceived change in the affect associated with dreams: the fading
affect bias and its moderators. Dreaming 2008;18,2743.

TE
D

75. Walker MP, van der Helm E. Overnight therapy? The role of sleep in emotional brain
processing. Psychol Bull 2009;135:73148.
76. Malinowski JE, Horton CL. Metaphor and hyperassociativity: the inagination mechanisms
behind emotion assimilation in sleep and dreaming. Front. Psychol. 2015; 6: 1132.

EP

77. Llewellyn S. Such stuff as dreams are made on? Elaborative encoding, the ancient art of
memory, and the hippocampus. Behav Brain Sci 2013;36:589607.

AC
C

78. Cipolli C, Poli D. Story structure in verbal reports of mental sleep experience after awakening in
REM sleep. Sleep 1992;15:13342.
79. Montangero J, Ivanyi CT, de Saint-Hilaire Z. Completeness and accuracy of morning reports
after a recall cue: comparison of dream and film reports. Conscious Cogn 2003;12:4962.
80. Wamsley EJ, Tucker M, Payne JD, Benavides JA, Stickgold R. Dreaming of a learning task is
associated with enhanced sleep-dependent memory consolidation. Curr Biol 2010;20:8505.
81. Wamsley EJ, Perry K, Djonlagic I, Reaven LB, Stickgold R. Cognitive replay of visuomotor
learning at sleep onset: temporal dynamics and relationship to task performance. Sleep 2010;33:59
68.
82. Wamsley EJ, Stickgold R. Memory, Sleep and Dreaming: Experiencing Consolidation. Sleep
Med Clin 2011;6:97108.

33

ACCEPTED MANUSCRIPT
83. Arkin AM, Antrobus JS. The effects of external stimuli applied prior to and during sleep on
sleep experience. In: Ellman SJ, Antrobus JS (eds) The mind in sleep: psychology and physiology.
New York, NY: John Wiley & Sons, Inc;1991:256-307.
84. Cipolli C, Fagioli I, Mazzetti M, Tuozzi G. Incorporation of presleep stimuli into dream
contents: evidence for a consolidation effect on declarative knowledge during REM sleep? J Sleep
Res 2004;13:31726.

RI
PT

85. Wamsley EJ. Dreaming and offline memory consolidation. Curr Neurol Neurosci Rep
2014;14:433.

SC

86. Dumel G, Carr M, Marquis L-P, Blanchette-Carrire C, Paquette T, Nielsen T. Infrequent dream
recall associated with low performance but high overnight improvement on mirror-tracing. J Sleep
Res 2015;24:37282.
87. Murri L, Arena R, Siciliano G, Mazzotta R, Muratorio A. Dream recall in patients with focal
cerebral lesions. Arch Neurol 1984;41:1835.

M
AN
U

88. Doricchi F, Violani C. Dream recall in brain-damaged patients: A contribution to the

neuropsychology of dreaming through a review of the literature. In: Antrobus JS, Bertini M (eds)
The neuropsychology of sleep and dreaming. Hillsdale, NJ: Erlbaum, 1992:99-129.
89. Gaillard JM. Brain lateralization during sleep and dreaming. In: Horne JA (ed.) Sleep '88.
Stuttgart: Fischer Verlag, 1989:177-81.

TE
D

90. Fuller PM, Saper CB, Lu J. The pontine REM switch: past and present. J Physiol 2007;584:
73541.
91.Lavie P, Pratt H, Scharf B, Peled R, Brown J. Localized pontine lesion: nearly total absence of
REM sleep. Neurology 1984;34:11820.

EP

92. Jacobs L, Feldman M, Bender MB. Eye movements during sleep. I. The pattern in the normal
human. Arch Neurol 1971;25:1519.

AC
C

93. Hobson JA, Stickgold R, Pace-Schott EF. The neuropsychology of REM sleep dreaming.
Neuroreport 1998;9:R114.
94. Muzur A, Pace-Schott EF, Hobson JA. The prefrontal cortex in sleep. Trends Cogn Sci
2002;6:47581.
95. Solms M. Neurobiology and the neurological basis of dreaming. Handb Clin Neurol
2011;98:51944.
96. Leu-Semenescu S, Uguccioni G, Golmard J-L, Czernecki V, Yelnik J, Dubois B, et al. Can we
still dream when the mind is blank? Sleep and dream mentations in auto-activation deficit. Brain
2013;136:307684.
97. Murri L, Massetani R, Siciliano G, Giovanditti L, Arena R. Dream recall after sleep interruption
in brain-injured patients. Sleep 1985;8:35662.
98. Greenberg MS, Farah MJ. The laterality of dreaming. Brain Cogn 1986;5:30721.
34

ACCEPTED MANUSCRIPT
99. Kosslyn SM, Ganis G, Thompson WL. Neural foundations of imagery. Nat Rev Neurosci
2001;2:63542.
100. Kerr NH, Foulkes D. Right hemispheric mediation of dream visualization: a case study. Cortex
1981;17:6039.

RI
PT

101. Kosslyn SM, Thompson WL, Alpert NM. Neural systems shared by visual imagery and visual
perception: a positron emission tomography study. Neuroimage 1997;6:32034.
102. Bischof M, Bassetti CL. Total dream loss: a distinct neuropsychological dysfunction after
bilateral PCA stroke. Ann Neurol 2004;56:5836.

SC

103. Murri L, Mancino M, Massetani R, Canapicchi R, Puglioli M, Rossi G Effect of acute and
chronic brain damage on dreaming. Res Comm Psychol Psychiatry Behav 1989;14:12142.

M
AN
U

104. Poryazova R, Huber R, Khatami R, Werth E, Brugger P, Barath K, et al. Topographic sleep
EEG changes in the acute and chronic stage of hemispheric stroke. J Sleep Res 2015;24:5465.
105. Maquet P, Pters J, Aerts J, Delfiore G, Degueldre C, Luxen A, et al. Functional neuroanatomy
of human rapid-eye-movement sleep and dreaming. Nature 1996;383:1636.
106. Maquet P, Degueldre C, Delfiore G, Aerts J, Pters JM, Luxen A, et al. Functional
neuroanatomy of human slow wave sleep. J Neurosci 1997;17:280712.

TE
D

107. Braun AR, Balkin TJ, Wesenten NJ, Carson RE, Varga M, Baldwin P, et al. Regional cerebral
blood flow throughout the sleep-wake cycle. An H2(15)O PET study. Brain 1997;120:117397.
108. Braun AR, Balkin TJ, Wesensten NJ, Gwadry F, Carson RE, Varga M, et al. Dissociated
pattern of activity in visual cortices and their projections during human rapid eye movement sleep.
Science 1998;279:915.

EP

*109. Nir Y, Tononi G. Dreaming and the brain: from phenomenology to neurophysiology. Trends
Cogn Sci 2010;14:88100.

AC
C

110. Pace-Schott EF. The neurobiology of dreaming. In: Kryger MH, Roth T, Dement WC (eds)
Principles and Practice of Sleep Medicine (5th edn). Philadelphia, PA: Elsevier, 2011:563575
111. Dang-Vu TT, Schabus M, Desseilles M, Sterpenich V, Bonjean M, Maquet P. Functional
neuroimaging insights into the physiology of human sleep. Sleep 2010;33:1589603.
112. Maquet P, Ruby P, Maudoux A, Albouy G, Sterpenich V, et al.. Human cognition during
REM sleep and the activity profile within frontal and parietal cortices: a reappraisal of functional
neuroinaging data.Prog Brain Res. 2005;150:219-27
113. Scarpelli S, DAtri A, Gorgoni M, Ferrara M, Gennaro LD. EEG oscillations during sleep and
dream recall: state- or trait-like individual differences? Front Psychol 2015;6:605.
114. Foulkes D, Fleisher S. Mental activity in relaxed wakefulness. J Abnorm Psychol 1975;84:66
75.
35

ACCEPTED MANUSCRIPT
115. Christoff K, Gordon AM, Smallwood J, Smith R, Schooler JW. Experience sampling during
fMRI reveals default network and executive system contributions to mind wandering. Proc Natl
Acad Sci USA 2009;106:871924.
116. Wu CW, Liu PY, Tsai PJ, Wu YC, Hung CS et al. Variations in connectivity in the
sensorimotor and default-mode networks during the first nocturnal sleep cycle. Brain Connect.
2012;2:177-90.

RI
PT

117. Koike T, Kan S, Misaki M, Connectivity pattern changes in default-mode network with deep
non-REM and REM sleep. Neurosci Res. 2011;69:322-30.
118) Picchioni D, Duyn JH, Horovitz SG. Sleep and the functional connectome. Neuroimage
2013;80:387-96

SC

119. Domhoff GW. The neural substrate for dreaming: is it a subsystem of the default network?
Conscious Cogn 2011;20:116374.

M
AN
U

*120. Pace-Schott EF, Picchioni D. The neurobiology of dreaming. In: Kryger MH, Roth T,
Dement WC (eds.), Principles and Practice of Sleep Medicine (6th edn). Philadelphia: Elsevier,
2016: 529-38.
121. Schwartz S, Maquet P. Sleep imaging and the neuro-psychological assessment of dreams.
Trends Cogn Sci 2002;6:2330.
122. Pace-Schott EF. The frontal lobes and dreaming. In: Barrett D, McNamara P (eds) The new
science of dreaming: Vol. 1.Westport, CT: Praeger, Greenwood Press, 2007:115154.

TE
D

123. Eichenlaub J-B, Bertrand O, Morlet D, Ruby P. Brain reactivity differentiates subjects with
high and low dream recall frequencies during both sleep and wakefulness. Cereb Cortex
2014;24:120615.

EP

124. Eichenlaub J-B, Nicolas A, Daltrozzo J, Redout J, Costes N, Ruby P. Resting brain activity
varies with dream recall frequency between subjects. Neuropsychopharmacology 2014;39:1594
602.

AC
C

125. De Gennaro L, Cipolli C, Cherubini A, Assogna F, Cacciari C, Marzano C, et al. Amygdala

and hippocampus volumetry and diffusivity in relation to dreaming. Hum Brain Mapp
2011;32:145870.
126. De Gennaro L, Lanteri O, Piras F, Scarpelli S, Assogna F, Ferrara M, et al. Dopaminergic
system and dream recall: An MRI study in Parkinsons disease patients. Hum Brain Mapp
2016;37:113647.
127. Fox KCR, Spreng RN, Ellamil M, Andrews-Hanna JR, Christoff K. The wandering brain:
meta-analysis of functional neuroimaging studies of mind-wandering and related spontaneous
thought processes. Neuroimage 2015;111:61121.
128. Carr M, Nielsen T. Daydreams and nap dreams: Content comparisons. Conscious Cogn
2015;36:196205.

36

ACCEPTED MANUSCRIPT
129. Doricchi F, Iaria G, Silvetti M, Figliozzi F, Siegler I. The "ways" we look at dreams: evidence
from unilateral spatial neglect (with an evolutionary account of dream bizarreness). Exp Brain Res.
2007;178:450-61.
130. Daltrozzo J, Claude L, Tillmann B, Bastuji H, Perrin F. Working memory is partially
preserved during sleep. PLoS ONE 2012;7:e50997.

RI
PT

131. Wamsley EJ, Antrobus JS. The expression of trace conditioning during non-REM sleep and its
relation to subjective experience. Neurobiol Learn Mem 2009;92:28391.
132. Fell J, Klaver P, Lehnertz K, Grunwald T, Schaller C, Elger CE, et al. Human memory
formation is accompanied by rhinal-hippocampal coupling and decoupling. Nat Neurosci
2001;4:125964.

SC

133. Steinvorth S, Wang C, Ulbert I, Schomer D, Halgren E. Human entorhinal gamma and theta
oscillations selective for remote autobiographical memory. Hippocampus 2010;20:16673.

M
AN
U

*134. Fell J, Fernndez G, Lutz MT, Kockelmann E, Burr W, Schaller C, et al. Rhinal-hippocampal
connectivity determines memory formation during sleep. Brain 2006;129:10814.
135. Misane I, Tovote P, Meyer M, Spiess J, Ogren SO, Stiedl O. Time-dependent involvement of
the dorsal hippocampus in trace fear conditioning in mice. Hippocampus 2005;15:41826.
136. Schabus M, Dang-Vu TT, Albouy G, Balteau E, Boly M, Carrier J, et al. Hemodynamic
cerebral correlates of sleep spindles during human non-rapid eye movement sleep. Proc Natl Acad
Sci USA 2007;104:131649.

TE
D

137. Kahn D, Pace-Schott EF, Hobson JA. Consciousness in waking and dreaming: the roles of
neuronal oscillation and neuromodulation in determining similarities and differences. Neuroscience
1997;78:1338.

EP

138. Cantero JL, Atienza M, Madsen JR, Stickgold R. Gamma EEG dynamics in neocortex and
hippocampus during human wakefulness and sleep. Neuroimage 2004;22:127180.

AC
C

139. Fell J, Staedtgen M, Burr W, Kockelmann E, Helmstaedter C, Schaller C, et al. Rhinalhippocampal EEG coherence is reduced during human sleep. Eur J Neurosci 2003;18:17116.
140. Takeuchi T, Ogilvie RD, Murphy TI, Ferrelli AV. EEG activities during elicited sleep onset
REM and NREM periods reflect different mechanisms of dream generation.. Clin Neurophysiol
2003;114:21020.
141. Esposito MJ, Nielsen TA, Paquette T. Reduced Alpha power associated with the recall of
mentation from Stage 2 and Stage REM sleep. Psychophysiology 2004;41:28897.
142. Marzano C, Ferrara M, Mauro F, Moroni F, Gorgoni M, Tempesta D, et al. Recalling and
forgetting dreams: theta and alpha oscillations during sleep predict subsequent dream recall. J
Neurosci 2011;31:667483.
143. Scarpelli S, Marzano C, DAtri A, Gorgoni M, Ferrara M, De Gennaro L. State- or trait-like
individual differences in dream recall: preliminary findings from a within-subjects study of multiple
nap REM sleep awakenings. Front Psychol 2015;6:928.
37

ACCEPTED MANUSCRIPT
144. Mlle M, Marshall L, Fehm HL, Born J. EEG theta synchronization conjoined with alpha
desynchronization indicate intentional encoding. Eur J Neurosci 2002;15:9238.
145. Klimesch W. EEG alpha and theta oscillations reflect cognitive and memory performance: a
review and analysis. Brain Res Brain Res Rev 1999;29:16995.

RI
PT

146. Osipova D, Takashima A, Oostenveld R, Fernndez G, Maris E, Jensen O. Theta and gamma
oscillations predict encoding and retrieval of declarative memory. J Neurosci 2006;26:752331.
147. Sederberg PB, Kahana MJ, Howard MW, Donner EJ, Madsen JR. Theta and gamma
oscillations during encoding predict subsequent recall. J Neurosci 2003;23:1080914.

SC

148. Anderson KL, Rajagovindan R, Ghacibeh GA, Meador KJ, Ding M. Theta oscillations mediate
interaction between prefrontal cortex and medial temporal lobe in human memory. Cereb Cortex
2010;20:160412.

M
AN
U

149. Chellappa SL, Frey S, Knoblauch V, Cajochen C. Cortical activation patterns herald successful
dream recall after NREM and REM sleep. Biol Psychol 2011;87:2516.
150. Koulack D, Goodenough DR. Dream recall and dream recall failure: an arousal-retrieval
model. Psychol Bull 1976;83:975984.
151. Krueger JM, Rector DM, Roy S, Van Dongen HPA, Belenky G, Panksepp J. Sleep as a
fundamental property of neuronal assemblies. Nat Rev Neurosci 2008;9:9109.

TE
D

152. Krueger JM, Tononi G. Local use-dependent sleep; synthesis of the new paradigm. Curr Top
Med Chem 2011;11:24902.
153. Magnin M, Bastuji H, Garcia-Larrea L, Mauguire F. Human thalamic medial pulvinar nucleus
is not activated during paradoxical sleep. Cereb Cortex 2004;14:85862.

EP

154. Massimini M, Ferrarelli F, Murphy M, Huber R, Riedner B, Casarotto S et al. Cortical

reactivity and effective connectivity during REM sleep in humans. Cogn Neurosci 2010;1:176-83

AC
C

155. Marshall L, Mlle M, Hallschmid M, Born J. Transcranial direct current stimulation during
sleep improves declarative memory. J Neurosci 2004;24:998592.
156. Jakobson AJ, Fitzgerald PB, Conduit R. Induction of visual dream reports after transcranial
direct current stimulation (tDCs) during Stage 2 sleep. J Sleep Res 2012;21:36979.
157. Jakobson AJ, Fitzgerald PB, Conduit R. Investigation of dream reports after transcranial direct
current stimulation (tDCs) during slow wave sleep (SWS). J Sleep Biol Rhythms 2012;10:16978.
158. Stumbrys T, Erlacher D, Schredl M. Testing the involvement of the prefrontal cortex in lucid
dreaming: a tDCS study. Conscious Cogn 2013;22:121422.
159.Voss U, Holzmann R, Tuin I, Hobson JA. Lucid dreaming: a state of consciousness with
features of both waking and non-lucid dreaming. Sleep 2009;32:1191200.

38

ACCEPTED MANUSCRIPT
160. Voss U, Holzmann R, Hobson A, Paulus W, Koppehele-Gossel J, Klimke A, et al. Induction of
self awareness in dreams through frontal low current stimulation of gamma activity. Nat Neurosci
2014;17:8102.
161. Dodet P, Chavez M, Leu-Semenescu S, Golmard J-L, Arnulf I. Lucid dreaming in narcolepsy.
Sleep 2015;38:48797.

RI
PT

162. Axelrod V, Rees G, Lavidor M, Bar M. Increasing propensity to mind-wander with

transcranial direct current stimulation. Proc Natl Acad Sci USA 2015;112:33149.

163. Bertini M, De Gennaro L, Ferrara M, Curcio G, Romei V, Fratello F, et al. Reduction of

transcallosal inhibition upon awakening from REM sleep in humans as assessed by transcranial
magnetic stimulation. Sleep 2004;27:87582.

SC

164. Ioannides AA, Corsi-Cabrera M, Fenwick PBC, del Rio Portilla Y, Laskaris NA, Khurshudyan
A, et al. MEG tomography of human cortex and brainstem activity in waking and REM sleep
saccades. Cereb Cortex 2004;14:5672.

M
AN
U

165. Dresler M, Koch SP, Wehrle R, Spoormaker VI, Holsboer F, Steiger A, et al. Dreamed
movement elicits activation in the sensorimotor cortex. Curr Biol 2011;21:18337.
166. Schenck CH, Bundlie SR, Ettinger MG, Mahowald MW. Chronic behavioral disorders of
human REM sleep: a new category of parasomnia. Sleep 1986;9:293308.
167. Arnulf I. REM sleep behavior disorder: motor manifestations and pathophysiology. Mov
Disord 2012;27:67789.

TE
D

168. Peigneux P, Laureys S, Fuchs S, Collette F, Perrin F, Reggers J, et al. Are spatial memories
strengthened in the human hippocampus during slow wave sleep? Neuron 2004;44:53545.

EP

169. Dresler M, Wehrle R, Spoormaker VI, Koch SP, Holsboer F, Steiger A, et al. Neural correlates
of dream lucidity obtained from contrasting lucid versus non-lucid REM sleep: a combined
EEG/fMRI case study. Sleep 2012;35:101720.

AC
C

170. Rak M, Beitinger P, Steiger A, Schredl M, Dresler M. Increased lucid dreaming frequency in
narcolepsy. Sleep 2015;38:78792.
171. Oudiette D, Paller KA. Upgrading the sleeping brain with targeted memory reactivation.
Trends Cogn Sci 2013;17:1429.
172. Rasch B, Bchel C, Gais S, Born J. Odor cues during slow-wave sleep prompt declarative
memory consolidation. Science 2007;315:14269.
173. Batterink LJ, Paller KA. Sleep-based memory processing facilitates grammatical
generalization: Evidence from targeted memory reactivation. Brain Lang 2015.
doi:10.1016/j.bandl.2015.09.003.
174. Rudoy JD, Voss JL, Westerberg CE, Paller KA. Strengthening individual memories by
reactivating them during sleep. Science 2009;326:1079.

39

ACCEPTED MANUSCRIPT
175. van Dongen EV, Takashima A, Barth M, Zapp J, Schad LR, Paller KA, et al. Memory
stabilization with targeted reactivation during human slow-wave sleep. Proc Natl Acad Sci USA
2012;109:1057580.
176. Haynes J-D, Rees G. Decoding mental states from brain activity in humans. Nat Rev Neurosci
2006;7:52334.

RI
PT

*177. Horikawa T, Tamaki M, Miyawaki Y, Kamitani Y. Neural decoding of visual imagery during
sleep. Science 2013;340:63942.
178. Andrillon T, Nir Y, Cirelli C, Tononi G, Fried I. Single-neuron activity and eye movements
during human REM sleep and awake vision. Nat Commun 2015;6:7884.

SC

179. Leclair-Visonneau L, Oudiette D, Gaymard B, Leu-Semenescu S, Arnulf I. Do the eyes scan

dream images during rapid eye movement sleep? Evidence from the rapid eye movement sleep
behaviour disorder model. Brain 2010;133:173746.

M
AN
U

180. De Carli F, Proserpio P, Morrone E, Sartori I, Ferrara M, Gibbs SA, et al. Activation of the
motor cortex during phasic rapid eye movement sleep. Ann Neurol 2016;79:32630.
181. Valli K, Frauscher B, Gschliesser V, Wolf E, Falkenstetter T, Schnwald SV, et al. Can
observers link dream content to behaviours in rapid eye movement sleep behaviour disorder? A
cross-sectional experimental pilot study. J Sleep Res 2012;21:219.
182. Herlin B, Leu-Semenescu S, Chaumereuil C, Arnulf I. Evidence that non-dreamers do dream:
a REM sleep behaviour disorder model. J Sleep Res 2015;24:6029.

TE
D

183. Bellucci C, Vandi S, Iloti M, Pizza F, Russo PM, Tuozzi G, et al. Dissociated rapid eye
movement sleep dream experiences in type 1 narcolepsy: a case report. Sleep Med. 2016;19;150-2.

AC
C

EP

184. Benedetti F, Poletti S, Radaelli D, Ranieri R, Genduso V, Cavallotti S, et al. Right hemisphere
neural activations in the recall of waking fantasies and of dreams. J Sleep Res 2015;24:57682.

40