International Forum of Psychoanalysis
ISSN: 0803-706X (Print) 1651-2324 (Online) Journal homepage: http://www.tandfonline.com/loi/spsy20
Recent advances in sleep physiology of interest to
psychoanalysis
George K. Kostopoulos
To cite this article: George K. Kostopoulos (2012) Recent advances in sleep physiology of
interest to psychoanalysis, International Forum of Psychoanalysis, 21:3-4, 229-238, DOI:
10.1080/0803706X.2012.657674
To link to this article: http://dx.doi.org/10.1080/0803706X.2012.657674
Published online: 05 Mar 2012.
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Date: 01 September 2016, At: 04:42
International Forum of Psychoanalysis. 2012; 21: 229238
ORIGINAL ARTICLE
Recent advances in sleep physiology of interest to psychoanalysis
GEORGE K. KOSTOPOULOS
Abstract
Evidence from recent electroencephalographic and magnetoencephalographic sleep studies is reviewed in relation
to consciousness and dreams, two fundamental issues in psychoanalytic theory and practice. The rich dynamics of
the macro- and microstructure of human sleep indicate specific brain disintegrating mechanisms as underlying the loss
and alteration of consciousness in non-rapid eye movement (NREM) and REM sleep, respectively. Transient state
changes and dynamic interactions between elements of sleep graphoelements (i.e. K-complexes and spindles) are
described; these, beyond their involvement in controlling consciousness level, may support the consolidation or
modification of therapeutic experiences. Higher powers than in awake-state gamma-band electrographic activity
(known to underlie cognitive processes), which we observed in specific medial prefrontal cortical areas, are proposed
to support content in dreaming (REM) and mentation (NREM). These areas lie in remarkably close proximity to
the ‘‘default system’’ and ‘‘theory of mind’’ areas, which may be parts of the neural correlates of intrapsychic
and intersubjective processes. Specific activations of limbic circuits were observed in REM sleep in consistency with
the emotional content of dreams. Current brain imaging technology in sleep studies offers new opportunities to
explore the mechanisms underlying consciousness and dreaming, a unique area of convergence between biology and
psychology.
Key words: sleep, neurophysiology, consciousness, dream, rapid eye movements, electroencephalography, psychoanalysis
Modern neuroscience has opened several new
research paths, which can sustain a fruitful dialogue
with psychoanalysis (Kandel, 2005), starting from
the fundamental path of searching for the neuronal
correlates of consciousness (Koch, 2004) and extending to paths related to intrapsychic processes
and even intersubjectivity. In terms of the latter, one
can mention the research related to the ‘‘default
system’’ (Gusnard & Raichle, 2001), ‘‘theory of
mind’’ processes (Amodio & Frith, 2006), brain
‘‘mirror circuits’’ (Sinigaglia & Rizzolatti, 2011), and
neurodynamics of pair bonding through dissolution
and relearning (Freeman, 1995).
The role of the unconscious and the meaning of
dreams are central issues in psychoanalytic theory
and practice. Recent advances in brain research have
allowed a view of dreaming as the recollection of an
important state of homeostasis characterized by an
altered state of consciousness (Hobson, 2009).
Dreaming therefore offers a rare opportunity of
convergence between biology and psychology.
Here, I will describe some recent findings from our
electrophysiological studies of sleep, focussing on
two converging subjects:
1. the very fast dynamics of losing and regaining
consciousness in sleep, which suggest the possibility that major changes in our state of mind may
allow developments of intersubjective origin to
occur not only during wakefulness but also
when we sleep;
2. brain mechanisms underlying dreaming as they
may pertain to its clinical significance.
Background on the neurophysiology of sleep
Polysomnography has characterized the macrostructure of sleep (Hobson, 2009; Jouvet, 1999; Kandel,
Schwartz, & Jessel, 1991; Steriade & MacCarley,
2005), recognizing during each night several 90minute cycles consisting of successive rapid eye
movement (REM) and non-REM (NREM) periods
of sleep (Figure 1). This macrostructure is qualitatively conserved in mammalian phylogeny. Early
Correspondence: George K. Kostopoulos MD, PhD, Department of Physiology, Medical School, University of Patras 26500 Patras, Greece. Tel: 30 2610
969157, 30 2610 969155. Fax: 30 _2610 997215. E-mail: [email protected]
(Received 20 September 2011; accepted 9 January 2012)
ISSN 0803-706X print/ISSN 1651-2324 online # 2012 The International Federation of Psychoanalytic Societies
http://dx.doi.org/10.1080/0803706X.2012.657674
230
G. K. Kostopoulos
Figure 1. Desynchronizing microarousals (MA). Hypnogram (AW, awake; REM, rapid-eye movement sleep; SISIV, non-REM sleep
stages 14) with 1 s resolution, which allows the detection of all MAs per night; the time-compressed display is misleading in terms of their
duration, which does not in fact exceed a few seconds. The first MA is marked by an arrow. Modified from Kokkinos and Kostopoulos
(2011), with the permission of the publisher.
sleep cycles have longer NREM periods, and as we
approach morning, the percentage of REM sleep
increases. Total sleep time and the percentage of
REM sleep decrease with age.
Sleep onset results from a combination of
hypothalamic diurnal (i.e. ‘‘clock genes’’ in the
suprachiasmatic nucleus) and homeostatic (e.g.
adenosine) factors, which inhibit specific arousing
and REM/NREM cycle-controlling centers in the
diencephalon and brainstem. The latter provide with
forebrain with diffuse neuromodulation from
monoamines (such as norepinephrine, serotonin,
and dopamine) and acetylcholine. Compared with
the awake state, the NREM brain is devoid of all
neuromodulation and shows decreased metabolic
and electrophysiological activity, whereas in REM
sleep the brain is modulated by acetylcholine and
is very active. This activation, reflected in a desynchronized electroencephalographic (EEG) trace, can
be contrasted with maximal muscle atonia, which led
to REM sleep being termed ‘‘paradoxical.’’ William
Dement succinctly summarized the above by
characterizing NREM as an idle brain in a movable
body, whereas REM is an active hallucinating brain
in a paralyzed body. Finally, the sensory gates to the
cortex are closed during sleep.
In parallel to sleep, a host of important autonomic,
endocrine, and immune functions are rhythmically
regulated, so the reciprocal interactions that occur
between sleep and the body’s homeostatic mechanisms cannot be overemphasized. Total sleep or
specific REM and NREM sleep deprivation leads
to severe physical and mental health problems. As
we fall asleep, we lose access to sensory input, and
our brain starts to process internally generated
information. Normal sleep always starts with a
NREM phase, and in the next three successive
stages (1, 2, and 34) we gradually lose consciousness, which is regained, albeit in a deranged manner,
in REM sleep.
Recent functional magnetic resonance imaging
and positron-emission tomography studies during
REM sleep have revealed in specific areas activations
(associational sensory cortices, amygdala, parahippocampal cortex, parietal operculum, anterior cingulate, pontine tegmentum, and deep frontal white
matter) and deactivations (primary sensory cortices,
dorsolateral prefrontal cortex, and posterior cingulate), which are consistent with the phenomenology
and provide some clues to the mechanisms underlying the characteristics of dreams. In patients who
have had a stroke or frontal lobotomy, lesions in
two of the activated zones the parietal operculum
and the deep frontal white matter lead to a
cessation of dream reports (Solms, 2011).
According to the psychoanalytic theory, the dream
we remember in the morning is a disguised,
scrambled expression of our unconscious repressed
wishes. The drive is fulfilled, but in such a way that the
psyche and sleep are protected. The dream we
remember in the morning, the ‘‘manifest content,’’
derives in a symbolic code from a ‘‘latent content,’’
that is, the underlying thoughts, urges, conflicts, and
needs. Decoding this derivation may uncover the true
meaning of the dream, which will offer therapeutic
opportunities for the patient, thus justifying the
dream as the ‘‘royal road’’ to the unconscious.
Dreams are less puzzling now than they were
before the 1953 discovery of REM sleep, when we
used to think that the mind was idling in sleep and
that dreaming was a rare and therefore significant
event. The brain is active and fosters the electrochemical events underlying several different dreams
every night (conservatively calculated as more than
150,000 per lifetime). Rodolfo Llinas (2001) even
considers dreams to be our basic state, except that
attention is directed internally and organizes our
memories.
Dreams appear throughout sleep, but with important qualitative and quantitative differences:
dreams occurring during REM sleep are much
more frequent, more vivid, full of delusions, and
often bizarrely reminiscent of psychotic delirium.
They contain much movement, but we do not act
Sleep physiology and psychoanalysis
our dreams due to active hyperpolarization of the
motoneurons, especially in REM sleep. Due to a lack
of noradrenaline and serotonin, as well as the
deactivation of the dorsolateral prefrontal cortex,
regions known to support working memory and
time-counting, the brain cannot focus on problemsolving, organize analytical thought or remember its
dreams unless the person is woken up during a
dream, and then it occurs only in a confabulatory way.
It is important to realize that all our knowledge of
dream content is based on subjective reports, which
are a function of Broca’s and other brain language
areas that are activated upon awakening. Neurology
has long provided ample evidence of the arbitrary
interpreting and story-making tendency of our left
brain in an effort to make sense, often very unreliably, of its activations. Given this rationalizing
power of our mind (the ‘‘interpreter’’ described by
Gazzaniga and by Reuter-Lorenz, Bayes, Mangun, &
Phelps, 2010), that amnesia the occurs during sleep,
and the confabulation upon awakening, one seriously doubts the validity of dream reports. In view
of the recent progress in sleep neuroscience, many
believe that the nature and role of dreams cannot be
revealed except in the frame of a scientific study of
sleep why we sleep and which brain mechanisms
cause it.
As for the first, sleep certainly provided an
evolutionary advantage in terms of energy conservation and ecological adaptation, allowing a diurnal
replenishment of the important cellular constituents
of macromolecular biosynthesis. In particular, REM
sleep is biologically adaptive, as evidenced by its
presence in all mammals, its predominance in the
early developing years of life, and its rebound after
REM sleep-specific deprivation. Of most relevance
to psychology, memory consolidation depends heavily on an overnight rehearsal and on discrete brain
synaptic plasticity mechanisms operating in both
REM and NREM sleep, most notably on a dialogue
between the hippocampus, where the day’s experiences are coded, and the frontal cortex, which is
needed for their long-term storage. Sleep spindles
play a pivotal role in this dialogue and have been
shown to cause long-term potentiation in cortical
neurons (Diekelmann & Born 2010; O’Neill, Pleydell-Bouverie, Dupret, & Csicsvari, 2010; Siapas &
Wilson 1998; Steriade & McCarley, 2005’).
The dynamics of losing and regaining
consciousness in sleep
With regard to sleep mechanisms, these are obviously related to the neural correlates of consciousness (Crick & Koch, 1990). In deep NREM sleep,
we lose both primary consciousness (i.e. general
231
awareness, including perception and emotion) and
secondary or subjective consciousness, or the
awareness of awareness, which depends on language
and so is enriched by abstract analysis (thinking) and
the metacognitive components of consciousness
(self-reflection, or awareness of awareness) as well
as volition. In dreaming, the primary consciousness
of sleep is regained but lacks volition and reflection
on self and on reality.
It may take a long time before we can understand
the unconscious, in the way it is meant in psychoanalysis, but a productive start in this direction can
be made, first, by examining the brain mechanisms
by which we lose consciousness, and second, by
adopting those definitions of consciousness which
may lead us to feasible experiments using current
technology. Most simply put by Gerald Edelman
(2006), ‘‘Consciousness is what you lose on entering
a dreamless deep sleep.’’ I believe the definition that
is most promising in helping us find what we lose is
‘‘Consciousness is information integrated’’ (Tononi,
2010). Has our sleeping brain lost its dynamic
complexity or its capacity to integrate the enormously diverse patterns of its activity into a unique
consciously perceived whole?
The awake brain is very rich in information. It
contains an enormous number of independent
circuits, interacting in a very complex way, which mostly thanks to the thalamocortical re-entrant
loops can be transiently integrated in a functional
unit. All recently advanced hypotheses about the
mechanisms underlying consciousness include some
role for the thalamocortical system (Kostopoulos,
2001) Thus, when we lose consciousness, we probably lose some important function of the thalamocortical system, as most evidently shown in
experimental studies on mechanisms underlying
the loss of consciousness in sleep and in certain
types of epilepsy. What is then lost differentiation
or integration?
During the whole of sleep, and especially in the
second stage of NREM sleep, a dynamic confrontation of arousing and antiarousing mechanisms is
evident in the macro- and microstructure of the
EEG. Loss and regaining of consciousness is continuously debated by tens of microarousals each
night, which are normally too short to fully awaken
us. Microarousals are characterized by either EEG
desynchronization or EEG synchronization (Halasz,
1998). Figure 1 shows an example of all the
desynchronizing microarousals of a subject’s sleep.
On average, we counted 3199 desynchronizing
microarousals per night, distributed mostly in
REM and stage 2 NREM sleep (Kokkinos &
Kostopoulos, 2011; Kokkinos, Koupparis, Stavrinou, & Kostopoulos, 2009).
232
G. K. Kostopoulos
The definitive step in losing consciousness is
accomplished during the first episode of NREM
stage 2 characterized by spindles and K-complexes.
How does this happen? Spindles have been shown to
result from a hyperpolarization-induced rhythmical
firing of the thalamocortical neurons, which is
reinforced by corticothalamic excitation and spread
by cortico-cortical excitation. Because of the hyperpolarization of thalamocortical neurons during the
spindles, the thalamic gates to the cortex are closed.
K-complexes, generated in the cortex, constitute a
hypnogenic response to arousal stimuli. The large
negative wave is paralleled by a ‘‘down-state’’
(inactivity) of the cortical neurons.
To investigate this dynamic role of K-complexes
and spindles, we examined their relationship and
found that sporadically observed fast spindles
(1315 Hz) were invariably interrupted by any
concurrently occurring K-complex and usually replaced by a short rhythm of about 8.2 Hz (Figure 2;
Kokkinos & Kostopoulos, 2011). K-complexes are
then usually followed within 1 second by spindles.
These are invariably faster by about 1 Hz than the
sporadic fast spindles or the spindles interrupted by
K-complexes. A paucity of spindles then follows for
many seconds. In spite of their robust relationship,
the association of spindles to K-complexes is not
causal. Both are rather caused independently by
brainstem afferents to the thalamus and cortex
following a stimulus that is not strong enough to
cause arousal. What this dynamic relationship may
accomplish are the following:
1. A dynamic window of information-processing is
opened, allowing some monitoring of possible
threats.
2. If the stimuli represent a lack of threat, sleep is
maintained or protected.
3. The spindles’ role in learning (they have been
shown to cause long-term potentiation in cortical neurons) may be enhanced when they
follow a K-complex.
Studying the sleep periods devoid of the stagespecific graphic elements (K-complexes, delta waves,
REM, etc.), magnetoencephalogram (MEG) derived
magnetic field tomography (MFT; Ioannides 1994)
reveals distributed patterns of cortical and subcortical brain activations and deactivations of high and
low frequency on a millimeter and microsecond
scale. These can, by themselves, distinguish the
sleep stages (REM and NREM 14) and, in line
with the much slower metabolic studies (Dang-Vu,
Schabus, Desseilles, Sterpenich, Bonjean, & Maquet, 2010), provide clues to the mechanisms
underlying sleep and the phenomenology of dreaming. Brain activity during both NREM and REM
sleep is observed to be greatly differentiated in space
and time. Some specific areas (expanded on later)
have higher gamma-band activations even than in
the awake state. So, the brain in sleep is still rich in
information content and in complexity. Loss of consciousness may therefore be ascribed to a loss of integrating
ability, and this can in turn be attributed to (1) a loss
of brain connectivity during NREM (shown with
transcranial magnetic stimulation; Massimini, Boly,
Casali, Rosanova, & Tononi, 2009), (2) a closing of
the thalamic gates to all senses, and (3) the bistability
of cortical neurons between extreme ‘‘up’’ and
‘‘down’’ states (Steriade & MacCarley, 2005).
Despite the fact that we experience the diminution
of consciousness as a gradual process when we fall
asleep, it actually has very fast dynamics throughout the
night, and for a good reason: lack of monitoring the
environment coupled with muscular atonia is a very
precarious state for an animal to be in. Dynamic
state shifts have already been demonstrated in the
awake state, probably as a result of unconscious
processes that are continuously operating in the
background, for example preparing the words for
our speech, making decisions based on somatic
memories, or bringing to the foreground long-held
memories linked to a particular smell. These are the
unconscious processes that operate all our implicit,
nondeclarative, or procedural learning, and which
Eric Kandel (2005) proposed map onto the ‘‘nonrepressed ego’’ of Freud, apparently working as
transient instigators of our conscious behavior.
Experimental evidence has attributed the roles of
specific types of such unconsciously mobilized
memories to specific brain areas skills and habits
to the striatum, priming to the cerebral cortex,
classically conditioned emotional responses to the
amygdala, and so on (Kandel et al., 1991). Recent
studies have tried to decipher the stages of sleep
most involved in this procedural (motor) learning
(Diekelmann & Born, 2010; Stavrinou, Kolia,
Koupparis, Athanasopoulou, Damaskos, & Kostopoulos, 2011). It seems that the dynamics of
interfacing consciousness with these unconscious
processes may create fleeting moments of inspiration
or revelation, of extending our intrapsychic dimensions. They may also allow the ‘‘unlearning and new
bonding’’ (Freeman, 1995) that may be related to
the ‘‘moments of intersubjective meeting’’ of psychoanalysis. It is logical to assume that these result from
transient but dramatic changes in brain processes
underlying consciousness. One therefore wonders
whether such dramatic changes also occur in sleep in
relation to dream content.
Sleep physiology and psychoanalysis
233
Figure 2. The K-complex, a synchronizing microarousal-related slow EEG wave characterizing nonrapid eye movement stage II sleep. (A)
Waveform superposition and average (white line trace) of 195 K-complexes from a subject’s whole night’s sleep. (B) Topographical sketches
of the averaged negative (blue vertical line at time zero in (A)) and positive (red vertical line in (A)) peaks of the K-complex. (C) The
averaged timefrequency plot of the power of the K-complexes derived from the Fz electrode. Note the dynamics: during the approximately
0.5 s duration of the K-complex, the sporadically appearing spindles are interrupted, replaced by a theta-frequency short oscillation and
then repeated (in all cases) at a higher frequency. Modified from Kokkinos and Kostopoulos (2011), with the permission of the publisher.
234
G. K. Kostopoulos
REM sleep research and the significance of
dream content
The discovery of REM sleep six decades ago was
heralded as the ‘‘start of an objective study of
dreaming’’ (see Jouvet, 1999). We may know today
that REM and dreams cannot be equated since
under certain conditions they can exist independently of each other. Even so, REM sleep, with
its accompanying characteristics (atonia, metabolic
activation, cholinergic modulation, and EEG
desynchronization) indicates the time at which the
most vivid and bizarre dreams can most often be
reported. (We report dreaming when awoken
from both REM and NREM sleep, but the statistics
favor REM sleep by 4:1.) Thus, REM sleep is the
most helpful surrogate marker we can use in
searching the nature of this most covert cognitive
event.
The Freudian view of the clinically useful nature
of dreams (Freud, 1900) has been recently enriched
with neuroscientific observations ascribing importance to the role of the dopaminergic ‘‘appetitive’’
system of the brain (Solms, 2011). The role of
dreams for psychoanalysts is to preserve sleep in the
face of unconscious needs for excitement. Conversely, the activationsynthesis hypothesis (Hobson,
2009) considers dreams to be a subjective report
of our thoughts, an epiphenomenon of brain activation during the whole of sleep, but mostly correlated
to REM sleep resulting from the brain’s high
activation, solely internal input, and solely cholinergic modulation. Dreams may provide a virtual reality
model (protoconsciousness) in preparation for
integrative functions, including learning and secondary consciousness. The obvious connection to
development has been emphasized by the genetic
reprogramming hypothesis (Jouvet, 1999) and the
functional state-shift hypothesis (recall of childhood
memories; Koukkou & Lehmann, 1983). The neurocognitive school of thought (see Nir & Tononi,
2010) sees dreaming as producing simulations of the
world by actively drawing on memory schemas,
general knowledge, and episodic information. In
this view dreams have no function, being a spandrel
of the mind, a by-product of the evolution of sleep
and consciousness.
What triggers dreams, and do specific brain
areas sustain their neural correlates?
A question on the origin of dreams pertains to both
the nature of dreams and their usefulness in psychoanalytic practice. Psychoanalysis proposes that
dreams originate from psychic motives that are later
instantiated as sensory percepts. As an alternative to
this top-down hypothesis, a bottom-up theory has
been proposed according to which the brainstem
activates the sensory cortices and the synthesis of
their responses is interpreted as dreaming (see
Hobson, 2009; Nir & Tononi, 2010; Solms, 2011).
Accepting the latter view may cast doubts on the
significance of dreams as a reliable tool in therapy.
REM episodes do not trigger dreams. However,
they mark their occurrence in time with good
approximation, so it might be revealing to learn the
brain activity responsible for REMs. In the awake
condition, our saccades are primarily driven by
activity in the bilateral frontal eye fields. MFTderived images and connectivity studies during sleep
have revealed rich interactivity leading to or following the onset of REM episodes, with similarities as
well as important differences compared with waking
saccades (Figure 3; Ioannides, Corsi-Cabrera, Fenwick, del Rio Portilla, Laskaris, & Khurshudyan,
2004). Using mutual information analysis of the
timing of activation of the brain’s current sources in
sleep, we identified an orbitofrontal-amygdalo-parahippocampal-pontine sequence of activity about 100
msec leading to the REM episodes. This sequence
testifies to the emotional activation during REM
sleep, but it is not solely responsible for the initiation
of REM sequences, which appears to depend on a
recurrent (approximately 4 Hz) slow build-up of
activity in the pontine nuclei in continuous dialogue
with the frontal eye field.
An experimentally tangible question, then, is:
which areas of the brain show electrophysiological
activity suggesting that they could sustain cognition
during sleep? In our MEG sleep studies of electrographically core (tonic) periods throughout the night
(Figure 4; Ioannides, Kostopoulos, Liu, & Fenwick,
2009), we observed the following as sleep progressed:
1. There was a stage-dependent differentiation in
both slow and gamma-band activation as well as
inactivations with NREM stages 14. It should
be noted that gamma-band activations (25
Hz) are indicative of cognition (see Gross &
Gotman, 1999).
2. A progressive increase in gamma power was
seen along the dorsal areas close to the midline
that was greater than during the active, awake
state.
3. Gamma activation increased first in the precuneus during NREM stages 1 and 2, and then
in the left dorsomedial prefrontal cortex
(DMPFC) in NREM stages 3 and 4, which
was the most prominent, expanding laterally in
the left hemisphere in REM sleep.
Sleep physiology and psychoanalysis
235
Figure 3. (A) Grand statistical parametric maps for leftward eye movements during rapid eye movement (REM) sleep. The loci of
common changes are identified after the data from each subject have been transformed into the Talairach space. The common loci for the
three subjects are displayed after back-transforming the results and projecting them onto the magnetic resonance imaging (MRI) scan of
one subject (red, increase; the time interval and the threshold p-value are printed inside each panel). Sagittal MRI slices for activity leading
to the onset of a saccade (the contrast is REMs to the left versus the awake status using 12 ms windows). A sequence is shown of a relative
increase in right hemisphere activity in REMs beginning in the orbitofrontal cortex and amygdala (left), followed by activity in the
parahippocampal gyrus (middle), and finally activity in the eye-moving pontine nuclei (right). Modified from Ioannides et al. (2004), with
the permission of the publisher. (B) Hypothetical diagram to explain the multiple factors controlling the start of an eye movement. The
slow (about 4 Hz) spontaneous activity of the pontine nuclei is affected during awake saccades by descending inputs deriving from the
frontal eye fields. In REM sleep, influences from limbic structures acquire major importance, partly because of their release from the
inhibition exerted on them by the dorsolateral prefrontal cortex (DLPFC), which is deactivated in REM sleep. EOG, xxxx; OFC,
orbitofrontal cortex.
4. Both increases appeared specifically in the
middle of areas where delta waves had already
maximally developed.
5. In REM sleep, gamma-band activity was seen
prominently in the left DMPFC.
6. The motor cortex was spared from slow activity
during all NREM sleep stages.
7. Low gamma activation occurred in the hypothalamus, brainstem, and cerebellum.
8. NREM stage 1 sleep was similar to REM sleep
in having decreased gamma activity in the
brainstem and posterior areas.
9. Several other cortical and subcortical changes in
gamma activation were found to characterize
different sleep stages.
When trying to interpret these highly localized
findings in relation to psychoanalysis, one is
reminded of the two, possibly related, systems that
have been recently proposed to account for mental
operations that either take place during rest or
relate to introspection. The default system is a network of areas that show a reduction in activity during
externally directed attention, but an increase under
baseline conditions (Gusnard & Raichle, 2001). The
theory of mind (ToM) network provides the substrate
for how humans conceive others as intentional
agents and assess self-knowledge (Amodio & Frith,
2006). Some of the most prominent areas of
the default and ToM systems are located along
the dorsal medial brain and include the DMPFC
and, parietally, the cuneus and precuneus. These
locations and the ways in which dream characteristics behaved encouraged speculation that the
ToM system was involved in dreaming (Maquet
et al., 2005).
236
G. K. Kostopoulos
Figure 4. Statistical parametric maps contrasting the awake condition with nonrapid eye movement (NREM) stages 14 and REM sleep.
Three views: from the top, axial (A, B), mid-sagittal (C, D), and coronal (E, F). The levels of other cuts are marked by dotted white lines on
the first slice of rows A, C, and E. The left and right central sulci are highlighted in green. (A, C, E) Wide-band activity. (B, D, F) Gammaband activity. A red fill with a yellow outline marks common across-subjects increases in activity during sleep at p B 0.005, and those with a
white outline increases at p B 0.00001. Decreases are shown as a blue fill with dashed pink outline for p B 0.005, or with a white dotted
outline for p B 0.00001. To avoid clutter, the higher statistical significance contours (p B 0.00001) are shown for all REM cases, but for the
rest only for the axial and the dorsal aspect of the sagittal slices. White stars in the NREM4 and REM columns of (D) mark where the
yellow contour was in NREM2. From Ioannides et al. (2009), with the permission of the publisher.
Every night, we display two kinds of cognitive
activity: vivid and delirium-like dreams during REM
sleep, and more linear mentation during NREM
sleep. We found (Ioannides et al., 2009) that: (1) in
the left DMPFC, there was higher gamma activity
during REM sleep than in the awake state even
during a face affect recognition test; and (2) the left
DMPFC tonic REM area was found (after metaanalysis and plotting these data from the literature)
to be surrounded by the ‘‘ToM’’ and ‘‘default
system’’ areas. It can therefore be suggested that
the left DMPFC and precuneus may be the hub of
dreaming processes during REM sleep. In the same
study (Ioannides et al., 2009; see Figure 4), we also
found that gamma-band activity in NREM stage
4 sleep was higher than in REM sleep for both the
entire ventromedial prefrontal cortex and the parietal occipital temporal region (see Solms, 2011).
These activations could therefore allow for some
mentation during NREM sleep. Activation in dorsal
and ventral parts of medial prefrontal cortex may
thus be important for the mentation typical of REM
and NREM sleep, respectively.
Conclusion
The first conclusion we can draw is that MEG
studies show rich space-and-time differentiation of
brain activity during different sleep stages. EEG
studies show a diversity of very fast processes
protecting sleep (the dynamic interaction of
K-complexes and spindles) and an enormous
Sleep physiology and psychoanalysis
number of short-lasting microarousals from all
stages of sleep. It is concluded that the brain in
sleep is still rich in information content and complexity, and therefore consciousness is rather lost in
NREM because of defective integration, probably due
to a loss of brain connectivity.
Next, consciousness is continuously negotiated, with
the brain apparently monitoring and evaluating the
saliency and threat posed by internal homeostatic
and external stimuli. Desynchronizing microarousals
constitute brief but very dynamic windows of
information-processing that are apparently caused
by dramatic changes in global brain chemical modulation. Synchronizing microarousals may enhance
the role of spindles in consolidating the past day’s
experiences. Sleep appears to offer opportunities for
global cognitive changes, effectively changing brain
function in a way possibly analogous to ‘‘moments of
meaning’’ or ‘‘moments of meeting’’ during wakefulness, and/or for consolidating such therapy-related
events from the preceding day.
Dreaming evades the ‘‘top-down’’ and ‘‘bottomup’’ dichotomy. The debates on whether dreaming
originates from brainstem or higher forebrain areas,
thus respectively representing regular body needs or
specific mental functions (and ‘‘unfulfilled
wishes’’?), seem to be gross oversimplifications of a
very complex state of dynamic interactivity of areas
across the entire brain and body aiming at several
important functions. Meaningless ‘‘homeostatic’’
triggers of dreams may not come only from the
brainstem: they may also be the result of synaptic
homeostasis at the cortical level. Our demonstration
of limbic system activity anticipating REM episodes
may be an indication that dreams during REM sleep
may be triggered by such limbic activations, which is
consistent with the emotional content of many
dreams.
In addition, we forget our dreams (unless we are
awakened during them) because of aminergic demodulation and deactivation of the lateral prefrontal
cortex. Conversely, sleep and possibly dreaming are
involved in consolidation of the day’s experiences
into memory. Could this fact affect dream analysis
theory? Could a sound sleep be necessary for
consolidating in memory any psychic changes
achieved by psychotherapy the day before?
Where do our dreams reside? A brain area most
capable of sustaining cognitive activity during sleep and therefore dreaming or sleep mentation has
been found. The location of the left DMPFC tonic
REM area as a distinct center of the medial
prefrontal cortex surrounded by ToM areas, and
not far from the default system regions, makes it a
candidate as the hub of dreaming. Our demonstration of a continuous growth in this localized activity
237
from the awake state to NREM stages 1, 2, 3, and 4,
and then to REM sleep makes it also a candidate for
a network supporting the continuity of self-identity
during both sleeping and waking.
Dreaming in REM sleep seems to be supported
mostly by activity in the left DMPFC. Mentation in
NREM sleep may be related to ‘‘‘covert’’’ REM
processes that occur locally, especially in the left
DMPFC (higher gamma activity being seen in
NREM stage 4 sleep than during wakefulness), but
also in the ventral medial prefrontal cortex and the
parieto-temporal-occipital area (which shows greater
gamma activation in NREM than REM sleep).
Finally, using scanning techniques that assess
brain activity, scientists have determined which areas
of the brain are active or inactive during dreaming.
This, along with demonstrations of electrophysiological interactivity, suggest that modern technology
can address the scientific challenges of human sleep
mechanisms and their role in mental functions.
One should of course bear in mind the huge knowledge gap existing between the ‘‘language’’ of neurons
and the symbolic language we use to think about and
report our dreams. Technology is, however, ripe for
facing this challenge, first by studying the mechanisms underlying consciousness and dreaming,
combining psychological, metabolic and electrophysiological imaging, and second by moving away from
the stages of sleep towards sleep’s microstructure
with respect to both the temporal and spatial
correlates of brain function.
Epilogue
Psychoanalysts have certainly been using dream
reports to the benefit of their patients independent
of knowing the brain mechanisms that support them.
I believe, however, that a better knowledge of such
mechanisms is forthcoming thanks to advancements
in noninvasive brain imaging and the recent kindling
of interest in the crossroads of psychoanalysis and
neuroscience. Progress has been made with respect
to unconscious memory functions, whose relation to
dreaming is crucial but largely unknown. Technology is ripe to at least provide surrogate markers for
dream phenomenology and some knowledge, which
may not be yet explanatory but could help to
advance constraints and qualifiers for the use of
dreams in psychoanalysis. Such knowledge will,
I believe, make dreams a real road to the unconscious
in a more objective way, subject to crossfertilization
among the different analysis schools and therefore
providing a wider road that will eventually be
available to all and not only to royalty travelling the
‘‘royal road.’’
238
G. K. Kostopoulos
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Author
George K. Kostopoulos, MD (Athens, 1972), PhD
(Saskatchewan, Canada, 1977), has taught at McGill
University, Canada (19781982, 19861987), and
is currently professor and chairman of physiology
at the Medical School, University of Patras, Greece.
He is an experimental neurophysiologist with
training at the neuronal level as well as in EEGs.
His current research focusses on the physiology of
sleep (http://physiology.med.upatras.gr/NU).