ISSN 03621197, Human Physiology, 2013, Vol. 39, No. 6, pp. 590–601. © Pleiades Publishing, Inc., 2013.

Original Russian Text © I.N. Pigarev, M.L. Pigareva, 2013, published in Fiziologiya Cheloveka, 2013, Vol. 39, No. 6, pp. 31–44.

Sleep, Emotions, and Visceral Control

I. N. Pigareva and M. L. Pigarevab
a
Institute for Information Transmission Problems (Kharkevich Institute), Russian Academy of Sciences,
Moscow, 127994 Russia
b Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences, Moscow, 117485 Russia

Received April 8, 2013

Abstract—It is known that sleep is connected with sensory isolation of the brain, inactivation of the con
sciousness and reorganization of the electrical activity in all cerebral cortical areas. On the other hand, sleep
deprivation leads to pathology in visceral organs and finally to the death of animals, while there are no obvious
changes in the brain itself. It is still unclear how the changes in the brain activity during sleep could be con
nected with the visceral health. We assumed that the same brain areas and the same neurons that, in wakeful
ness, process exteroceptive information, switch, during sleep, to the processing of the interoceptive informa
tion. Thus, the central nervous system is involved in regulating the life support functions of the body during
sleep. The results of our experiments supported this hypothesis, explained many observations obtained in
somnology, and offered mechanisms of several pathological states connected with sleep. However, at the
present level of the visceral sleep theory, there is no understanding of the wellknown link between the emo
tional reactions of the body and transition from wakefulness to sleep, and sleep quality. In this study, an
attempt is undertaken to combine the visceral theory of sleep with the needinformational theory of emotions
proposed by P. Simonov. The visceral theory of sleep assumes that in living organisms there is a constant mon
itoring of the correspondence of the visceral parameters to the genetically determined values. Mismatch sig
nals evoke the feeling of tiredness and the need of sleep. This sleep need enters the competition with other
actual needs of the body. In accordance with the theory of Simonov, emotions connected with a particular
need play an important role in their ranking for satisfaction. We propose that emotional estimation of the
sleep need based on visceral signals occurs in the same brain structures which undertake this estimation for
other behavioral needs in wakefulness. During sleep, the same brain structures involved in estimating emo
tions continue to rank visceral needs and define their order for processing in the cortical areas and in the high
est centers of visceral integration. In the context of the proposed hypothesis, we discuss the results of the stud
ies on the link between sleep and emotions.

Keywords: visceral theory of sleep, needinformational theory of emotion, visceral control

DOI: 10.1134/S036211971306008X

1. INTRODUCTION: THE MAIN PARADOX
OF THE SLEEP STATE
There is probably no other sphere of physiological
science where the word “paradoxical” is mentioned as
frequently as in sleep physiology. Everyone has heard
about the paradoxical sleep phase and legends around
this state of the body. However, in our opinion, the
most paradoxical sleep phenomenon is that, despite
numerous studies in the last century, there is still no
generally acknowledged theory capable of explaining
the functional purpose of this state. As for the diffi
culty of developing such a theory, it is obviously con
nected with the main sleep paradox, which consists of
the contradictions among the following phenomena
that, at first glance, are difficult to combine.
Transition from wakefulness to sleep is connected
with pronounced changes in the electrical activity of
the brain, first of all, of the cerebral cortex. In the peri
ods of slowwave sleep, cortical neurons pass to peri
odical burst activity reflected in the slow waves of
EEG. Both humans and animals choose, for sleep,
quiet and dark places with a soft bedding to decrease
the level of activation of proprio and extero(distant)
receptors. In addition special neuronal mechanisms
raise the thresholds for sensory information on its way
to the cortex [1, 2]. All this makes an impression of the
informational isolation of the brain during sleep. At
this time, cortical output motor commands are also
blocked (socalled sleep atonia) [3]. In combination
with bright images of dreams, these observations led
to conclusion that sleep is a state needed, first of all,
to support the brain’s efficient functioning. Reviews
of these studies are presented in several publications
[4–6].
On the other hand, the most direct and logical
method of clarifying the functional role of sleep would
be the analysis of the consequences of temporal exclu
sion of sleep from animal life (sleep deprivation). For
the first time such experiments were performed on
dogs in the 1930s in the laboratory headed by K. Bykov

590
 SLEEP, EMOTIONS, AND VISCERAL CONTROL
[7]. Then, a large cycle of studies performed on rats
confirmed that sleep deprivation during several days
leads to numerous disturbances in the visceral sphere,
and finally to the death of experimental animals [8].
Recently, a great number of studies showing visceral
disorders, first of all, of the gastrointestinal tract,
related to disturbances of normal sleep in humans have
been accumulated [9].
A striking finding was that, in rats, the only organ
that did not suffer from sleep deprivation was the brain
[10]. This observation was frequently doubted, since it
is well known that sleep deprivation in humans is
accompanied by a decrease in attention and ability to
solve complex tasks [11]. This apparent contradiction
was solved by the discovery of the local sleep phenom
enon [12, 13]. It was shown that in some cases sleep
development in some cortical zones can take place
during behavioral wakefulness. Thus, it was natural to
explain the cognitive consequences of sleep depriva
tion by turning off of several cortical zones rather than
by the deterioration of brain efficiency.
It remained a puzzle how the informational isola
tion of the brain from the external world, which
accompanies the transition from wakefulness to sleep,
could be connected with visceral health.
Attempting to find a solution to this issue, we
advanced a rather simple hypothesis. According to this
hypothesis, during sleep, the brain is actually isolated
from exteroreceptive information. However, the same
brain neurons that, in periods of wakefulness, analyze
exteroreceptive information of different modality
switch over to the analysis of interoreceptive informa
tion coming from different visceral systems. Thus, the
central nervous system during sleep is involved in the
process of visceral regulation.
Despite the attractiveness of this approach, the
main obstacle—the generally recognized concept that
cerebral cortex is a system of specialized processors
tuned to the analysis of signals of definite sensory
modality—was in its way. This concept reflected itself
also in the adopted nomenclature of cortical zones,
such as visual, auditory, and somatosensory zones.
However, one should remember that during the cre
ation of computers, the development of specialized
processors was very soon given up, and all modern
machines are based precisely on universal processors.
There is no doubt that the construction of computers
created by human is far simpler than the organization
of the most powerful devices of information process
ing known to us, namely, an animal’s brain. It is diffi
cult to imagine that the principles of universal proces
sors were not used in the process of creating a living
brain. This consideration urged us to conduct a series
of experiments to check nontrivial predictions of the
visceral sleep hypothesis.
The results of experiments that would never have
been made in the absence of this hypothesis confirmed
this proposal [14–18]. A detailed review of these stud
ies, whose results allowed us to speak about the visceral
HUMAN PHYSIOLOGY Vol. 39 No. 6 2013
591
sleep theory, has been recently published [19]. In
terms of the suggested theory, many observations of
experimental somnology were explained, and the
mechanisms of a number of pathologies related to the
sleep state became clear.
However, there remained phenomena that did not
find explanation at the level of the development of the
visceral sleep theory. There were numerous indications
of the connection of the sleep state with the emotional
reactions of the body. To a certain extent, all of them
concerned the mechanism of transition from wakeful
ness to sleep. The negative effects of acute emotional
sensations on the quality of subsequent sleep and shifts
to the negative side of the emotional background after
sleep deprivation were described. We consider the
results of these analyses in detail below, in the con
cluding section.
In this study, we searched for a logical connection
between mechanisms of sleep triggering, control of
visceral systems, and mechanisms of the formation of
emotional reactions. The visceral sleep theory opened
an approach to understanding the relation between the
sleep state and the working of the visceral systems of
the body. In the sphere of the physiology of emotions,
the needinformational theory of emotions elaborated
by P. Simonov and his coworkers remains the most
developed [20, 21]. Both discussed approaches are
based on the analysis of information flows in the ner
vous system. Although, at first glance, these theories
concerned different issues of physiological activity, we
tried to bring these two directions together.
In the second section of this paper, we shall con
sider the main elements of the visceral sleep theory
and present the picture of changes of the main infor
mation flows in the nervous system in the sleepwake
fulness cycle suggested by this theory.
In the third section, we shall try to combine Simo
nov’s propositions of the needinformational theory of
emotions with concepts of neurophysiological mecha
nisms and the functional purpose of this state emerg
ing from the visceral theory.
Finally, in the fourth section, we shall briefly review
the papers on the relation between sleep and emo
tional states and discuss these results in the approach
suggested by us.
2. ASSUMPTIONS OF THE VISCERAL
SLEEP THEORY
The visceral sleep theory is based on the suggestion
that the same cortical zones and the same neurons that
in wakefulness analyze signals from exteroreceptors in
the state of sleep switch over to the analysis of interore
ceptive information. To test this hypothesis, responses
of different cerebral cortical regions to extero and
interoceptive stimulation in sleep and in wakefulness
were compared. It was shown that neurons of the
visual and somatosensory cortex of cats that in wake
fulness responded to visual and somatic stimulation in
592 PIGAREV, PIGAREVA
slow wave sleep began to respond to the electrical
stimulation of the intestine and stomach. These vis
ceral responses stopped in REM sleep and at awaken
ing [14]. Similar results were obtained on monkeys
[15, 16] and rabbits [17].
Further comparison of the natural myoelectrical
activity of the digestive organs with cortical activity dur
ing sleep showed that appearances in the EEG of the cor
tex of short desynchronizations in the periods of slow
wave sleep coincide with the appearance of migrating
myoelectric complexes in the stomach activity [19].
Analysis of spike activity in the cortical visual areas
of cats revealed in 30% of neurons in slow wave sleep
changes in the spike frequency determined by the
rhythmicity of the myoelectric activity of the duode
num and stomach. Such a relation never manifested
itself in wakefulness [22]. Finally, it was found that the
change in the composition of the intragastric medium
performed in the period of slow wave sleep (water infu
sion via fistula into the stomach) leads to changes in
the EEG pattern and activity of single neurons in the
brain cortex [18].
Note that the relationship of the organs of the
digestive system and the cortex was activated in peri
ods of slow wave sleep and stopped in REM sleep.
Nevertheless, the visceral sleep theory does not regard
slow wave and REM sleep as two essentially different
states. We assume that in both slow and REM sleep,
the brain is involved in processing of the visceral infor
mation and that during a complete sleep cycle, the
successive scanning of all life supporting systems of the
body takes place. Usually this process begins in the
organs of digestion, respiration, and heart, which have
a distinct rhythmicity. The interference of their activ
ity synchronizing during slow wave sleep determines
the waves of cortical EEG. The scanning then passes
to organs having no rhythmicity, for instance, liver,
kidneys, locomotor and reproductive systems. Finally,
the brain itself is a visceral organ also requiring control
of its state. The unrhythmical flow of afferentation
from these organs does lead to desynchronization of
the EEG in REM sleep. We assume that, although
cerebral cortex receive different afferent flows in REM
and slow wave sleep, the general trend of this process
ing is unique and directed on support of the workable
condition of the visceral systems.
The revealed alternation of cortical afferentation in
the sleepwake cycle force one to change the concepts
concerning the organization of the main information
flows in the nervous system. The proposed structure of
these flows in sleep and wakefulness suggested by us is
shown in Figs. 1 and 2.
In Figs. 1 and 2, the solid lines show the active
informationconducting pathways, and the dotted
lines show the pathways through which conduction at
the given moment is stopped. The main elements of
the scheme are structures determining the possibility
of conduction via one or another pathway. We do not
associate these elements with definite nervous mecha
nisms; therefore, we call them gate devices. These gate
devices have also a second regulating input, which
changes the threshold of signal propagation through
the given device. Structures with similar properties are
well known in neurophysiology. These can be, for
instance, triad synapses or synapses providing presyn
aptic inhibition.
Figure 1 shows the state of propagation pathways in
wakefulness. Information on the environment and
body state (the lower left corner of the scheme) passes
through an open gate device and is directed for analy
sis to the central block, the cerebral cortex. It is very
likely that other brain structures also will be in a simi
lar position. So far it has been experimentally demon
strated that this is true for the cortex. The results of
processing exteroceptive information in the cerebral
cortex are transmitted to a block providing behavior
and motor activity.
In parallel, the output signals are transmitted to a
block that we name Consciousness. The activation of
the neurons in this block leads to the feeling of self
perceptions and the perceptions of the surrounding.
The concept of consciousness is to a considerable
degree intuitive, it is difficult to define it in physiolog
ical terms, and apparently different persons give it a
slightly different meaning. Despite this, consciousness
is most frequently associated with the function of the
cerebral cortex. The results of sleep investigation per
mit us to put in doubt the validity of such a conclusion.
The consciousness is active in wakefulness and almost
completely switched off in sleep or under narcosis. At
the same time, the average level of activity of cortical
neurons does not change significantly in these states.
One has to accept that either consciousness is not
related to the activity of the brain’s neurons or the
localization of structures related to consciousness is
different. In the first case, the issue of the localization
of structures related to processes of consciousness
makes no sense at all. The second choice opens an
experimental way to search for structures connected
with the realization of consciousness. If consciousness
is active in wakefulness and switched off in sleep, it is
necessary to find structures whose neurons will behave
in a similar way. However, this is not the whole story.
The structures that need to carry out the role of the
“substrate of higher brain functions” should have a
wide range of associative connections with zones of all
sensory modalities in the cerebral cortex. Structures of
basal ganglia have such connections [23]. Moreover, it
was shown that excitatory cortical projections to the
neurons of basal ganglia are actually inactivated in the
state of sleep, and the background activity of neurons
of basal ganglia in these periods decreases to a com
plete stop [24–26]. Using the method of positron
emission tomography [27], it was found that in
humans, on transition from wakefulness to sleep, the
average level of cortical activity does not change, but
the level of basal ganglia declines drastically. This is
only a small part of the data that cast doubt on the
HUMAN PHYSIOLOGY Vol. 39 No. 6 2013
 SLEEP, EMOTIONS, AND VISCERAL CONTROL 593

Consciousness Wa k e f u l n e s s

Associative
Behavior, visceral
motor regulation
activity

Brain cortex

Exteroreceptors and Autonomic nervous

proprioreceptors system

Interoreceptors

Environment and the

subject’s body Internal organs

Fig. 1. Scheme of information flows in the animal body in wakefulness. Solid lines indicate active channels of signals transmission.
Dotted lines indicate channels blocked for signal propagation. Black circles with parallel lines are gate devices opening and clos
ing propagation via this or another pathway. Arrows with circles at the end are inputs of controlling synapses determining state of
gate devices. Additional explanations are in the text.

traditional views of the place of the cerebral cortex in
the hierarchy of the brain’s structures. However, a
detailed discussion of this issue is the subject of a sep
arate article.
The right part of the suggested scheme represents
the animal’s body. In wakefulness, information con
cerning the state of internal organs comes to structures
of the autonomic nervous system providing the local
control of their work [28].
During sleep, a radical change of information flows
in the nervous system occurs (Fig. 2). In an ideal case,
after receiving “permission” for sleep, gate devices
simultaneously shift to the opposite position. The
transfer of signals from extero and proprioreceptors
to the brain cortex is blocked. However, information
from the visceral systems of the body begins to come to
the cortex via the same input channels.
Most likely, the main structure in which afferenta
tion from extero and proprioceptive switches to
interoceptive is the thalamus. Active blocking of visual
signals transmission from the retina to the cerebral
cortex at the level of the thalamus was shown [1, 2]. It
is also well known that the pontogeniculooccipital
spikes reflecting activation passing from the pontine
nuclei through the lateral geniculate body appear in
the visual cortex during REM sleep [29, 30]. However,
the relation of these spikes to visceral signals has not
been studied so far.
Parallel to the change of cortical afferentation to
interoceptive, efferent cortical flows should also be
changed. Output signals from the cortex during sleep
reflect the results of the processing of visceral informa
tion and should not be directed to structures associ
ated with behavior and consciousness. In the scheme,
gate devices at these pathways are closed in the state of
sleep. At the same time conduction via the pathways
from the cerebral cortex to structures associated with
an associative processing of information from all vis
ceral systems is opening. It is likely that the nuclei of
the hypothalamus are such regions for associative vis
ceral regulation. However, the efficiency of the cor
ticohypothalamic relations in the sleepwake cycle
has not been investigated.
When visceral parameters via the involvement of
the cortex in the processes of their regulation are nor
malized, the “command” for sleep is removed, the
gate structures are shifted to the opposite position, and
the human or animal wakes up.
Such can be an ideal pattern of switching informa
tion flows in the sleepwake cycle. However, one

HUMAN PHYSIOLOGY Vol. 39 No. 6 2013

594 PIGAREV, PIGAREVA
Consciousness
Behavior,
motor
activity
Brain cortex
Exteroreceptors and
proprioreceptors
Environment and the
subject’s body
Fig. 2. Scheme of information flows in the animal body during sleep. Designations are the same as in Fig. 1.
should remember that the actual switching of gate
structures, especially under conditions of pathology,
can be extended in time. This can lead to the mixing of
exteroceptive and interoceptive information at the
input to the cerebral cortex. Output signals from the
cortex can also be directed to incorrect addresses. Pre
viously [19], we considered in detail the possible con
sequences of such false readdressing, and, on this
basis, simple mechanisms of such phenomena as sleep
hallucinations, the restless legs syndrome, dreams,
sleep palsy, and somnambulism were suggested. In the
same paper [19], a new phenomenon predicted by the
visceral sleep theory, visceral hallucination, is
described, and the possible mechanism of emergence
of motion sickness (seasickness), as a particular case of
visceral hallucinations, is suggested.
However, as noted, the visceral sleep theory did not
concern an important aspect of the sleep process,
namely, its interaction with emotional reactions.
Although sometimes the conclusion concerning emo
tional arrousal in sleep was not sufficiently logically
and experimentally justified, the data of other studies
left no doubt of the presence of such a connection. So,
it seemed important for us to try to understand the
nature of this interaction.
Dream
Associative
visceral
regulation
Autonomic nervous
system
Interoreceptors
Internal organs
3. EMOTIONS AND MECHANISM
OF TRIGGERING AND SUPPORTING SLEEP:
THEORETICAL CONSIDERATIONS
According to the visceral sleep theory, the main
elements providing transitions from wakefulness to
sleep and back are the gate devices opening or closing
the conduction of extero or interoceptive informa
tion (Figs. 1, 2). The change in the states of these gates
should proceed according to commands incoming
from the regions of the central nervous system regulat
ing the sleepwake cycle. Since these commands are
simple and of the same type for all neurons to which
they are addressed, their generation and transfer needs
a limited number of elements having branched projec
tions over a large surface of the correspondent region
of the nervous system. Neurons of several discovered
sleep “centers” have such properties [4]. Now it is
important to understand how the command for transi
tion from wakefulness to sleep and back can be gener
ated.
The visceral sleep theory suggests that sleep is nec
essary to restore the efficiency of the visceral sphere of
the body. Consequently, one can expect that current
parameters of the given visceral system have to be con
stantly compared to the genetically predetermined
values. This process is shown schematically in Fig. 3a.
The block determining the need (or pressure) of sleep
HUMAN PHYSIOLOGY Vol. 39 No. 6 2013
 SLEEP, EMOTIONS, AND VISCERAL CONTROL
(a)
Mechanism of need for sleep
Current value Reference value
of visceral of visceral
parameters (A) parameters (B)
Magnitude of need in sleep
is proportional to mismatch
of input signals A and B
|A–B|
Feeling Need
of tiredness in sleep
Fig. 3. Schemes explaining the first stage of sleep occurring independently in each visceral system and leading to appearance of
sleep pressure (a) and second stage permitting sleep (b).
subtracts from the current values of visceral parame
ters (A) their reference value (B). The absolute magni
tude of this difference (|A – B|) will determine the feel
ing of tiredness or pressure (need) for sleep coming
from the given visceral system, its individual organs, or
their parts.
At the subsequent stage of decision making on
transition to sleep (Fig. 3b), signals of tiredness from
different visceral systems should apparently be
summed up in the device with threshold designated in
the scheme as the neuron–threshold element. The out
put signal of this threshold element will be the com
mand permitting sleep. This command will switch the
gate devices from the state for wakefulness into the
state for sleep. The output signal of the threshold ele
ment, as for any other neuron in the nervous system,
does not entirely depend on the summed signals at the
input. The second important element determining its
excitation is the threshold. The signal controlling this
threshold should be the result of comparison of inde
pendent parameters. First of all, it should accumulate
information on the magnitude of the need for sleep, on
the current position of the body in the environment,
and on the environmental state, and reflect the proba
bility of the safe satisfaction of the need for sleep at the
given moment of time.
Formulated in this way, the conditions of the tran
sition to sleep immediately remind us about the
famous formula of emotions suggested by P. Simonov
for assessing the value of the emotional reaction asso
ciated with a definite behavioral need:
Emotion = function of [N ⋅ (AI–IN)],
where N is the need value, AI is available information,
and IN is information prognostically necessary to sat
isfy this need.
HUMAN PHYSIOLOGY Vol. 39 No. 6 2013
595
(b)
Mechanism of sleep development
Signals of
tiredness from Signals of threshold
different control
visceral
systems
Command,
permitting sleep and
directed to
controlling
synapses (Fig. 1)
Neuron–threshold element
In our situation N is need for sleep. We deliberately
used the word need for sleep as a synonym of the term
that is more widespread in somnology, “sleep pres
sure,” to emphasize sleep’s similarity with any other
behavioral situation. In his papers, Simonov also
included need for sleep in the number of basic biolog
ical needs [20].
The difference of AI and IN reflects the probability
of satisfying this need under specific conditions. We
suggest that the need for sleep, as all other needs of the
body, passes through a stage of emotional assessment.
The emotional assessment of the need for sleep is
more likely performed in the same nervous apparatus
in which the emotional assessment of other behavioral
needs is performed. In the case of a high need for sleep
and an environmental state providing greater possibil
ities for sleep as compared to the needed amount, the
emotion will be positive. In the case of sleep depriva
tion, when the available conditions for normal sleep
turn out to be considerably lower than those needed,
the emotion will be negative. When the emotional
assessment of the need for sleep is formed, this need
will be exhibited for an “auction of needs” together
with all the actual needs of the body at the given
moment, and it will be solved which of them is given
preference. The value of the obtained emotional esti
mates will play a vital role, performing the known
switching function of emotions [20].
In the case that the need for sleep prevails, the
command coming from this level of the chain of deci
sion making will lower the threshold in the “neuron
threshold element” block (Fig. 3), which will lead to
its activation. The impulses generated as a result of the
lowering of the threshold will act as controlling com
mands for the gate devices on information flows
(Figs. 1, 2) to switch them into the opposite position.
596 PIGAREV, PIGAREVA
The animal or human will begin to fall into a sleep,
while their nervous system will switch to processing
signals coming from interoreceptors to restore body
efficiency.
Simonov wrote [20], that the switching function of
emotions is especially clearly seen in the process of the
competition of motifs in determining the dominant
need. He wrote that the dependence of emotions not
only on the amount of need but also on the probability
of its satisfaction significantly complicates the compe
tition of coexisting motives, as a result of which behav
ior is frequently reoriented to a less important but
more easily attainable goal. The causes of several prob
lems arising in the system of sleep control probably are
dependent on this peculiarity of emotions.
It would seem that, at this point, we could consider
our task accomplished. We suggested possible ways of
the interaction of the apparatus of emotional estimates
and the system of sleep initiation. Analysis of this sur
prising functional decussation opened the new ways
for understanding of information mechanisms of
pathological situations associated with falling asleep,
as well as emotional and visceral disorders. However,
subsequent logical analysis demonstrated that the
mechanism of switching behavior from the wakeful
ness mode to the sleep mode was only the first level of
the possible involvement of the apparatus of emotions
in the organization of the sleep process. The next level
of this participation extending already to the entire
subsequent sleep period was immediately apparent.
We repeat again: during sleep, numerous informa
tion flows from interoreceptors distributed in all
organs of the animal or human body are directed to the
brain, and this raises the problem of processing and
transferring this information to different brain cortical
areas and to higher integration centers of visceral sys
tems.
However, since from the informational point of
view, the states of sleep and wakefulness now seem to
be functionally symmetrical states, it can be assumed
that the general principles of the brain’s work with
input signals are similar in both situations. Let us try to
apply the elements of the organization of complex
behavior known to us from the study of wakefulness to
the analysis of visceral information processing, hap
pening during the state of sleep.
In wakefulness, behavior is determined by a combi
nation of diverse needs of the body, and the brain
searches for ways to satisfy these needs, successively
assessing their importance. The most important ele
ment of such ranking is the emotional assessment of
the need.
The combination of signals of tiredness, which
begin to come from different visceral systems already
in the state of wakefulness and reflect the deviation of
the current parameters of visceral systems from per
missible normal values, form the general need for
sleep, which determines the transition of the body to
sleep. However, after falling asleep, the same signals of
tiredness begin to reflect quite different and competing
needs.
Again, to select the sequence of connection for dif
ferent visceral systems to the blocks of central process
ing during the period of sleep, apart from the signals of
the value of need for sleep coming from them, one
should also take into account the available informa
tion at the given moment on the current state of this
system and the information needed for its restoration.
So, we again return to the need to perform an emo
tional assessment of the needs for different visceral
systems.
Thus, during sleep, in the same way as during wake
fulness, the brain structures connected with estima
tions of emotions can rank the arising visceral prob
lems and determine the sequence in which their sig
nals are sent for processing to higher centers of visceral
analysis and integration. As a result, various cortical
areas will be involved in this process. Different initial
states of the bodies will determine a different process
ing order in the cortical zones of signals from visceral
systems. This will determine the individual EEG sleep
pattern.
One can proceed further and suggest that the
mechanism of emotional assessment was created ini
tially for providing the work of visceral systems of the
body. Only later, with the brain’s complication and
appearance of new forms of interaction of the organ
isms with the environment, the same developed and
useful algorithms of processing interoceptive informa
tion were applied also to processing of exteroceptive
signals. We can still observe reflections of this history
as visceral components of emotional reactions to
external stimulations during wakefulness. They may
seem sometimes useful, but more frequently have no
functional sense. Like dreams, visceral components of
emotional reactions are not a serious hazard and
therefore special mechanisms for their suppression
have not been formed. However, when due to the
change of the efficiency of the synaptic transmission
via this or another pathway, the harmonic picture of
the interchange of extero and interoceptive informa
tion, as well as signals of the emotional assessments of
this information is disturbed, we encounter patholog
ical situations of this or another level of severity. How
ever, the consideration of these cases is beyond the
scope of this study.
In the concluding section of our paper, we shall dis
cuss the results of several studies devoted to investiga
tion of the link between sleep and emotions and try to
look at them in the context of the above mentioned
concepts.
4. EMOTIONS AND MECHANISM
OF TRIGGERING AND MAINTAINING SLEEP
The connection of emotions and sleep was reported
in many studies on humans and animals. Note that
HUMAN PHYSIOLOGY Vol. 39 No. 6 2013
 SLEEP, EMOTIONS, AND VISCERAL CONTROL
approach to experimental studies of emotions is con
nected with fundamental complications. The emo
tional state is exclusively subjective. In humans it was
found that emotional experiences about which the
experimenter becomes aware from the verbal reports
of the subject are usually accompanied by various
responses in the visceral sphere (changes in the heart
rate, respiration rate, skin galvanic reaction, etc.).
These visceral responses were concidered as an indica
tor and measure of emotional stress. In experiments
on animals, the report of emotional sensations cannot
be received. However, it is quite justified to consider
that visceral responses identical to those that were
obtained in similar situations in humans can be
assessed as the reflection of an emotional arousal. On
the other hand, one should not forget that in the state
of wakefulness similar changes in visceral parameters
occur constantly, without being accompanied by any
emotional manifestations, and simply reflect the cur
rent life activity of the body. Thus, no change, e.g., in
the heart rate, can be assessed as an undisputable
reflection of emotional sensation.
This consideration becomes especially important
when we analyze results obtained in the state of sleep.
The observed changes in the activity of visceral sys
tems were frequently interpreted as a consequence of
the emotional experiencing of events in dreams. This
point of view for a long time was supported by the
common belief that dreams are associated with peri
ods of REM sleep since in this phase of sleep, the heart
rate and respiration depth drastically change. This
belief is still prevalent, although it was repeatedly dem
onstrated that reports of dreams can be obtained also
at the awakening of the subjects during slow wave sleep
[30]. As for slow wave sleep, the heart and respiration
rates are quite stable. Moreover, reports on dreams
obtained on awakening from REM sleep do not always
include emotional components. As for the visceral
storms of REM sleep, these are phenomena constantly
observed in each episode of such a state in humans and
animals. That is hardly possible to conclude about
emotional activation in REM sleep based only on the
changes in visceral parameters taking place in this
phase of sleep.
In review of published data on the interaction of
emotions and sleep we would like first to remind a
series of fundamental studies performed on cats in the
1970s in the laboratory headed by T. Oniani [31, 32].
In these studies, important observations were made
that were later partly forgotten. It is enough to men
tion the observations of prolonged desynchronizations
on the background of deep nonREM sleep, con
firmed by awakening thresholds. Several studies of this
group dealt with the pattern of activity of limbic brain
structures in different sleep phases. Unfortunately,
only visceral components were used as criteria of emo
tional reactions, and the EEG of different brain struc
tures was recorded monopolarly, using a common ref
erence electrode. The latter circumstance does not
HUMAN PHYSIOLOGY Vol. 39 No. 6 2013
597
permit accepting with confidence the suggested local
ization of the sources of the observed potential
changes. However, the obtained results remain useful
for planning future experiments with the use of new
and more accurate methodical procedures.
Recently, comprehensive reviews of studies reflect
ing the interrelations of emotions and sleep in humans
were published [32, 33]. In most cases they demon
strated the connection of emotional excitement in the
period of wakefulness with the subsequent period of
sleep. First of all, it was manifested in the difficulty of
falling asleep [34]. As a result of the emotional arousal
before falling asleep, sleep becomes less deep, and fre
quent episodes of waking (increased sleep fragmenta
tion) were recorded. Much attention was also given to
the reduction of the latency of the first episode of
REM sleep [35].
These phenomena fit well to suggested above
mechanisms of falling asleep. This mechanism pro
pose that the need for sleep enters the competition
with other behavioral needs, and emotional evaluation
of these needs determine its outcome. Highly emo
tional events in the period of wakefulness creates a
need in the assessment of this event to prolong the pos
itive emotional state or decrease the effect of negative
emotions. The pronounced emotional component
increases the rating of this need. Thus, the rank of the
need for sleep decreases, and the onset of its domina
tion is delayed. Now, for transition to sleep, a consid
erably greater pressure of sleep is needed, i.e., a more
pronounced deviation of the parameters of the visceral
systems from the norm.
In the suggested approach, the physiological basis
of the recommendations on sleep hygiene becomes
clear. Moreover, new key factors of the impact on the
process of falling asleep open. Needs competition
determining the falling asleep depend not only on the
values of the needs but also on the information avail
able and necessary for their satisfaction. It is also worth
paying attention to the pathways of transfer to the
brain of visceral information necessary for the forma
tion of the need for sleep. One can expect that a short
term artificial increase of this activity will exert a pro
nounced somnogenic effect.
We shall pay special attention on the revealed
decrease in the latency of the first episode of REM
sleep after a strong emotional arousal before falling
asleep [35]. This also fits into the suggested model.
The decrease in the latency of REM sleep, in other
words, simply means a decrease in the duration of the
first sleep cycle. How can the visceral sleep theory
explain the phenomenon of dividing the process of
sleep into cycles? After falling asleep central nervous
system should deal with restoration of the visceral sys
tems. With the use of emotional evaluation the prob
lems of various visceral systems are ranked and put in
sequence for servicing. The simplest subsequent strat
egy would be the elimination of all problems in the first
system and transition to the next one. However, in this
598 PIGAREV, PIGAREVA
case, it may turn out that towards the moment of
awakening that is frequently caused by external sig
nals, part of the visceral systems would remain without
the necessary servicing. Moreover, the urgency of their
problems would still increase with time. Another,
more reasonable strategy would be a preliminary
assessment of the probable duration of the uninter
rupted sleep and distribution of this time between all
urgent needs. Scanning all systems as a first approxi
mation in this first cycle of sleep would allow us to
solve the most urgent problems. Under the possibility
of sleep continuation, one could pass to the next level
of task approaching in the second cycle, etc. up to the
elimination of the need for sleep or its minimization
when the rating of the remaining need for sleep
becomes lower than the competing rating of another
urgent need set from the sphere of exteroreception.
The suggested need in cyclic scanning of different vis
ceral systems, parallel to the inner periodicity of many
visceral processes may be kept in mind during discus
sion of the mechanisms of microcyclic changes in the
electrical activity of the brain in different stages of
sleep, which have recently attracted the attention of
researchers [36].
After an event that caused an emotional arousal in
wakefulness when the need in assessing possible con
sequences of this event actively competes with the
need for sleep and postpone the period of falling
asleep, the predicted period of uninterrupted sleep
also decreases. As a consequence, the duration of sleep
cycles decreases; hence, the latency of the first episode
of REM sleep. Indeed, the emotional arousal in wake
fulness played here a detrimental role and increased
sleep fragmentation. However, this hardly occurred in
order to approach the experiencing of the emotional
problems of wakefulness in dreams during the first epi
sode of REM sleep.
The fact that the events of the day can affect the
process of subsequent falling asleep is easily perceived
intuitively. More interesting are the reports that there
is also an inverse influence. The quality and quantity of
sleep considerably change humans’ response to events
of the subsequent period of wakefulness [37].
Under conditions of a deficiency of adequate sleep,
for instance, in the case of shift work, negative emo
tions to aversive events considerably intensify, while
positive responses to pleasant events, in contrast, are
inhibited [37, 38]. Prolonged sleep deprivation inten
sifies the sensation of a depressive mood, anger, frus
tration, tension, and irritability [38–41]. Note that the
metaanalysis of the results of a large number of inves
tigations showed that sleep deprivation affects the
mood rather than indices of cognitive responses [42].
In subjects who woke up, a better mood was
recorded in those cases when they were awakened after
termination of the period of REM sleep, i.e., when the
sleep cycle ended, compared to cases of awakening
during REM sleep [43].
Several papers dealt with the specific influence of
sleep deprivation on the subjective assessment of emo
tional stimuli. Certainly, these data are not so simple to
compare since they considerably depend on the pat
tern of the presented stimuli. However, the general
tendency manifested itself always: sleep deprivation
shifted the emotional background to the negative side.
For instance, an increase in the number of negative
estimates was observed on presentation of visual
images whose content was changed from emotionally
neutral to increasingly negative [44]. When a set of
pleasant, neutral, and unpleasant stimuli was used,
sleep deprivation did not affect the assessment of the
pleasant and unpleasant stimuli. However, subjects
after sleep deprivation more negatively assessed neu
tral images; their mood was distinctly negative, and
the objective assessment of caution declined [45]. In
this study, the conclusion was made that sleep is asso
ciated with the fine regulation of the emotional assess
ment according to “better safe than sorry” principle.
Thus, an uncertain situation is more preferably
assessed as dangerous than as safe [45, 46].
The effect of sleep deprivation on the perception of
visual images of different emotional content was stud
ied also using papillography as an indicator of process
ing cognitive and emotional information. The authors
[47] conclude that sleep deprivation changes the affec
tive estimate to a more negative one in ranking emo
tionally neutral stimuli.
Despite the diversity of the experimental
approaches to the study of the effect of low quality of
sleep on the period of subsequent wakefulness, one
common picture was observed: it was always a shift of
the emotional background towards the negative side
[48–50].
The possible mechanisms of this phenomenon are
also clear. If sleep as a result of deprivation procedures
was excluded or interrupted, this means that for some
visceral systems, the need for sleep was not satisfied.
Hence, the available information on the satisfaction of
this need (AI in Simonov’s formula of emotions)
turned out to be considerably smaller than the neces
sary information (IN). As a result, a negative emo
tional state is evoked. The more sleep was reduced or
disturbed, the more negative the emotional state at the
moment of awakening. It is well known that against the
negative emotional background, all negative emotions
become more unpleasant, and the attractiveness of all
positive emotions decreases [51]. This was observed in
the aforementioned studies. One should take into the
account that probably also visceral problems that do
not reach our consciousness pass through the same
emotional assessments as the events during wakeful
ness. Thus, their interrelation is quite natural.
In some studies, the authors, due to the reasons
mentioned previously, relate to emotions mainly the
phase of REM sleep. Thus, after periods of sleep with
a high content of REM sleep, the subjects more fre
quently assessed the presented visual stimuli as nega
HUMAN PHYSIOLOGY Vol. 39 No. 6 2013
 SLEEP, EMOTIONS, AND VISCERAL CONTROL
tive [52–54]. Based on these data, the conclusion was
made that namely this state of sleep modulates the
processing of emotional information in humans. It is
considered that REM sleep is involved in the adequate
emotional response necessary on the next day to assess
the potential danger and control of reactivity in
response to stimuli with an emotional, especially
threatening, background [55–57].
While interpreting such kind of data one should
remember that an increase in the proportion of REM
sleep indicates a decrease in the duration of individual
sleep cycles and, hence, an increase in sleep fragmen
tation. As noted above, the fragmentation of sleep
reduces its efficiency in the restoration of visceral well
being and increases the possibility that some visceral
problems will remain unsolved at the moment of
arousal from sleep. As a result, the subsequent wake
fulness will develop against an negative emotional
background. We have already discussed its conse
quences. However, one should also remember that in
most cases, REM sleep terminates the sleep cycle.
Thereby, processes of REM sleep turn out to be most
vulnerable in the case of unexpected sleep interrup
tions. These interrupted processes will not only deter
mine the negative emotional state on awakening, but
with time can comprise the main zone of risk for
health. Changes in the heart rate, as well as cardiac
and respiration arrest, in combination with the body
temperature dropping and muscular atony in periods
of REM sleep give grounds to suppose that during this
period the efficiency of the cardiovascular system is
restored. Possibly this determines the well known rela
tion of disturbances of coronary circulation and emo
tional agitation.
In conclusion, we would like to say that our
approach is based on the assumption that the same
brain structures and the same neurons in the sleep
wake cycle are alternately involved in the work with
intero and exteroceptive information flows. The
experiments performed earlier confirmed that the
cerebral cortex works in this way. The hypothesis
advanced in the given paper suggests that this may be
true also for other regions of the brain, in particular,
for structures involved in processes of the emotional
assessment of needs. According to Simonov’s need
informational theory, such structures are the hypo
thalamus, amygdala, hippocampus, and prefrontal
cortex [56–58]. The method of electroencephalogra
phy in combination with positronemission and mag
netic resonance imaging demonstrated that the activ
ity of these structures in sleep at definite moments can
exceed the level of their activity in quiet wakefulness
[35, 59]. These data can serve still another indirect
argument in favor of the visceral theory of sleep.
ACKNOWLEDGMENTS
We are grateful to A.L. Kalinkin, who drew our
attention to the importance of searching for the rela
HUMAN PHYSIOLOGY Vol. 39 No. 6 2013
599
tion of the visceral sleep theory and mechanisms of
emotions, and to V.V. Raevskiy and E.V. Levichkina
for their critical discussion of the manuscript.
The study was supported by the Russian Founda
tion for Basic Research, project nos. 130400941 and
130400741.
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Translated by I.A. Pogosyants