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Primary consciousness can be defined as simple aware- multiplicity of conscious substates during waking and
Perception
Detailed visuomotor and other ness that includes perception and emotion. As such, it the contrasting single-mindedness of dreaming 2.
sense modality information is ascribed to most mammals. By contrast, secondary Waking consciousness is richer than dream con-
that constitutes the consciousness depends on language and includes such sciousness in allowing the measurable distinction
representational structure of
features as self-reflective awareness, abstract thinking, between task and default modes of the brain3 and the
awareness. Such awareness
must involve the interaction volition and metacognition1. In adult humans, dreams related difference between background and foreground
and integration of emotion. that occur during rapid eye movement (REM) sleep have processing 4. Dream consciousness is richer than waking
features of primary consciousness but, as shown in FIG. 1 consciousness in its ability to create a remarkably reli-
Secondary consciousness and Supplementary information S1 (table), dreams do able simulacrum of the world and the notable capacity
Subjective awareness including
perception and emotion that is not strongly evince the characteristics of secondary to integrate highly disparate images and themes into a
enriched by abstract analysis consciousness. seamless scenario, as shown in FIG. 1.
(thinking) and metacognitive In humans, consciousness varies dramatically in Dreaming abounds in features of primary conscious-
components of consciousness
intensity and quality during the sleep–wake cycle. ness, especially perceptions and emotions, which are
(awareness of awareness).
Whether we are awake (and alert with the full panoply produced by the brain without external stimulation. But,
Rapid eye movement (REM) of secondary aspects of consciousness), asleep (with compared with waking, dreaming is deficient in its fail-
sleep greatly diminished awareness) or dreaming (with the ure to recognize its own true condition, its incoherence
Sleep with electroencephalo- internally generated perceptions and emotions of pri- (or bizarreness), its severe limitation of thought and its
graphic evidence of brain
activation (similar to that of
mary consciousness) depends on the three objectively impoverishment of memory (see Supplementary infor-
waking) but with inhibition of identifiable states of the brain: waking, non-rapid eye move- mation S1 (table), which illustrates the scientific utility
muscle tone (as measured by ment (NREM) sleep and REM sleep (BOX 1). The strategies of subjective experience). In consideration of these data,
electromyography) and by which those states are investigated are outlined in we might expect that some brain processes are enhanced
involuntary saccadic eye
movements (the REMs).
Supplementary information S2 (box). during REM sleep (during which humans dream),
Waking consciousness can be defined as the aware- others are suppressed and still others remain the same as
ness of the external world, our bodies and our selves they are during waking 5. As will be discussed below, that
Division of Sleep Medicine,
Harvard Medical School, (including the awareness of our awareness) that humans is exactly what we find.
Boston, Massachusetts, experience when awake. When dreaming we are also In this Review, I first describe the differences between
02215, USA. consciously aware; we have perception and emotion, primary and secondary consciousness in relation to
e‑mail: allan_hobson@hms. which are organized in a scenario-like structure, but we waking and sleep. I then consider evolutionary and
harvard.edu
doi:10.1038/nrn2716
erroneously consider ourselves to be awake despite abun- developmental aspects of REM sleep, the sleep stage
Published online dant cognitive evidence that this cannot be true. Another that correlates highest with dreaming. This is followed
1 October 2009 difference between waking and dreaming is the striking by an overview of theories of the function of REM sleep,
including the new hypothesis that primary conscious- model for control of the conscious state, which explains
ness is an important building block on which secondary the psychological features of dreaming and waking at the
consciousness is constructed. last, I describe the AIM mechanistic (neuronal and molecular) level, and I
use the AIM model to show that lucid dreaming is an
intermediate position between REM sleep and waking.
An important caveat is that although the distinctive
features of dream consciousness (see Supplementary
information S1 (table)) are maximally correlated with
REM sleep, they are also found — to a limited degree —
in nREM sleep, especially in stage I, at sleep onset, and in
stage II, late in the night 6−8. Because of sleep inertia, it is
difficult to evaluate the reports of mental content when
subjects attempt to awaken from the deeper stages III
and Iv of nREM sleep9, so it is unclear whether some
features of dream consciousness also occur during these
stages. For these reasons, I focus here on the comparison
between waking and REM sleep because the similarities
and differences are reliable and informative with respect
to theories of consciousness. Importantly, all the varia-
bles under discussion in this Review, be they psychologi-
cal or physiological, can be differentiated quantitatively
rather than qualitatively 6.
100
Dement deprived human subjects of REM sleep and
reported that 3–5 days of this procedure triggered cog-
Non-therian nitive deterioration36,37. on the first night sleep was
150
mammals Early therian interrupted only 5 times to prevent REM sleep, but on
mammals
the fifth night 50 arousals were needed, indicating that the
body was attempting a homeostatic ‘catch up’ on lost
REM sleep
REM sleep. The conclusion — that it was dreaming, not
First true REM sleep only in hatchlings
200 mammals NREM sleep sleep, that was essential to mental health — was chal-
Unknown lenged by Anthony Kales, who showed that equivalent
amounts of nREM sleep deprivation were equally del-
eterious38. Although the relative benefits of REM and
nREM sleep to mental health are still being investigated,
250 Mammal-like reptiles
it should be noted that both stages of sleep are almost
Figure 2 | Developmental and evolutionary considerations. a | Human sleep and age. certainly useful. In any case, it is clear that both stages
The marked preponderance of rapid eye movement (REM) sleep Nature
in Reviews | Neuroscience
the last trimester of are exquisitely regulated and conserved39,40.
pregnancy and the first year of life decreases progressively as waking time increases. The significance of these early studies in humans
Note that non-rapid eye movement (NREM) sleep time, like waking time, increases after is clear: sleep is essential to mental health. needless
birth. Despite its early decline, REM sleep continues to occupy approximately 1.5 hours to say, psychologists generally adhere to the theory of
per day throughout life. This suggests that its strongest developmental contribution is to
psychological benefit 41,42. The fact that sleep depriva-
early brain–mind development but that it subsequently plays an equally indispensable
part in brain–mind maintenance. b | The evolution of REM sleep. Birds and mammals
tion invariably causes psychological dysfunction sup-
evolved separately after branching off from the ancestral tree many millions of years ago. ports the functional theory that the integrity of waking
Both birds and mammals are homeothermic, and both classes of animal have appreciable consciousness depends on the integrity of dream con-
cognitive competence. Restoration of thermoregulatory capacity is a strongly evidenced sciousness and that of the brain mechanisms of REM
function of REM sleep. With respect to the possible enhancement of cognitive skills by sleep.
REM, it is significant that both birds and mammals are capable of problem solving and A paradoxical improvement in mood is observed in
both can generate forms of verbal communication (‘primitive language’). Part a is depressed patients after one night of REM sleep depriva-
modified, with permission, from REF. 27 © (1966) American Academy for the tion43,44. Equally paradoxical is the complete suppression
Advancement of Science. Part b is reproduced, with permission, from REF. 10 © (1970) of REM by the monoamine oxidase-inhibiting (MAoI)
American Museum of Natural History.
drugs that are used to treat depression. These facts invite
speculation and further study. For now, we can say only
Sleep and energy regulation. The most convincing evi- that the monoamines serotonin, noradrenaline, hista-
dence of sleep function comes from the experiments mine and dopamine, as explained below, are important in
of Allan Rechtschaffen and colleagues33. Rats that were the regulation of sleep, mood, learning and temperature
subjected to total sleep or selective REM sleep depri- control. The balance between these biogenic amines and
vation all died with a stereotyped syndrome of caloric acetylcholine is central to our concepts of the regulation
and thermal dyscontrol. En route to their demise, the of cognition and mentation.
Forebrain
+ + + Forebrain — immature cycle
Midbrain
Brainstem Activation
+ Deactivation
Pons
– –
Medulla REM sleep
Activation Deactivation
Spinal column Aminergic NREM sleep
neuron REM-on
Cholinergic
neuron REM-off
Sleep and learning. Giuseppe Moruzzi was the first serotonin-norepinephrine reuptake inhibitors (SnRIs)
to suggest that sleep mediates plastic processes in the actually enhances learning 54–57. Could it be that updating
brain45. numerous studies subsequently showed that memory with newly learned material is only a small part
REM sleep duration is augmented when animals learn a of the learning maintenance task of the sleeping brain?
new task and that REM sleep deprivation interferes with Could it be that we must relearn all that we already
such learning 18,19,46–49. These effects — if they were found know, as well as integrate new experiences into that vast
at all — are small, prompting some critics to deny that storehouse of data? or do we simply need to rerun our
there is any significant benefit to learning from sleep50–52. built-in virtual reality simulation circuits to prevent
Whether or not such a conclusion is justified, it must be disuse-induced memory loss?
admitted that learning cannot be the only or even the The hyperassociative and synthetic properties of
prime function of sleep. A more overarching and com- dreaming suggest tentative answers to these important
pelling theory is needed, but any such theory should be questions. The fact that no more than 20% of dream
compatible with and take account of scientific findings, material is in any way related to what the dreamer rec-
which support the hypothesis that the brain changes the ollects of events in his or her life history 58 indicates that
status of its information as it sleeps53. dreaming could represent a set of foreordained scripts or
If sleep is essential to memory, we must wonder scenarios for the organization of our waking experience.
why semantic memory does not seem to be strongly According to this hypothesis, our brains are as much
enhanced by sleep, why the enhancement of procedural creative artists as they are copy editors. What we may
learning by sleep, although statistically significant, is so need to navigate our waking world is an infinite set of
weak, why neither selective REM nor selective slow- charts from which we may draw the one best suited to an
wave sleep (SWS) deprivation impairs memory con- equally infinite set of real-life possibilities. To this end,
solidation and why the suppression of REM sleep with it makes sense to tie even remotely connected scraps of
selective serotonin reuptake inhibitors (SSRIs) and experience together to give our library of plots enough
confirmed that the cholinergic pedunculopontine teg- is likely that at least some regional activation patterns
mental neurons are REM-on cells and serotonergic dor- are caused by these autonomic control systems as, in
sal raphe nucleus and noradrenergic locus coeruleus the periphery, blood flow control is mediated by similar
neurons are REM-off cells98. It has also become clear that autonomic mechanisms. Thus, time is a fourth dimen-
GABA (γ-aminobutyric acid) and glutamate participate sion of the AIM model. Waking has high values of A,
in this process66. I and M, whereas REM has a high value of A but low
Waking consciousness is associated with the activation values of I and M (FIG. 4). The brain is activated in both
of all modulatory brainstem neurons — that is, the neu- states, but only in waking are the input–output gates
rons that manufacture and release the neuromodulators open and is aminergic modulation strong.
acetylcholine, dopamine, histamine, noradrenaline and The ‘state space’ approach also enables the mapping
serotonin90,92,99,100. Dopamine- and acetylcholine-releasing of exceptional mental states such as lucid dreaming 106
neurons are also active during REM sleep, but noradrena- and abnormal conditions such as coma and minimally
line-, serotonin- and histamine-releasing neurons shut off conscious states107. Sleep disorders such as narcolepsy 108
completely during that state92,101. nREM sleep is interme- and many psychiatric syndromes (such as depression43,44)
diate in that all modulatory neurons slow down relative to also find their place in the AIM state space66.
the waking state, but they do not shut off (as some of them
do during REM sleep). Imaging, lesion and eeG studies
owing to the inactivation of the REM-off cells, the The advent of brain imaging technology (positron emis-
activated but off-line brain is said to be aminergically sion tomography, single-photon emission computed
demodulated and, reciprocally, cholinergically hyper- tomography and MRI) has revolutionized sleep and
modulated100. The absence of three wake-state modu- dream research109–112. These techniques have revealed
lators and the persistence of dopamine release could a global deactivation of the brain during nREM sleep
explain some of the cognitive characteristics of dream- compared with waking and a subsequent reactivation
ing, such as the visual hallucinations, the bizarreness, during REM sleep — to levels above those seen in wak-
the lack of self-reflective awareness and the amnesia. ing — of the pontine tegmentum, the amygdala and its
Interestingly, dopamine has been proposed to mediate projections to the parahippocampal cortex, the anterior
the psychosis of mental illness, especially schizophre- commissure, the parietal operculum, the deep frontal
nia102, and it might have a similar role in the psycho- white matter and the midline thalamus109–111 (FIG. 5a).
sis of dreams. The importance of chemical balance is These findings fit well with the subjective experience
illustrated by these considerations. Whether a brain of the abeyance of consciousness during nREM sleep
generates a state of external awareness (waking) or and the reinstatement of consciousness (but now with
simulates that state (dreaming) may be a function of its an accentuation of such internally generated primary
neuromodulatory ratio. features as perception and emotion) during REM sleep.
The findings are also in agreement with reports by
The AIM model. When the differences in brainstem neu- patients that dreaming ceases after stroke damage to the
ronal activity during waking and REM sleep were first parietal operculum and deep frontal white matter 113,
noted, we proposed that the wake–nREM–REM sleep two of the brain areas shown by imaging methods to be
cycle was the result of interactions between the aminergic hyperactivated in REM sleep. Patients with therapeutic
REM-off cells and the cholinergic REM-on cells93. We interruptions of deep frontal white matter (lobotomy)
advanced the ‘activation-synthesis’ hypothesis of dream- also reported cessation of dreaming. By contrast, patients
ing71, which posits that brain activation during REM sleep with temporal lobe epilepsy experienced their seizures
results in the synthesis of dream mentation. Since that as “dreamy states”114; these patients also reported inten-
time, we have tested, modified and extended these two sification of nocturnal dreams, suggesting that the tem-
hypotheses in the light of new experimental data66,100,103. poral lobe and its connections to other brain regions are
Recent work has revealed additional mechanistic details involved in the generation of primary consciousness and
regarding neuronal control104,105 during REM sleep. For dreaming 113. As these structures are highly evolved in
example, the triggering mechanism for PGo waves in the lower mammals, it is possible that the limbic brain has
lateral pons has been shown to interact with glutaminergic an important role in mediating primary consciousness
neurons in the pontine reticular formation. and dreaming.
The claim that waking and dreaming are at once simi-
lar and different has been developed into the AIM model Lucid dreaming. How can primary and secondary aspects
and dream consciousness theory. A three-dimensional of consciousness be investigated neurobiologically?
AIM model (FIG. 4) describes different states of the brain A unique opportunity to advance the science of con-
and shows how they vary over the course of a day and sciousness in relation to sleep is the study of an unusual
night in adult humans. The model cannot yet explain state called lucid dreaming, in which subjects regain
the regional differences in brain activity that distinguish many aspects of waking while continuing to dream115.
REM sleep from waking. It remains to be seen whether new evidence from quantitative electroencephalo-
the blood flow changes measured with positron emission graphic (EEG) studies106 suggests that lucid dreaming is
tomography and functional MRI reduce to the changes the subjective experience of a waking dream in a hybrid
of value M in the AIM model. Because M is the com- brain state, with the rare but instructive coactivation of
posite ratio of aminergic and cholinergic influences, it both primary and secondary consciousness circuits.
When subjects shift from non-lucid to lucid REM synchronization of cortical neuronal activity that is
sleep, they show an increase in the high-frequency necessary to effect the temporal binding that is believed
(40 Hz) band of their frontal EEG106 (FIG. 5b). This sort to be essential to waking consciousness59. In addition,
of high-frequency EEG activity could represent the during lucid dreaming there is an increased coherence
of frontal activation with activation in the posterior
cortex 106 (FIG. 5c). This means that the cortex is not
a only more activated but also more synchronized when
subjects become aware that they are dreaming.
Parietal operculum
Functional MRI results complement and extend
Dorsolateral
prefrontal cortex Posterior cingulate these observations by revealing that dream lucidity is
Anterior cingulate correlated with increased activation of the cortical areas
that are thought to mediate the features of secondary
Deep frontal
Parahippocampal consciousness, including the precuneus, frontopolar
white matter
cortex and dorsolateral prefrontal cortex, temporal cortex and
Amygdala inferior parietal lobules (M. Czisch, R. Wehrle and M.
Pontine tegmentum
Activated Dresler, personal communication).
Deactivated
Conclusions and future directions
b The REM sleep–dream protoconsciousness hypothesis
proposed here suggests that the development and main-
tenance of waking consciousness and other high-order
brain functions depends on brain activation during sleep.
The hypothesis places an emphasis on the primary aspects
of consciousness, the basis for which — it is posited —
1.50 arises late in evolution and earlier in brain development
than do the brain substrates that support the secondary
Waking Lucid dreaming REM sleep 0.50 aspects of waking consciousness. Waking consciousness,
with its impressive secondary features, might be present
c CSD only in humans, who have the highly evolved and exten-
Waking Lucid dreaming REM sleep sive cortical structures that are probably necessary to
0.3 0.3 0.3 mediate the abstract aspects of conscious awareness.
CSD coherence
CSD coherence
CSD coherence
and the brain states that underlie them100. Without such the new neuroscience of dream consciousness sends an
a bridge, there is no safe passage between the genetic appeal for more detailed attention to phenomenology
and the phenotypic banks of the mind–brain chasm that could help those disciplines advance without loss
that still divides that field. To the humanities in gen- of their traditional and important adherence to meaning
eral, and to psychology and philosophy in particular, and to moral values.
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sUppleMeNTARY INFORMATION
See online article: S1 (table) | S2 (box)
desynchronized sleep phenomena: enhancement via electroencephalogram patterns during behavioral
small volume infusions. Brain Res. 191, 215–224 sleep in the cat. Electroencephalogr. Clin. All liNks Are Active iN the oNliNe PDF
(1980). Neurophysiol. 10, 291–296 (1958).
Biography
Allan Hobson directed the laboratory of neurophysiology at the
Massachusetts Mental Health Center (Boston, Massachusetts, uSA)
from 1968 to 2003. He has published more than 200 original peer-
reviewed articles and 10 books on sleep and dreaming. He is the recip-
ient of the Distinguished Investigator Award of the Sleep Research
Society and the Farrell Prize of the division of Sleep Medicine at
Harvard Medical School. In 2005 he moved to Sicily, where he now
lives with his family. He has taught his course on the basic science
of sleep and dreaming to graduate students throughout Europe and
Asia.
Online At a Glance
• We know how, but not why, the brain is activated in sleep. I suggest
that brain activation in sleep allows the development and mainte-
nance of circuits necessary for higher brain functions, including
consciousness.
• Brain activation and sleep occurs early in the development of mam-
mals and birds. It may therefore be a state of protoconsciousness in
those animals that evince rapid eye movement (REM) sleep.
• our dreams are reminders that we too were (and still are) proto-
conscious. We are always ourselves in our dreams; we sense, we
act and we feel vividly in an entirely fictive world of the brain’s
devising.
• The protoconscious state of REM sleep dreaming is as much a
preparation for waking consciousness as a reaction to it. We are as
much getting ready to behave as we are getting over the effects of
our behaviour.
• Dreams have more in common than not across individuals. As a
species, we need REM sleep dreaming to accomplish shared goals,
such as being capable of consciousness when awake.
• REM sleep dreaming can be viewed as a virtual reality pattern gen-
erator used by the brain to instantiate and maintain its readiness
for adaptive interaction with the world.
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