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This article was downloaded by: [Gazi University]On: 17 August 2014, At: 22:15Publisher: RoutledgeInforma Ltd Registered in England and Wales Registered Number: 1072954 Registered office: MortimerHouse, 37-41 Mortimer Street, London W1T 3JH, UK
Neuropsychoanalysis: An Interdisciplinary Journal
for Psychoanalysis and the NeurosciencesPublication details, including instructions for authors and subscription information:http://www.tandfonline.com/loi/rnpa20
The New Neuropsychology of Sleep: Implications for
PsychoanalysisJ. Allan Hobson
a
aLaboratory of Neurophysiology, Massachusetts Mental Health Center, 74 Fenwood Road,
Boston, MA 02115
Published online: 09 Jan 2014.
To cite this article:J. Allan Hobson (1999) The New Neuropsychology of Sleep: Implications for Psychoanalysis,Neuropsychoanalysis: An Interdisciplinary Journal for Psychoanalysis and the Neurosciences, 1:2, 157-183, DOI:
10.1080/15294145.1999.10773258
To link to this article: http://dx.doi.org/10.1080/15294145.1999.10773258
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57
The New Neuropsychology of Sleep: Implications
for Psychoanalysis
J Allan Hobson
Abstract:
n
his 1895 Project for a Scientific Psychology,
Sigmund Freud clearly stated his goal: to integrate the workings
of the mind with the workings of the brain. But in his day, too
little neurobiology was known to make his goal attainable and he
tried instead to understand such fascinating normal phenomena
as dreaming in exclusively psychodynamic terms. A century later,
Freud s brilliant but entirely speculative dream theory
is
in need
of radical revision,
not complete overhaul, because dreams,
as well as other unusual states of consciousness, can finally be
approached from the solidfoundation ofmodem neuroscience. In
other words, the goals of Freud s Project are at last within our
grasp. Ironically, an obstacle to progress
is
the tenacious adher-
ence oforthodox psychoanalysis to a theory that even by the stan-
dards of its originator,
is
now clearly outm04ed.
n
this paper, recent positron emission tomography (PET)
imaging and brain lesion studies
in
humans are integrated with
new basic research findings at the cellular level in animals to
explain how the formal cognitive features
of
dreaming may be the
combinedproduct
of
a shift in the neuromodulatory balance
of
the
brain and a related redistribution of regional blood
flow
The
human P T data indicate a preferential activation in rapid eye
movement (REM) sleep of the pontomesencephalic brainstem and
of
limbic and paralimbic cortical structures involved in the emo-
tional and mnemonic aspects of cognition. The pontine brainstem
mechanisms controlling the neuromodulatory balance of the brain
in rats and cats include noradrenergic and serotonergic influences
which enhance waking and impede REM via anticholinergicmech-
anisms, and cholinergic mechanisms which are essential to R
sleep and only come into ful l play when the serotonergic and
noradrenergic systems are inhibited.
n
REM, the brain thus be-
comes activated but processes its internally generated data
in
a
manner quite different from that
of
waking.
This paper combines with permission) the content
of
a recently pub
lished review by the author and his colleagues Robert Stickgold and Ed
ward Pace-Schott
(NeuroReport,
9:R9-R14, 1998) with an essay prepared
for a presentation to the Neuro-Psychoanalysis group
of
the
New
York
Psychoanalytic Institute on November 7, 1998. The author s research is
supported by NIMH grants MH13923 and MH48832, a NASA grant, and
by the Mind-Body Network of the John
D
and Catherine
T
MacArthur
Foundation.
J Allan Hobson is Professor of Psychiatry, Harvard Medical School;
Laboratory
of
Neurophysiology, Massachusetts Mental Health Center,
Boston.
The New Neuropsychology
n
Psychoanalysis
The field of sleep and dream research has recently
been invigorated by convergent new data from two
complementary neuropsychological sources Maquet
et aI., 1996; Braun et aI., 1997; Nofzinger, Mintun,
Wiseman, Kupfer, and Moore, 1997; Solms, 1997). In
the brain imaging and brain lesion studies to be re
viewed in detail below, the evidence for a strong brain
stem role in human REM sleep dream generation
complements the cellular and molecular level data in
animal studies and reveals an unexpectedly prominent
role
of
the limbic system in the selection and elabora
tion
of
dream plots. The emerging picture
of
dreaming
as
the synthesis
of
emotional and sensorimotor data
generated by the distinctive mechanisms
of
brain acti
vation in REM sleep will be
of
interest to all who
share Sigmund Freud s early vision of a psychology
founded on the solid base
of
neuroscience Freud,
1895) even as it forces revision
of
his highly specula
tive dream theory Freud, 1900).
Insofar as psychoanalysis remains committed to
Freud s view
of
dreaming, or to any revisions of that
view that retain the notion
of
disguise-censorship as
the mechanism of dream bizarreness, the new results
do not provide the faintest modicum of support. Also
without support is the corollary assumption that
dreaming affords privileged access to unconscious mo
tives via the technique
of
free association to bizarre
dream material.
If, instead, the modern psychoanalyst takes the
more open view, that afforded by the Activa
tion-Synthesis Hypothesis, that dreaming is a physio
logical projection test revealing, rather than
concealing, emotionally salient concerns, the prospect
is quite bright. The question is, can psychoanalysis
afford to admit that Freud was wrong about the dream
theory? Even if some would agree that it cannot any
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158
longer afford not to do so, the consequences
such
an avowal are profound and far-reaching. Because the
dream theory is so foundational, its renunciation
forces a major reformulation upon the whole field.
One face-saving approach is to revisit the 1895
Project for a Scientific Psychology, which Freud
abandoned in favor the 1900 dream theory, and to
proclaim that the goals he set himself in that work are
the very same goals we now see to be within reach.
The intervening century could thus be viewed
as
an
unfortunate interlude fraught with the perpetuation
many regrettable errors but with such important suc
cesses
as
the work
John Bowlby on attachment and
separation. With that idea in mind let us now review
the recent data, and in its light examine the current
status Freud s dream theory.
rain ased Differences between Waking and
Dreaming
The demonstration that the human brain activation
pattern REM sleep is distinctly different from that
waking has an important bearing upon our concep
tion of how conscious states are generated by the
brain. It supports the hypothesis that quite different
mechanisms underlie waking and dreaming conscious
ness and that those differentiated mechanisms are
causally determinant the differences in our subjec
tive experiences
the two states. For some time, it has
been the cognitive similarities between waking and
dreaming that have been emphasized by dream psy
chologists (Antrobus, 1983; Foulkes, 1990, 1993,
1997; Moffitt, 1995). These similarities have been as
cribed to brain activation processes that were thought
to be identical in the two states and this inference
identity was supported by evidence from neurophysi
ology shared electrical and ionic mechanisms for
cortical EEG activation seen in both REM sleep and
waking (Llinas and Pare, 1991). Besides being unable
to account for the robust differences between wake
and dream consciousness (Kahn, Pace-Schott, and
Hobson, 1997), this inference is now clearly in need
amendment on physiological
g r o u n ~
Until now, the best available candidate mecha
nism for the differentiation dreaming from waking
cognition has been the drastic reduction in the release
the neuromodulators norepinephrine and serotonin
which drop from their steady high levels in waking to
almost zero in the REM sleep cats and rats (Hobson,
1988, 1990, 1992, 1994, 1997a; Mamelak and Hob
son, 1989; Hobson and Stickgold, 1994, 1995a). We
J.
Allan Hobson
suggest that the newly described differences in re
gional activation found in humans may result from the
same neuromodulatory differentiation found in animal
studies (see Hobson and Steriade, 1986; Steriade and
McCarley, 1990, for reviews) and predict that it is just
a matter of time before more sophisticated imaging
confirms these chemical differences in the human
brain too. Indeed, a REM-related decline in central
nervous system (eNS) serotonin has recently been
demonstrated in humans using depth electrodes and
microdialysis (Wilson et aI
1997).
rain Mind States and the Studyof Consciousness
One of the strongest supports for the scientifically hy
pothesized unity
brain and mind comes from the
changes in conscious experience that
we
all experi
ence when we doze off, fall deeply asleep, and, later,
dream. The initial loss of contact with the outside
world at sleep onset with its flurry
fleeting hypna
gogic images, the deeply unconscious oblivion
sleep early in the night, and the gripping hallucinoid
scenarios of late-night dreams, all have such strong
and meaningful underpinnings in brain physiology as
to make all but certain the idea that our conscious
experience
is the brain-mind s awareness
its own
physiological states (Hobson, 1994, 1997).
But whether or not they are accepted
as
firm
proof of brain-mind identity, these simultaneous sub
jective and objective events encourage the concept
a unified system which we call the brain-mind (Kahn
et aI 1997). And they further encourage a detailed
accounting in the separable analytic domains the
neurophysiology and psychology the events that
change, or remain the same, as the brain changes state.
It is within this paradigm
simultaneous conscious
state and brain-state change that I now review and
integrate data from three sources:
1
The formal and quantitative characteristics con
sciousness in waking, sleeping, and dreaming;
2
The cellular and molecular level brain events that
have been measured in awake, NREM, and REM
sleeping animals; and
3
The neuropsychological analysis
the effect
brain lesions and regional blood flow changes upon
the conscious states humans.
REM Sleep Dreaming Defined
Formal Features of
R
Sleep Dreams
REM sleep dreams have several distinctive formal fea
tures which the underlying brain state must somehow
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h New Neuropsychology of Sleep
determine. They include: sensorimotor hallucinations;
bizarre imagery; the delusional belief that one is
awake; diminished self-reflective awareness; orienta
tional instability; narrative structure; intensification of
emotion; instinctual behaviors; attenuated volition;
and very poor memory. Table 1 summarizes these fea-
TABLE 1
The Formal Features of REM Sleep Dreaming
Hallucinations Especially visual and motoric, but occasionally in
any and all sensory modalities Snyder, 1970; McCarley and
Hoffman, 1981; Hobson, 1988; Zadra, Nielsen, and Don
deri, 1998).
Bizareness Incongruity imagery is
strange, unusual, or impossi
ble); Discontinuity imagery and plot can change, appear, or
disappear rapidly); Uncertainty persons, places, and events
are often bizarrely uncertain by waking standards) McCarley
and Hoffman, 1981; Porte and Hobson, 1986; Hobson et aI
1987; Hobson, 1988; Mamelak and Hobson, 1989; Williams,
Merritt, Rittenhouse, and Hobson, 1992; Reinsel, Antrobus,
and Wollman, 1992; Hobson and Stickgold, 1994, 1995b; Re
vonsuo and Salmivalli, 1995).
Delusion We are consistently duped into believing that we are
awake unless we cultivate lucidity) Purcell, Mullington,
Moffitt, Hoffman, and Pigea, 1986; LaBerge, 1990, 1992; Bar
rett, 1992; Kahan and LaBerge, 1994; Hobson, 1997b).
Self-reflection absent or greatly reduced relative to waking Recht
schaffen, 1978; Barrett, 1992; Bradley, Hollifield, and
Foulkes, 1992).
Lack of orientational stability Persons, times, and places are fused,
plastic, incongruous, and discontinuous McCarley and Hob
son, 1981; Hobson et aI., 1987; Hobson, 1988; Williams et
aI 1992; Rittenhouse et al., 1994; Stickgold, Rittenhouse, and
Hobson, 1994; Revonsuo and Salmivalli, 1995).
Narrative story lines Explain and integrate all the dream elements
in a confabulatory manner Foulkes, 1985; Cipolli and Poli,
1992; Hobson, 1988; Hunt, 1991; Montangero, 1991; Bla
grove, 1992).
Emotions increased Intensified and predominated by fear-anxiety
Nielsen, Deslauriers, and Baylor, 1991; Merritt, Stickgold,
Pace-Schott, Williams, and Hobson, 1994; Domhoff, 1996).
Instinctual programs especially fight-flight) often incorporated
Hobson and McCarley, 1977; Hobson, 1988; Jouvet, 1999).
Volitional control greatly attenuated Hartmann, 1966; Purcell et
aI 1986).
Memory deficits across dream-wake, wake-dream and
dream-dream transitions Cipolli, Baroncini, Fagioli, Fumai,
and Salzaruo, 1987; Fagioli, Cipolli, and Tuozzi, 1989;
Goodenough, 1991; Roussy et aI 1996; Pace-Schott,
Stickgold, and Hobson, 1997a,b; Roussy, Gonthier, Raymond,
Mercier, and DeKoninck, 1997).
159
tures and documents their identification and quantifi
cation. Our discussion is based upon our
psychophysiological theory
of
brain-mind isomor
phism.
We
assume that any enhancement or impair
ment)
of
any psychological function e.g., dreaming)
will be mirrored by enhancement or impairment) of
its physiological substrate s function e.g., REM
sleep). We have emphasized these formal aspects of
dreaming because they are noted in all REM sleep
dreams regardless of their specific narrative content.
We expect that REM sleep neurobiology will be able
to explain more about such features than it now can
about specific dream content.
ream Motor Hallucinosis Fictive Movement
The nature of the motor hallucinations of dreams de
serves special comment because it suggests that brain
mechanisms subserving active motor behaviors are
brought into play during REM. Thus, even office
bound intellectuals never dream of what they do every
day: sitting at their desks reading, writing, or analyzing
data Hartmann, 1996). Instead they ski, swim, fly or
play tennis in their dreams whether or not they have
recently done any of these things in their waking lives.
In contrast to the deficits in memory functions dis
cussed below, REM sleep dream consciousness rou
tinely has
more
motor hallucinatory content than
NREM consciousness and perhaps even more than
most waking fantasy. In this case we must look for
what has been
added
to brain function in REM. We
might expect to find an enhancement of those physio
logical processes which subserve internal visuomotor
activation. We would then predict selective activation
of
the visual system, the basal ganglia, the motor cor
tex, or subcortical motor pattern generators. The neu
rophysiological studies and PET data from humans
confirm these predictions.
ream Emotion
Emotion is a subjective experience that is intensified
in dreams. To account for the documented prominence
of
anxiety-fear, elation, and anger in dreams Nielsen
et aI., 1991; Merritt et aI., 1994; DoIhhoff, 1996) we
would not be surprised to find selective activation of
the limbic brain and this is the prediction most strongly
supported by the new neuroimaging evidence Maquet
et aI., 1996; Braun et aI., 1997; Nofzinger et aI., 1997).
That dream emotion is usually consistent with the
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6
dream narrative Foulkes, Sullivan, Kerr, and Brown,
1988 and bizarre incongruities between emotion and
narrative are rarer than incongruities among other
dream elements Merritt et al., 1994 , can be explained
by viewing dream emotion as a primary shaper
of
plots
rather than as a reaction to them Seligman and Yellen,
1987 . Thus in a classic anxiety dream, the plot may
shift from feeling lost, to not having proper creden
tials, adequate equipment, or suitable clothing, to miss
ing a train. These plots all satisfy the driving
emotion nxiety while
being only very loosely as
sociated with one another.
Dream ognition
The distinctively discontinuous and incongruous na
ture of dream cognition can be measured
as
a construct
termed bizarreness Hobson, Hoffman, Helfand, and
Kostner, 1987; Hobson, 1988 . Bizarreness in turn re
flects the hyperassociative quality of REM sleep
dream consciousness. The instability of time, place,
and, most strikingly, person is a qualitatively unique
feature of REM sleep dreams. A dream character may
thus have the name of one
of
our friends but the wrong
face, hairstyle, or clothing. Other dream characters are
true chimeras having some
of
the features of one indi
vidual and some
of
another. Even the sexual identity
of
dream characters is fluid, and this ambiguity can
be anatomically explicit, not just psychological.
Dream mnesia and Related ognitive Deficits
The loss
of
memory in REM sleep makes dreaming
consciousness much more difficult to recall than wak
ing consciousness. This phenomenological deficit logi
cally implies a physiological deficit: some functional
process, present and responsible for memory in wak
ing, is absent or at least greatly diminished in REM
sleep.
In our attempt to explain dream amnesia, we look
with interest at such functional deficits as the loss
of
noradrenergic and serotonergic modulation in REM
sleep. This is because these very neuromodulators
have been shown, in many human and animal studies,
to be critical to learning and memory and to such
memory-enhancing cognitive functions as perception
and attention via their direct CNS effects
as
well as
their indirect peripheral mechanisms Kandel and
Schwartz, 1982; Quatermain, 1983; Frith, Dowdy,
Ferrier, and Crow, 1985; Clark, Geffen, and Geffen,
Allan Hobson
1987, 1989; Kandel, 1989; McGaugh, 1990, 1995;
Coull, Middleton, Sahakian, and Robbins, 1992;
Witte, Gordon-Lickey, and Marrocco, 1992; Robbins
and Everitt, 1994; Cahill, Prins, Weber, and
McGaugh, 1994; Abel et aI 1995 . This REM-related
aminergic demodulation is best viewed
as
a subtrac
tion of noradrenaline and serotonin from the varied
neuromodulatory mixture facilitating waking cogni
tion, a mixture which,
of
course, includes acetylcho
line e.g., Hasselmo and Bower, 1993 which remains
abundant during REM.
The loss of orientational stability which is at the
cognitive root of dream bizarreness and the loss of
self-reflective awareness which is the basis of the de
lusion that we are awake in our dreams are two re
lated deficits which could be caused by the aminergic
demodulation of the brain in REM sleep. But we have
wondered, is there more to it than that? Could the
frontal lobes be selectively inactivated during REM
sleep? At least two of the new PET studies reviewed
in a later section now suggest that this is so Maquet
et aI 1996; Braun et aI., 1997 .
REM Sleep Neurophysiology
In
1953, Eugene Aserinsky and Nathaniel Kleitman,
working in Chicago, discovered that the brian-mind
exhibited periodic self-activation during sleep. At reg
ular 90- to 100-minute intervals they observed the
spontaneous emergence of electroencephalographic
EEG desynchronization, accompanied by clusters of
rapid saccadic eye movements or REMs together
with acute accelerations of heart and respiration rates.
When subjects were awakened and asked to report
their antecedent mental activity, REM sleep was asso
ciated with longer, more vivid, more motorically ani
mated, and more bizarre accounts than NREM
Foulkes, 1962,1982,1985,1993; Rechtschaffen, Ver
done, and Wheaton, 1963; Goodenough, Lewis, Sha
piro, Jaret, and Sleser, 1965; Ogilvie, Hunt, Sawicki,
and Samahalski, 1982; Foulkes and Schmidt, 1983;
Antrobus, 1983; Hobson, 1990; Cavallero, Cicogna,
Natale, Occhionero, and Zito, 1992; Waterman, Elton,
and Kenemans, 1993; Stickgold, Pace-Schott, and
Hobson, 1994; Antrobus, Kondo, and Reinsel, 1995;
Casagrande, Violani, Lucidi, Buttinelli, and Bertini,
1996; Porte and Hobson, 1986; Kahn et aI 1997 .
Thus, while some dreaming can occur in other stages
of sleep Foulkes, 1962; Cavallero et aI 1992; for
reviews see Foulkes, 1967, 1985; Kahn et aI 1997;
Nielson, 1999 , it is REM neurophysiology which
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The
New Neuropsychology of Sleep
161
Structural
Model
Cholinergic R Sleep Generation
REM
- NE 5HT
NREM
ake
The reciprocal interaction hypothesis (McCarley
and Hobson, 1975) provided a formal model for the
aminergic-cholinergic interplay at the synaptic level
and a mathematical model
of
the dynamics
of
the neu
robiological control system (Figure
1 .
In this section
we review subsequent
work
that has led to the alter
ation and elaboration (Figure 2)
of
the model.
C Activation Level A
1
..Ir 4l
B Dynamic
Model
t> RIM..:.Q
REM On . /
-----
Although there is abundant evidence for a pontine per
ibrachial cholinergic mechanism
of
REM generation
centered in the pedunculopontine (PPT) and laterodor
sal tegmental (LDT) nuclei (for recent reviews see
Hobson, 1992; Hobson, Datta, Calvo, and Quattrochi,
Figure
1.
The Original Reciprocal Interaction Model
of
physiological
mechanisms determining alterations in activation level. (A)
Structural
model
of
Reciprocal Interaction
REM-on cells
of
the pontine reticular
formation are cholinoceptively excited and/or cholinergically excitatory
(ACH
at their synaptic endings. Pontine REM-off cells are noradrener
gically (NE)
or
serotonergically (5HT) inhibitory
-
at their synapses. (B)
Dynamic Model
During waking the pontine aminergic system is tonically
activated and inhibits the pontine cholinergic system. During NREM sleep
aminergic inhibition gradually wanes and cholinergic excitation recipro
cal ly waxes. At REM sleep onset aminergic inhibit ion is shut
off
and
cholinergic excitation reaches its high point. (C)
ctivation level
As a
consequence
of
the interplay
of
the neuronal sys tems shown in A and B,
the net activation level
of
the brain is at equally high levels in waking and
REM sleep and a t abou t hal f this peak level in NREM sleep (Hobson,
1992).
The Reciprocal Interaction Hypothesis
The discovery
of
the ubiquity
of
REM sleep in mam
mals provided the brain side of the brain-mind state
question with an animal model (Dement and Wolpert,
1958; Jouvet and Michel, 1959; Jouvet, 1962; Snyder,
1966; Dallaire, Toutain, and Ruckebusch, 1974).
While animal studies showed that potent and wide
spread activation
of
the brain did occur in REM sleep,
it soon became clear that Moruzzi and Magoun s
(1949) concept
of
a brainstem reticular activating sys
tem required extension and modification to account for
the differences between the behavioral and subjective
concomitants
of
waking and those of REM sleep
(Hobson and Brazier, 1981).
A conceptual breakthrough was made possible by
the discovery of the chemically specific neuromodula
tory subsystems
of
the brainstem (Dahlstrom and
Fuxe, 1964; for reviews see Foote, Bloom, and Aston
Jones, 1983; Hobson and Steriade, 1986; Jacobs and
Azmita, 1992) and
of
their differential activity in wak
ing (noradrenergic and serotonergic systems on,
cholinergic system damped) and REM sleep
(noradrenergic and serotonergic systems off, choliner
gic system undamped) (Trulson and Jacobs, 1970; Chu
and Bloom, 1973, 1974; Hobson, McCarley, and Wyz
inski, 1975; McCarley and Hobson, 1975; McGinty
and Harper, 1976; Cespuglio, Faridi, Gomez, and
Jouvet, 1981; Aston-Jones and Bloom, 1981; Lydic,
McCarley, and Hobson, 1983, 1987; Jacobs, 1986;
Rasmussen, Morilak, and Jacobs, 1986; Reiner, 1986;
Lydic, Baghdoyan, and Lorinc, 1987; Steriade and
McCarley, 1990).
The resulting model
of
reciprocal interaction
(McCarley and Hobson, 1975) provided a theoretical
framework for experimental interventions at the cellu
lar and molecular level that has vindicated the notion
that waking and dreaming are at opposite ends
of
an
aminergic-cholinergic neuromodulatory continuum,
with NREM sleep holding an intermediate position
(Figure 1). This spectrum
of
brain activity across the
states
of
waking, NREM, and REM must be the neuro
biological substrate of the conscious experience asso
ciated with these states. We now devote our careful
attention to a review
of
the cellular and molecular
level details, in the context
of
the reciprocal interac
tion concept, to provide a basis for our discussion of
the new human imagery data in a later section.
most strongly supports dream psychology (Kahn et aI.,
1997). For this reason, we restrict our integrative ef
forts to the neuropsychology
of
REM sleep dreaming.
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162
J. Allan Hobson
GABAergic nuclei
e.g.
substantia
nigra
pars
reticulat8
REM
Off REM On
B
Ach
+0:
1 i
5-HT 5.
:
----..., --- ----...-------,
Figure
2.
Synaptic Modifications
of
the Original Reciprocal Interaction
Model Based Upon Recent Findings. Reported data from animal (cat and
rodent) are shown as solid lines, some
of
the recently proposed putative dy
namic relationships are shown as dotted lines, and
references are indicated
by numbers see key below .
The
exponential magnification
of
cholinergic
output predictedby theoriginalmodel (Figure 1)
can
alsooccur in this model
with mutuallyexcitatory cholinergic-non-cholinergic interactions (7) taking
the place of the previously postulated, mutually excitatory cholinergic-cho
linergic interactions. Therefore the basic shape
of
reciprocal interaction s
dynamic model (illustrated in Figure
IB)
and its reluctant alternation
of
be
havioral state (illustrated in Figure 1C) would also result from this revised
model. The additional synaptic details
can
be superimposed
on
this revised
reciprocal interaction model without altering the basic effects
of
aminergic
and cholinergic influences on the REM sleep cycle.
For
example: i. Excit
atory cholinergic-non-cholinergic interactions utilizing ACh and the excit
atory amino acid transmitters enhance firing
of
REM
-on cel ls (6, 7) whi le
inhibitory noradrenergic (4), serotonergic (3) and autoreceptor cholinergic
(1) interactions suppress REM-on cells.
Cholinergic effects upon aminer
gic neurons are bothexcitatory (2), as hypothesized in the originalreciprocal
interactionmodel andmay also operate via presynaptic influences
on
norad
renergic-serotonergic as well as serotonergic-serotonergic circuits (8).
Inhibitory cholinergic autoreceptors (1)could contributeto the inhibition of
LOT
and
PPT
cholinergic neurons whichis also causedby noradrenergic (4)
and serotonergic (3) inputs.
iv.
GABAergic influences(9, 10) as well asother
neurotransmitters suchas adenosine and nitric oxide (see text) maycontrib
ute to the modulation
of
these interactions.
Abbreviations:
open circles, ex
citatory postsynaptic potentials; closed circles, inhibitory postsynaptic
potentials; mPRF, medial pontine reticular formation; PPT, pedunculopon
tine tegmental nucleus; LOT, laterodorsal tegmental nucleus; LCa, peri-lo
cus coeruleus alpha; 5HT, serotonin; NE, norepinephrine; ACh,
acetylcholine; GL, glutamate; AS, aspartate; GABA, gamma-aminobutyric
acid.
References:
1. Baghdoyan, Fleegal, Lydic, 1997; EI Manseri, Sa
kai,
Jouvet, 1990; Kodama
Honda, 1996;Leonard
Llinas, 1990, 1994;
Luebke, McCarley, Greene, 1993; Roth, Fleegal, Lydic, Bagndoyan,
1996; Sakai
Koyama, 1996; Sakai, EIManseri,
Jouvet, 1990. 2. Egan
North, 1985, 1986.3. Horner,Sanford,Annis, Pack, Morrison, 1997;Leo
nard Llinas, 1994; Luebke, Green, Semba, Kamodi, McCarley, Reiner,
1992; Thakkar, Strecker,
McCarley, 1997. 4. Sakai,
Koyama, 1996.
5. Portas, Thakkar, Rannie,
McCarley, 1996. 6. Sakai
Koyama, 1996;
Sakai Onoe, 1997; Vanni-Mercier, Sakai, Lin, 1989; Yamamoto, Ma
melak, Quattrochi,
Hobson, 1990a, b. 7. Greene
McCarley, 1990; Leo
nard Llinas, 1994; Sakai Koyama, 1996. 8. Li, Greene, Rannie,
McCarley, 1997. 9. Nitz Siegel, 1997; Datta, 1997b; Datta, Curro-Dossi,
Pare, Oakson, Steriade, 1991. 10. Porkka-Heiskanen, Strecker, Stenberg,
Bjorkum, McCarley, 1997a.
GA A
locus
Ach
t
coeruleus
2.
Experimental REM Sleep Induction and Suppression
Microinjection of cholinergic agonist or cholinesterase
inhibitors into many areas of the paramedian pontine
reticular formation induces REM sleep (Baghdoyan,
1993; Datta, 1995, 1997a; McCarley, Greene, Rannie,
and Portas, 1995; McCarley et aI., 1997), not all pon
tine PPT and LDT neurons are cholinergic (Steriade
et aI., 1988; Leonard and Llinas, 1990, 1994; Kang
and Kitai, 1990; Kamondi, Williams, Hutcheson, and
Reiner, 1992; Sakai and Koyama, 1996) and cortical
acetylcholine release may be as high during wake
fulness as during sleep (Jasper and Tessier, 1971; Mar
rosu et aI., 1995; Jimenez-Capdeville and Dykes,
1996).
The original claim, that themedial pontine reticu
lar formation (mPRF) was cholinergic, was clearly in
error. While many
of
the mPRF cells are excited by
acetylcholine as originally hypothesized, their own ex
citatory neurotransmitter now appears to be glutamate,
not acetylcholine. For this and other reasons to be
discussed below, reciprocal interaction (McCarley and
Hobson, 1975) and reciprocal inhibition (Sakai, 1988)
models for control of the REM sleep cycle by brain
stem cholinergic and aminergic neurons have recently
been questioned (Leonard and Llinas, 1994). Specifi
cally, the self-stimulatory role of acetylcholine on
pontine PGO-bursting neurons has not been confirmed
in in vitro slice preparations (Leonard and Llinas,
1995). For example, ACh has been shown to hyperpo
larize cell membranes in slice preparations
of
the ro
dent parabrachial nucleus (Egan and North, 1986)
LDT (Luebke, McCarley, and Greene, 1993; Leonard
and Llinas, 1994) and PPT (Leonard and Llinas,
1994). Similarly, LDT and PPT neurons with burst
discharge properties most like those hypothesized to
occur in PGO-burst neurons ( type I neurons) may
not be cholinergic (Leonard and Llinas, 1990).
Much evidence remains, however, that the recip
rocal interaction model accurately describes essential
elements of REM sleep cycle control even though
some
of
its detailed synaptic assumptions need correc
tion, as shown in Figure 2. Numerous findings confirm
the hypothesis that cholinergic mechanisms are essen
tial to the generation
of
REM sleep and its physiologi
cal signs (for recent reviews see Hobson, Lydic, and
Baghdoyan, 1986; Hobson and Steriade, 1986; Sakai,
1988; Steriade andMcCarley, 1990; Jones, 1991; Hob
on, 1992b; Hobson et aI., 1993; Datta, 1995, 1997).
A selection of many recent examples follows.
mesopontine
tegmentum
1
7. GL.
;1 _ 7. Ach
cholinergic non-cholinergic
PPT
and LOT mPRF and Lea
- Ach +OAch - NE
~ 1 . ~
6. 4.
5-HT
3.
raphe
NE+Q 0
B +Ach
B
GABA
i
14
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The New Neuropsychology Sleep
Rodrigo-Angulo, McCarley, and Hobson, 1987; Bagh
doyan, Lydic, Callaway, and Hobson,
1989;
Vanni
Mercier, Sakai, and Lynn, 1989; Velazquez-Moctez
uma, Gillin, and Shiromani, 1989; Yamamoto, Ma
melak, Quattrochi, and Hobson, 1990a,b; Hobson et
aI 1993 . In addition to these short-term REM induc
tion sites, carbachol injection into a pontine site in the
caudal peribrachial area has been shown to induce
long-term over seven days REM enhancement
Calvo, Datta, Quattrochi, and Hobson, 1992; Datta,
Calvo, Quattrochi, and Hobson, 1992; Datta, Quat
trochi, and Hobson, 1993 . In rats, it has been difficult
to enhance REM sleep with carbachol Deurveiller,
Hans, and Hennevin, 1997 , but rat strains which are
genetically supersensitive to ACh show enhanced
REM sleep Benca et. aI., 1996 . In addition to the
well-known suppression
REM by muscarinic antag
onists Hobson et aI., 1986 , the new presynaptic anti
cholinergic agents have also been shown
to
block
REM Salin-Pascual and Jimenez-Anguiano, 1995;
Capece, Efange, and Lydic, 1997 .
holinergic Neurons and
R
Sleep
Cholinergic type II and III PPT and LDT neurons
have firing properties which make them well suited
for the tonic maintenance
REM Leonard and Lli
nas, 1990 , and both PPT and LDT neurons show spe
cifically c-fos and foslike immunoreactivity Fos-LI
following carbachol-induced REM sleep Shiromani,
Malik, Winston, and McCarley, 1995; Shiromani,
Winston, and McCarley, 1996 suggesting that they
participate in the genesis that state. Low amplitude
electrical stimulation the LDT enhances subsequent
REM sleep Thakkar, Portas, and McCarley, 1996
while electrical stimulation of the cholinergic LDT
evokes excitatory postsynaptic potentials in pontine
reticular formation neurons and these EPSPs can be
blocked by scopolamine Imon, Ito, Dauphin, and
McCarley, 1996 . The excitatory amino acid, gluta
mate, when microinjected into the cholinergic PPT,
increases REM sleep in a dose-dependent manner
Datta, 1997b; Datta and Siwek, 1997 .
cetylcholine Release and R sleep
Microdialysis studies show enhanced release
en
dogenous acetylcholine in the medial pontine reticular
formation during both natural Kodama, Takahashi,
andHonda, 1990 and carbachol-induced Lydic, Bagh-
163
doyan, and Lorine, 1991 REM sleep. Thalamic ACh
concentration mesopontine origin is higher in both
wake and REM than in NREM Williams, Comisarow,
Day, Fibiger, and Reiner, 1994 , and a REM-specific
increase
ACh in the lateral geniculate body has
been observed Kodama and Honda, 1996 . Both mus
carinic and nicotinic receptors participate in the depo
larization thalamic nuclei by the cholinergic
brainstem Curro-Dossi, Pare, and Steriade, 1991 .
holinergic Mediation of PGO Waves
PGO input to the LGB is cholinergic Steriade, Pare,
Parent, and Smith, 1988 , and can be antidromically
traced to pontine PGO-burst neurons Sakai and
Jouvet, 1980 . Stimulation
mesopontine neurons in
duces depolarization cortically projecting thalamic
neurons Curro-Dossi et
aI
1991 . Neurotoxic lesions
pontomesencephalic cholinergic neurons reduce the
rate PGO spiking Webster and Jones, 1988 and
PGO wavescan be blocked by cholinergic antagonists
Hu, Bouhassira, Steriade, and Deschenes, 1988 . It
may not be an exaggeration to state that the evidence
for cholinergic REM-sleep generation is now
so
over
whelming and so widely accepted that this tenet the
reciprocal interaction model is an established prin
ciple.
minergic Inhibition of the holinergic R
Generator
At the heart the reciprocal interaction concept is
the idea that cholinergic REM sleep generation can
only occur when the noradrenergic and serotonergic
mediators waking release their inhibitory constraint
the cholinergic generator. The evidence for inhibi
tory serotonergic and noradrenergic influences on cho
linergic neurons and REM sleep is now also quite
strong.
Decreased Serotonin Release in Natural
R
Sleep
In the cat, extracellular levels
serotonin are higher
in waking than in NREM and higher in NREM than
REM in the dorsal raphe Portas and McCarley, 1994
and the medial pontine reticular formation Iwakiri,
Matsuyama, and Mori, 1993 . This same state-depen
dent pattern is observed in the hypothalamus the rat
Auerbach, Minznberg, and Wilkinson, 1989; Imeri,
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164
DeSimoni, Giglio, Clavenna, and Mancia, 1994).
Moreover, reduced extracellular serotonin concentra
tion in REM sleep has recently been demonstrated in
the human amygdala, hippocampus, orbitofrontal cor
tex and cingulate cortex Wilson et aI., 1997). Since
most of these structures show selective activation in
PET images of REM sleep, it can be inferred that the
human limbic system is turned on but demodulated
during dreaming.
Serotonergic Suppression of holinergic Systems and
R Sleep
Serotonergic neurons from the dorsal raphe have been
shown to synapse o n LDT and PPT neurons Honda
and Semba, 1994). Serotonin has been shown to hy
perpolarize rat cholinergic LDT cells in vitro Luebke
et aI., 1992; Leonard and Llinas, 1994) and to reduce
the proportion
of
REM sleep in vivo Horner, Sanford,
Annis, Pack, and Morrison, 1997). Serotonin has been
shown to counteract the REM-like carbachol-induced
atonia
of
hypoglossal motoneurons Kubin, Reignier,
et aI., 1994; Kubin, Tojima, Reignier, Pack, and Da
vies, 1996; Okabe and Kubin, 1997).
Suppression of
R
by Serotonin gonists
Microinjection
of
the serotonin agonist 8-0H-DPAT
into the peribrachial region impedes REM initiation
in cats Sanford et aI., 1994) and systemic injection
of
8-0H-DPAT into serotonin-depleted rats also sup
presses REM Monti et aI., 1994). Simultaneous unit
recording has shown that microinjection of 8 0H-
DPAT selectively suppressed the firing
of
REM-on
but not REM-and wake-on cells
of
the cholinergic
LDT and PPT Thakkar et aI., 1997). In vivo microdia
lysis of serotonin agonists into the dorsal raphe nu
cleus DRN) decreased DRN levels
of
serotonin
presumably via serotonin autoreceptors on DRN
cells) which in turn increased REM sleep percent Por
tas, Thakkar, Rainnie, and McCarley, 1996). Meso
pontine injection of a serotonin agonist depressed ACh
release in the lateral geniculate body Kodama and
Honda, 1996).
Suppression
of
R by Endogenous Norepinephrine
and its gonists
Locus coeruleus neurons have been shown to become
quiescent during REM in the monkey Rajkowski, Si-
J. Allan Hobson
lakov, Ivanova, and Aston-Jones, 1997) as well as in
the cat and rat Hobson and Steriade, 1986). Electrical
stimulation of the pons in the vicinity of the noradren
ergic) locus coeruleus reduced REM sleep in rats
Singh and Mallick, 1996). The alpha-2 noradrenergic
agonist clonidine suppresses REM in human subjects
Nicholson and Pascoe, 1991; Gentili etaI.,
1996) and
the cat Tononi, Pompeiano, and Cirelli, 1991) while
the noradrenergic antagonist idazoxan increases REM
when injected into the pontine reticular formation
of
cats Bier and McCarley, 1994). That the REM-sup
pressive effects
of
serotonin and norepinephrine are
additive is indicated by the suppression of REM sleep
in humans by acute dosage
of
antidepressant drugs
which inhibit the reuptake
of
serotonin, norepineph
rine, or both Vogel, 1975; Nicholson, Belyavin, and
Pascoe, 1989; Vogel, Buffenstein, Minter, and Hen
nessy, 1990).
Like cholinergic enhancement, aminergic sup
pression of REM sleep is now an established principle.
The 5-HT
1A
serotonin receptor may be of the greatest
importance in the inhibition
of
cholinergic firing in
the cat PPT Sanford et aI., 1994) and LDT Sanford
et aI., 1997) while the alpha-l receptor may be the
most important site for adrenergic REM suppression
Ross, Gresch, Ball, Sanford, and Morrison, 1995).
Modification
of
the Reciprocal Interaction Model
Modifications of simple reciprocal inhibition or inter
action models, which are consonant with recent find
ings, have been proposed for the brainstem control
of
REM sleep. All such modifications retain one or both
of the major tenets
of
the reciprocal interaction model:
cholinergic facilitation and adrenergic inhibition
of
REM.
Leonard and Llinas 1994) suggest in regard
to
the McCarley and Hobson 1975) model that indi
rect feedback excitation via cholinergic inhibition of
an inhibitory input or cholinergic excitation
of
an ex
citatory input or some combination
of
the two could
replace direct feedback excitation in their
model p.
327). A similar mutually excitatory or mutually inhibi
tory interaction between REM-on cholinergic and
REM-on noncholinergic mesopontine neurons has
also been proposed Sakai and Koyama, 1996). Such
a mechanism is depicted in Figure 2.
From recent in vitro studies in the rat, the follow
ing elaboration of reciprocal interaction has been pro
posed by
Li
et
ai.
in the McCarley laboratory Li et
aI., 1997). During waking, presynaptic nicotinic facili-
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The
New Neuropsychology
of
Sleep
tation
of
excitatory locus coeruleus noradrenergic in
puts to the dorsal raphe enhances serotonergic firing.
During REM, when the locus coeruleus is silent, this
same presynaptic nicotinic input may facilitate sero
tonergic self-inhibition by the raphe neurons them
selves. In vivo microdialysis studies
of
GABA in the
cat further postulate selective suppression of norad
renergic locus coeruleus neurons by GABAergic inhi
bition during REM as
proposed by Nitz and Siegel
1997 .
It is important to realize that many of the studies
questioning reciprocal interaction Egan and North,
1986; Leonard and Llinas, 1990, 1994; Luebke et aI.,
1992 have been carried out on in vitro rodent models.
Exploring the relationship of these findings
to
the in
vivo mechanisms generating REM sleep signs in the
cat is only in its early stages Hobson et aI 1993;
Datta, 1995; Sakai and Koyama, 1996 . It seems possi
ble, for example, that the hyperpolarization by ACh
of cholinergic cells cited in these studies might be
explained by the presence
of
ACh autoreceptors which
contribute to homeostatic control of cholinergic activ
ity Leonard and Llinas, 1990, 1994; EI Manseri et
aI 1990; Sakai et aI 1990; Sakai and Koyama, 1996;
Kodama and Honda, 1996; Roth et
aI
1996; Bagh
doyan et aI., 1997 . In contrast to the hyperpolariza
tion
of
some mesopontine cholinergic neurons
by
cho
linergic agonists, in vitro studies have shown the
majority of medial pontine reticular formation
mPRF neurons to be depolarized by carbachol
Greene and McCarley, 1990 . This suggests that the
exponential self-stimulatory activation which can be
triggered by cholinergic stimulation in diverse meso
and medial pontine sites Hobson and Steriade, 1986;
Hobson et aI., 1986, 1993; Steriade and McCarley,
1990 may involve excitatory neurons which are non
cholinergic. Such cholinergic self-regulation com
bined with cholinergic-noncholinergic mutual
excitation is schematized in Figure
2
We conclude that the two central ideas
of
the
model are strongly supported by subsequent research:
1 noradrenergic and serotonergic influences enhance
waking and impede REM via anticholinergic mecha
nisms; 2 cholinergic mechanisms are essential to
REM sleep and come into full play only when the
serotonergic and noradrenergic systems are inhibited.
By restricting our discussion to cholinergic and
aminergic mechanisms, we do not exclude the contri
butions to the modulation
of
behavioral state of other
neuromodulatory systems such
as
GABAergic systems
Nitz and Siegel, 1997 ; nitroxergic systems Leonard
and Lydic, 1997 ; glutamatergic systems Qnoe and
165
Sakai, 1995 ; glycinergic systems Chase, Soja, and
Morales, 1989 ; histaminergic systems Saper, Sherin,
and Elmquist, 1997 ; adenosinergic systems McCar
ley et aI., 1997 ; or the neuropeptides Bourgin et aI.,
1997 . Nor do we exclude the contributions
of
numer
ous nonpontine structures such as the basal forebrain
Szymusiak, 1995 ; hypothalamus Saper et aI 1997 ;
the amygdala Sanford, Ross, Tejani-Butt, and Mor
rison, 1995 ; thalamic nuclei Mancia and Marini,
1997 ; central gray area Sastre, Buda, Kitahama, and
Jouvet, 1996 ; or the medulla Chase and Morales,
1990 . These other systems are reviewed elsewhere
Kahn et aI., 1997; Hobson, Pace-Schott, and
Stickgold, 2000 . Rather, we emphasize here those
aminergic and cholinergic mechanisms associated
with the executive control of REM sleep in reciprocal
interaction/inhibition models McCarley and Hobson,
1975; Sakai, 1988; Steriade and McCarley, 1990 .
While the studies we have reviewed here are nec
essarily restricted to data obtained in subhuman
models
of
REM sleep, an abundant psychopharmaco
logical literature provides indirect evidence that the
same mechanisms operate at the cellular and molecu
lar level in the human brain Sitaram, Wyatt, Dawson,
and Gillin, 1976; Sitaram, Moore, and Gillin, 1978a,b;
Hobson and Steriade, 1986; Nicholson et aI 1989;
Vogel et aI., 1990; Gillin, Sutton, and Ruiz, 1991;
Perry and Perry, 1995 . We now turn our attention to
new, more direct evidence supporting the assumptions
of cross-species homology.
um n Neuropsychology
Until recently, the experimental study of human REM
sleep dreaming has been limited on the physiological
side by the poor resolving power
of
the EEG. Even
expensive and cumbersome evoked-potential and
computer-averaging approaches have not helped to an
alyze and compare REM-sleep physiology with that
of waking in an effective way. This limitation has
probably reinforced the erroneous idea that the brain
activation picture
of
REM sleep and waking are identi
calor
at least, very similar.
Fortunately, technological advances in the field
of human brain imaging have now made it possible to
describe a highly selective regional activation pattern
of
the brain in REM sleep. At the same time, experi
ments
of
nature, in the form
of
strokes, have allowed
the locale
of
brain lesions to be correlated with deficits
or accentuations of dream experience in patients Dor
icchi and Violani, 1993; Solms, 1997 . The remark-
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66
J. Allan Hobson
KEY: 1Increase; 1Decrease; - No Change.
P T maging Studies
of
R Sleep reaming
ably complementary results
of
these two approaches
are summarized in Table
2
TABLE 2
Imaging
of
Brain Activation in REM
nd
the Effects of Brain
Lesions on Dreaming
to be important for spatial imagery construction, an
important aspect
of
dream cognition. As Maquet (Ma
quet and Franck, 1997) emphasizes, those cortical ar
eas activated in REM are rich in afferentation from
the amygdala (anterior cingulate, right parietal opercu
lum) while those areas with sparse amygdalar affer
entation (prefrontal cortex, parietal cortex, and
precuneus) were deactivated in REM. Maquet et al.
interpreted their data in terms of the selective pro
cessing, in REM, of emotionally influenced memories
(see also Braun et aI., 1997; Maquet and Franck,
1997).
In another H
2
5
0 PET study, Braun et
aI
(1997)
replicated the Maquet group s findings
of
a consistent
REM-related brainstem, limbic, and paralimbic activa
tion. When REM-sleep brain activity was compared
to brain activity in delta NREM, with presleep waking
and with postsleep waking, Braun et
aI
showed rela
tive activation
of
the pons, the midbrain, the anterior
hypothalamus, the hippocampus, the caudate, and the
medial prefrontal, caudal orbital, anterior cingulate,
parahippocampal, and inferior temporal cortices in
REM sleep as compared to each of the above three
conditions (Table 3). Based on these observations, the
Braun group offered the following speculations which
are relevant
to
the neurology of dreaming.
The ascending reticular activation of REM
sleep may proceed relatively more via a ventral cholin
ergic route from the brainstem through the basal fore
brain rather than via the dorsal route through the
thalamus which is preferred in waking.
2
The activation of the cerebellar vermis in
REM sleep may reflect an input from the brainstem
vestibular nuclei and thus constitute a source of neu
ronal activation causing fictive movement in dreams
(Leslie and Ogilvie, 1996; Hobson, Stickgold, Pace
Schott, and Leslie, 1997).
3
The strong REM sleep-related activation of
the
basal ganglia
suggests that these subcortical struc
tures may play an important role in ascending thala
mocortical activation. The mediating network links
brainstemto the basal ganglia via the intralaminar thal
amic nuclei and proceeds to the cortext via the ventral
anterior and ventromedial thalamic nuclei. Because
this network contains multiple regulatory back projec
tions to the pedunculopontine tegmentum, a possible
role for the basal ganglia in the rostral transmission
of
PGO waves is suggested. The basal ganglia may
initiate motor activity and be related to the ubiquity
of hallucinated motion in dreams (Hobson, 1988;
Porte and Hobson, 1996).
(right)
PET Studies of Lesions Studies of
Activation in REM Effects on
Dreaming
REGION
Pontine Tegmentum
Limbic Structures
Striate Cortex
Extrastriate Cortex
Parietal Operculum
Dorsolateral Prefrontal
Cortex
Mediobasal FrontalCortex
Two very recent and entirely dependent PET studies
confirm the importance
of
the pontine brainstem in
the REM sleep activation of the human brain (Braun
et aI., 1997; Maquet et aI., 1996). This is an important
advance because it validates, for the first time, the
experimental animal data on the critical and specific
role of the pontine brainstem in REM-sleep genera
tion. At the same time these new studies also provide
important new data for our understanding
of
dream
synthesis by the forebrain. Instead
of
the global, re
gionally nonspecific picture of forebrain activation
that had been suggested by EEG studies, all of these
new imaging studies indicate a preferential activation
of limbic and paralimbic regions of the forebrain in
REM sleep compared to waking or to NREM sleep
(Braun et aI., 1997, Maquet et aI., 1996; Nofzinger et
aI., 1997). One important implication
of these discov
eries is that dream emotion may be a primary shaper
of dream plots rather than playing the secondary role
in dream plot instigation that was previously hypothe
sized (Hobson and McCarley, 1977).
Maquet et
aI
(1996) used an H
2
5
0 positron
source to study REM-sleep activation in their subjects
who were subsequently awakened for the solicitation
of dream reports. In addition to the pontine tegmen
tum, significant activation was seen in both amygdalae
and the anterior cingulate cortex (Table 3). Signifi
cantly, despite the general deactivation in much of the
parietal cortex, Maquet et
aI
reported activation of
the right parietal
operculum
brain region thought
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The New Neuropsychology of Sleep
167
TABLE 3
Subcortical and Cortical Regional
Brain
Activation
and
Deactivation Revealed by Recent PET Studies
Comparing
REM Sleep
with Waking
and
with NREM Sleep
Comparison
REM vs. all other stages REM vs. waking
REM vs. pre- ( post-*) REM vs. NREM 3 4
sleep waking
Study
Maquet et aI., 1996 Nofzinger et aI., 1997 Braun et aI., 1997 Braun et aI., 1997
Technique H
2
0
18PDG
H
2
0
H
2
0
Subcortical Areas
Brainstem
Pontine tegmentum
increase
increase (R
increase
Midbrain
increase*
increase
Dorsal mesencephalon
increase
Diencephalon
Thalamus
increase: L
increase
Hypothalamus
increase: R, Lat
increase: A-POA
increase: A-POA
Limbic system
Left amygdala
increase
increase
Right amygdala
increase
Septal nuclei
increase
Hippocampus
increase*
increase
Basal ganglia striatum
Caudate
increase: A, I, L increase*
increase
Putamen
increase
Ventral striatum (n. ac-
increase
increase
cumbens, sub.innominata)
Cerebellum
increase
increase
(vermis)*
(vermis)
Cortical Areas
Frontal
Dorsolateral Prefrontal
decrease:
increase
decrease: 46*
L: 10, 46 47
R: 8, 9, 10, 11, 46
Opercular
decrease: 45*
Paraolfactory
increase
Lateral orbital
increase: 11, 12
decrease: 11 *
Caudal orbital
increase
increase
Gyrus rectus
increase
Parietal
Brodmann area 40
increase: R A 40
decrease: 40*
(supramarginal gyrus)
decrease: L 40
Angular gyrus
decrease: 39*
Precuneus
decrease
Temporal
Middle
increase R
Posterior superior
increase: 22
Inferior fusiform
increase: 37, 19 increase: 37, 19
(postsleep only)
Occipital
Postrolandic sensory
increase
Limbic ssociated
Medial (prelimbic) prefrontal
increase: R 32
increase: 10
increase: 10
Anterior cingulate
increase: 24
increase: 24
increase: 32*
increase: 32
Posterior cingulate
decrease: 31
dec: R sm. areas
decrease*
Infralimbic
increase: 25
Insula
increase: L
decrease-P
increase: A I
Parahippocampal
increase
increase: 37*
increase: 37
Entorhinal
increase
inc. (in fusiform)
Temporal pole
increase: 38
Abbr: L-Ieft h ~ m i s p h r R-right hemisphere; A-anterior; P-posterior; C-caudal; M-medial; Lat.-lateral; I-inferior; S-superior; A-POA anterior preoptic area; all numerals
Brodmann s area
*Change relative to both pre- and postsleep waking (Braun et
aI. , 1997
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68
4
The REM-associated activation
of
unimodal
associative visual (Brodmann areas 19 and 37) and
auditory (Brodmann area 22) cortex contrasts with the
maintained (NREM and REM) sleep-related deactiva
tion
of
heteromodal association areas in the frontal and
parietal cortices. Interestingly, the inferior temporal
cortex (Brodmann areas 19 and 37) contains the fusi
form gyrus, a structure known to
be
involved in human
face recognition (McCarthy, Puce, Gore, and Truett,
1997) another common,
if
often bizarrely uncertain,
dream feature.
5
The REM-associated increase in activation
of
the
limbic associated medial prefrontal area
contrasts
with the prominent decrease in the executive portions
of
the frontal cortex (dorsolateral and orbital prefron
tal cortices). This medial area, which has the most
abundant limbic connections in the prefrontal cortex,
has been associated with arousal and attention. Disrup
tion of this area has been shown to cause confabula
tory syndromes formally similar to dreaming (Braun et
aI., 1997). Interestingly, lesions
of
the anterior limbic
cortex, especially the neighboring anterior cingulate,
often result in a distinctive syndrome in which dream
ing increases in vivacity and reality and dreaming be
come confused (Solms, 1997). From these findings as
well as primary visual cortex deactivat ion in REM,
the Braun group has recently suggested that REM con
stitutes, in the cortex, a unique condition
of
internal
information processing (between extrastriate and lim
bic cortices) functionally isolated from input (via stri
ate cortex) or output (via frontal cortex) to the external
world (Braun et aI., 1998).
Confirming the widespread limbic activation of
the human brain in REM, Nofzinger et
aI
(1997) de
scribed increased glucose utilization in the lateral hy
pothalamic area and the amygdaloid complex using an
I8F-fluoro-deoxyglucose (FDG) PET technique (Table
3). Nofzinger et
aI
note that,
The
largest area
of
activat ion is a bilateral confluent paramedian zone
which extends from the septal area into ventral stria
tum, infralimbic, prelimbic, orbitofrontal and anterior
cingulate
cortex
(p. 192). The authors suggest that
an important function
of
REM sleep is the integration
of
neocortical function with basal forebrain hypothala
mic motivational and reward mechanisms.
An equally interesting H
Q
PET finding, rele
vant to the cognitive deficits in self-reflective aware
ness, orientation, and memory during dreaming was
significant
deactivation
in REM,
of
a vast area
of
dorsolateral prefrontal cortex (Maquet et aI., 1996;
Braun et al., 1997). Using SPECT, a similar decrease
in cerebral blood flow to frontal areas during REM
J. Allan
Hobson
had earlier been noted (Madsen et aI., 1991). This dor
solateral prefrontal deactivation during REM, how
ever, was not replicated by the Nofzinger et
aI
FDG
study and this discrepancy remains to be clarified. U
s-
ing the finer time-resolution offered by functional MRI
(fMRI) imaging (Huang-Hellinger et aI., 1995; Ives et
aI., 1997; Sutton et aI., 1997) this area of research can
be expected to provide more detail in the near future.
The fact that considerable portions
of
executive
and association cortex are far less active in REM than
in waking led Braun et
aI
(1997) to speculate that
R M
sleep may constitute a state
of
generalized
brain activity with the specific exclusion
of
executive
systems which normally participate in the highest or
der analysis and integration
of
neural information
(p. 1190). In terms
of
cortical-subcortical networks,
Braun et aI suggest further that
the
limbic loop
connecting ventral striatum, anterior thalamus and
paralimbic cortices, appear to be activated during
REM sleep However, the prefrontal or associa
tion loop, connecting the caudate, dorsomedial thala
mus and prefrontal cortices
appears to be activated
only in a partial
or
fragmentary
way
(p. 1191). Fig
ure 3 integrates findings from these first three PET
studies comparing REM sleep to other states.
Loss Dreaming fter Cerebral Lesions
An entirely complementary set
of
findings and conclu
sions has been reached following a neuropsychological
survey of 332 clinical cases with cerebral lesions
(Solms, 1997). The 112 patients who reported a
global cessation
of
dreaming had damage either in
the parietal convexity or suffered disconnections
of
the mediobasal frontal cortex from the brainstem and
diencephalic limbic regions. Solms, who was appar
ently unaware
of
the recent PET studies, cited the
much earlier single subject report
of
a PET glucose
activation of limbic and prelimbic structures in REM
(Heiss, Pawlik, Herholz, Wagner, and Wienhard,
1985). With respect to the visual imagery aspect, a
decrease in the vivacity
of
dreaming was reported
by two patients with damage to the seat
of
normal
vision in the medial-occipital-temporal cortex (espe
cially areas V
3
,
V
3a
,
and V
4
but not VI, V
s
or V
6
Solms (1997) also-reports that his patients with pon
tine lesions continued to dream and concludes that the
pons is not necessary for human dreaming. Based
upon the difficulty
of
suppressing REM by experimen
tal lesions
of
the pons in animals, we suggest an alter
native explanation. It seems to us that any lesion
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Th e
New Neuropsychology
of
Sleep
Dorsolateral
Prefrontal
ortex
ctivated in R
Deactivated
in R
Figure 3. Convergent Findings
on
Relative Regional Brain Activation and
Deactivation in REM Compared to Waking. A schematic sagittal view
of
the human brain showing those areas of relative activation and deactivation
in REM sleep compared to waking and/or NREM sleep which were re
ported in
two or more
of the three PET studies published to date (Maquet
et aI., 1996; Braun et aI., 1997; Nofzinger et aI., 1997). Only those areas
which could be easily matched between two or more studies are schemati
cally illustrated here and a realistic morphology of the depicted areas is
not implied. Note that considerably more extensive areas of activation are
reported in the individual studies and these more detailed findings are
given in Table 3. The depicted areas in this figure are thus most realistically
viewed as representative portions of large eN S areas subserving similar
functions (e.g., limbic-related cortex, ascending activation pathways and
multimodal association cortex).
capable of destroying the pontine REM sleep genera
tor mechanism would have to be
so
extensive as to
eliminate consciousness altogether.
motionally Salient emory Processing
Concerning the functional significance of the imaging
results, all three
of
the image study authors assign
REM sleep a role in the processing of emotion in mem
ory systems (Maquet et aI., 1996; Braun et aI. 1997;
Nofzinger et aI., 1997; Maquet and Franck, 1997). Ad
ditionally, both the Maquet and Braun groups suggest
the possible origin
of
dream emotionality in REM
associated limbic activation and dream-associated ex
ecutive deficiencies in REM-associated frontal deacti
vation (Braun et aI., 1997; Maquet and Franck, 1997).
Additional findings support this proposed cortico-lim
bic interaction. First,
as
shown in Table 3 the cingu
late cortex has consistently shown increased activation
in REM in other PET studies (Buchsbaumet
aI.
1989).
Second, FDG PET activation of anterior medial struc
tures, including the anterior cingulate and medial fron
tal cortex, was found to correlate with REM density
in the REM period during which FDG uptake occurred
169
(Hong, Gillin, Dow, Wu, and Buchsbaum, 1995). Al
though these authors interpret this medial activity cor
relation with REM density
as
resulting from the
activity
of
midline attentional systems in response to
cortically generated dream imagery (Hong et aI.
1995), it is equally possible that activation
of
these
structures reflects the limbic and paralimbic activity in
REM suggested by the Nofzinger, Maquet, and Braun
studies (Maquet et aI., 1996; Braun et aI., 1997; Nof
zinger et aI. 1997). Finally, a recent study
of
human
limbic structures with depth electrodes has shown that
a distinctive rhythmic delta-frequency EEG pattern
occurs only during REM sleep (Mann, Simmons, Wil
son, Engel, and Bragin, 1997).
The regional activation during REM may reflect
a specific activation
of
subcortical, and cortical, limbic
structures for the adaptive processing of emotional and
motivational learning (Maquet et aI. 1996; Nofzinger
et aI. 1997). Such processing may, in turn, account
for the emotionality and psychological salience of
REM sleep dreams (Hobson, 1988; Braun et aI. 1997).
Some support for this comes from a PET (glucose)
study showing correlation between content-analyzed
dream anxiety and medial frontal activation
(Gottschalk et
aI.
1991).
reud sDream Theory Revised in the Light of
Modern Sleep
an d
Dream Research
There are five basic tenets to Freud s disguise--eensor
ship dream theory which can now be contrasted with
aspects of the activation-synthesis hypothesis.
The instigation
dreaming was, for Freud,
caused by the upsurge
of
unconscious wishes follow
ing suspension of their wake-state repression. We
would now say that dreaming is caused by brain acti
vation during sleep. In NREM sleep, residual brain
activation is at a low level hence dreaming is less
intense and less sustained, whereas in REM the brain
activation is
as
vigorous as that in waking but that
activation is both biochemically and regionally differ
entiated from waking.
The bizarre character dreaming was, for
Freud, determined by the disguise and censorship
of
the unconscious wishes. In order to protect conscious
ness from disruption (which would otherwise lead to
awakening), such defensive processes as displacement,
condensation, and symbolization were called into
play. Even the visual hallucinosis of dreaming was
viewed by Freud as a regression to the sensory side
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7
that served to neutralize the impact o the unconscious
wishes on consciousness.
We
would now say that dreaming is bizarre be
cause o the distinctive neurophysiology o REM sleep
with its shift from top-down cortical control in waking
to bottom-up phasic autoactivation epitomized by the
PGO process. The distinctive regional activation pat
tern
o
the forebrain (with limbic, paralimbic, and pa
rietal cortical regions taking precedence over the
dorsolateral prefrontal cortex), and the global shift in
the biochemical mode
o
information processing
(caused by the noradrenergic and serotonergic demod
ulation) also contribute to dream bizarreness.
The visual nature dreams is for activation-syn
thesis, not defensive as Freud asserted, but rather the
direct result o both bottom-up activation processes
(which also convey information about brainstem/eye
movement commands). The degree to which primary
vs. secondary unimodal and multimodal cortices medi
ate dream vision and the relative influence
o
subcorti
cal--cortical vs. corticocortical activation processes
remains to be clarified. But the answers to these fasci
nating questions have no direct bearing on the dis
guise-censorship postulate which is the heart o the
Freudian dream theory.
While dreaming, we never sit and watch but are
constantly moving through dream space. Thus dreams
are not properly thought o as simply visual but more
accurately as visuomotor. This feature was not recog
nized by Freud even he did correctly infer the neces
sity
o
inhibiting motor output to prevent the
behavioral enactment o the fictive movement o
dreams. This is a key point for activation-synthesis
(and any modern general theory
o
hallucinosis) be
cause o the apparent link between brainstem motor
pattern generators and cortical sensory processes. A
strong implication is that far from being a feedback
regression to the sensory side, dream hallucinosis re
sults from a feed-forward conveyance
o
data about
motor intentions to the sensory processors in the up
per brain.
The emotional character
dreams
was not easily
dealt with by Freud's theory. He repeatedly side
stepped the obvious inconsistency between the pres
ence o sleep-disruptive anxiety and his mechanistic
postulate o disguise and censorship o the psychonox
ious dream content. The presence o dream anxiety
also inveighed against his guardian o sleep func
tional hypothesis. In other parts o Freudian theory
anxiety is viewed as a symptom o inadequate compro
mise between id and ego functions and he supposed
it to so operate in dreaming sleep.
J. Allan Hobson
Activation-synthesis has always regarded anxiety
(which is the leading emotion in all dreams and all
dreamers [Nielsen et aI., 1991; Merritt et aI., 1994;
Domhoff, 1996]) as the primary product
o
limbic lobe
activation. This speculative hypothesis has now re
ceived powerful support from recent PET studies
(showing amygdala, parahippocampal cortex, and an
terior cingulate gyrus activation in human REM
sleep).
In this sense anxiety (and the two other prominent
dream emotions, elation and anger) can be seen as
major dream plot organizers and shapers
o
the emo
tional salience o dreams. For the reform-minded psy
choanalyst, this should be heard as brain-music
o
divine inspiration because it suggests that dreaming is
a conscious state in which the impact o emotion upon
cognition is more clearly demonstrated than in wak
ing. A major reason for this shift must be that, together
with the limbic lobe activation, the seat
o the execu
tive control o cognition in the dorsolateral prefrontal
cortex is deactivated in REM
But let
us
make no mistake. This cortex vs. limbic
system construct in no way vindicates disguise-censor
ship nor does it support any interpretive scheme that
carries any trappings o that dogma. On the contrary,
it favors the view that dreams are, in part, the transpar
ent exposure
o
an individual's cognitive associations
to, and means o coping with, anxiety (where anxiety
is viewed
as
an inherent, existential emotion that is
designed to interact with cognition in an adaptive
disruptive manner).
mnesia for Dreams Freud ascribed dream for
getting to repression. Why repression was needed
the dreams had already been bowdlerized by disguise
and censorship was never made clear. Activation-syn
thesis says that both the dream forgetting following
awakening and the defective episodic memory that oc
curs within dreams is a simple, state-dependent amne
sia compounded by the global aminergic demodulation
and the deactivation
o working memory mechanisms
in the dorsolateral prefrontal cortex. Activation-syn
thesis further asserts that the reason that dream recall
is enhanced by spontaneous or stimulated awakenings
from REM sleep is because the aminergic demodula
tion and prefrontal cortical deactivation o REM are
suddenly reversed. As is well known, even these post
arousal recollections are evanescent probably because
it takes several minutes to reinstate waking cognition.
From the Neuron to the Dream: Freud's
Project Realized
Taken together, these new neuroimaging and brain le
sion studies strongly suggest that the forebrain activa-
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The New Neuropsychology o Sleep
tion and synthesis processes underlying dreaming are
very different from those o waking. Not only is REM
sleep chemically biased, but the preferential choliner
gic neuromodulation and aminergic demodulation are
associated with selective activation of the subcortical
and cortical limbic structures which mediate emotion
and with relative inactivation o the frontal cortex
which mediates directed thought . A unifying neuro
biological hypothesis is that the regional blood flow
changes are causally linked to the neuromodulatory
dynamics in the following way. Those areas which are
inactivated in REM are those undergoing aminergic
demodulation but are uncompensated by cholinergic
modulation while the activated areas are those heavily
targeted by cholinergic modulatory neurons.
Whatever the link between the neuromodulatory
and regional blood flow data, these findings greatly
enrich and inform the integrated picture ofREM sleep
dreaming as emotion-driven cognition with deficient
memory, orientation, volition, and analytic thinking.
And now that we know that there is a close fit between
the animal and human data regarding the mechanism
and pattern
o
brain activation in REM sleep, we are
in a much stronger position to strengthen the brain
based theory
o
dreaming first proposed twenty years
ago Hobson and McCarley, 1977 . We will now at
tempt to integrate the newly discovered facts from the
human imaging studies with the cellular and molecular
level findings gleaned from the animal model in order
to answer four questions: 1 What is the origin
o
dreaming? 2 Why are dreams cognitively distinc
tive? 3 Why are dreams forgotten? 4 What is the
function o dreaming?
The Origin reaming
Dreaming is a state o consciousness arising from the
activation o the brain in REM sleep. The brain activa
tion which underlies dreaming is, like that o waking,
a result o the excitation o forebrain circuits by im
pulses arising in the ascending activation systems
o
the brainstem e.g., pontine and midbrain reticular ac
tivating systems and basal forebrain e.g., cholinergic
Nucleus Basalis
o
Meynert . This activation process
prepares the forebrain to process data with associated
cognitive awareness. But REM-sleep brain activation
differs from that o waking in three important ways:
There is selective activation o occipital, parietal
and limbic zones with a selective inactivation
o
frontal regions.
7
2 The mechanism o the brainstem triggering o fore
brain activation involves the spontaneous excitation
o
cholinergic neurons in the pontomesencephalic
LDT and PPT nuclei. This occurs as the inhibitory
restraintupon themdeclines with the near total arrest
o
firing by noradrenergic neurons in the locus coer
ulus and serotonergic neurons in the raphe nuclei.
3
Besides the recruitment o the pontine and mesen
cephalic reticular formation which mediate the
tonic thalamocortical activation the disinhibited
cholinergic system appears to
pl y
role in provid
ing the activated forebrain with phasic activation
signals, the PGO waves, that have two targets o
particular relevance to dream theory:
a The lateral geniculate body and posterolateral
cerebral cortex, the presumed substrates of
visual imagery in dreaming, and
b Limbic and paralimbic structures, the pre
sumed substrates o emotion and emotionally
salient dream memories.
The istinctive Nature ream ognition
The selective activation process described above may
account for such distinctive cognitive features o
dreaming as:
The intense and vivid visual hallucinosis, due to
autoactivation o the visual brain;
2 The intense emotions, especially anxiety, elation,
and anger, due to the autoactivation o the amyg
dala, and more medial limbic structures;
3 The delusional belief that we are awake, the lack
o directed thought, the loss of self-reflective
awareness, and the lack o insight about illogical
and impossible dream experience, due to the com
bined and possibly related effects of aminergic de
modulation and the selective inactivation o the
frontal cortices;
4
The bizarre cognition o dreaming which is charac
terized by incongruities and discontinuities o
dream characters, loci, and actions, due to an orien
tational instability caused by:
a the chaotic nature o the pontine autoactiva
tion process and its sporadic engagement o
association cortices,
b the absence o frontal cortical monitoring,
and
c the memory deficits.
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172
J. Allan Hobson
Figure 4 Physiological Signs and Regional Brain Mechanisms
of
REM
Sleep Dreaming Separated into the Activation (A), Input Source (I), and
Modulation (M) Functional Components of the AIM Model (see Hobson,
1992a; Hobson et aI., 2000). Dynamic changes in A, I and M during REM
sleep dreaming are noted adjacent to each figure. Note that these are highly
schematized depictions which illustrate global processes and do not at
tempt to comprehensively detail all the brain structures and their interac
tions which may be involved in REM sleep dreaming (see text, Table 3
and Hobson et aI., 2000 for additional anatomic details).
ream orgetting
The practically total amnesia that most humans have
for their dream consciousness is most likely a joint
product
of
the aminergic demodulation and the frontal
deactivation of REM sleep. Cellular and molecular
level studies
of
learning and memory all concur in
supporting a role for the aminergic neuromodulators,
especially serotonin, norepinephrine, and dopamine
(Flicker, McCarley, and Hobson, 1981; Kandel and
Schwartz, 1982; Quartermain, 1983; Libet, 1984; Frith
et aI 1985; Montarolo et aI 1986; Kandel, 1989;
Abel et aI 1995). Without their mediation, signals
which arrive at a postsynaptic neuron may have in
stantaneous effects upon its membrane potential but
lack the specific second messenger instruction needed
by intracellular metabolic substrates to store a record
of the membrane events.
At first glance, this failure to record intercellular
transactions would seem to be at odds with the en
hancement of learning hypothesis advanced in the next
section. But
if
we recall that it is consolidation, not
acquisition that is hypothetically enhanced, it may be
quite useful
to
direct the brain-mind to the exclusive
task of processing information already acquired in
waking and
to ignore or
even
disc rd the
informa
tion that it necessarily generates as it self-activates in
the interests of consolidation. On this view, the dream
is the often meaningless sometimes meaningful noise
that is made when the brain enters its active, memory
consolidation mode.
Of course, it is also quite possible, and even prob
able, that a key aspect of memory consolidation in
volves emotional salience. But whether this aspect is
very different from that operating in the waking
st te s those psychologists who regard dreaming as
a privileged communication from the unconscious
mind still
hold rem ins
to be established.
The unction
reaming
ort x
minergically
demodulated
t
Recent memory
tOrientation
en lY input
blocked
Real wortd data unavailable
otor
outputblocked
Real
action
impossible
Pons
minergic neurons off
tNE
t T
Chotinergicneurons
on
t ch
Modulation
Input Source
P O syst m tumed