2 The New Neuropsychology of Sleep: Implications For Psychoanalysis

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The New Neuropsychology of Sleep: Implications for

Psychoanalysis
J. Allan Hobson
Laboratory 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:
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157
The New Neuropsychology of Sleep: Implications

for Psychoanalysis
Downloaded by [Gazi University] at 22:15 17 August 2014
J. Allan Hobson
Abstract: In 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, if not complete overhaul, because dreams,
as well as other unusual states of consciousness, can finally be
approached from the solid foundation of modem neuroscience. In
other words, the goals of Freud's Project are at last within our
grasp. Ironically, an obstacle to progress is the tenacious adherence of orthodox psychoanalysis to a theory that even by the standards of its originator, is now clearly outm04ed.
In 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
combined product ofa shift in the neuromodulatory balance of the
brain and a related redistribution of regional blood flow. The
human PET 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 emotional and mnemonic aspects of cognition. The pontine brainstem
mechanisms controlling the neuromodulatory balance ofthe brain
in rats and cats include noradrenergic and serotonergic influences
which enhance waking and impede REM via anticholinergic mechanisms, and cholinergic mechanisms which are essential to REM
sleep and only come into full play when the serotonergic and
noradrenergic systems are inhibited. In REM, the brain thus becomes 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 published review by the author and his colleagues Robert Stickgold and Edward 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 and 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 reviewed in detail below, the evidence for a strong brainstem 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 elaboration of dream plots. The emerging picture of dreaming
as the synthesis of emotional and sensorimotor data
generated by the distinctive mechanisms of brain activation 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 speculative 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 motives via the technique of free association to bizarre
dream material.
If, instead, the modern psychoanalyst takes the
more open view, that afforded by the Activation-Synthesis Hypothesis, that dreaming is a physiological 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
158
longer afford not to do so, the consequences of 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 of 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 of
many regrettable errors but with such important successes as the work of 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 of Freud's dream theory.
Brain-Based Differences between Waking and
Dreaming
The demonstration that the human brain activation

pattern of REM sleep is distinctly different from that
of waking has an important bearing upon our conception of how conscious states are generated by the
brain. It supports the hypothesis that quite different
mechanisms underlie waking and dreaming consciousness and that those differentiated mechanisms are
causally determinant of the differences in our subjective experiences of the two states. For some time, it has
been the cognitive similarities between waking and
dreaming that have been emphasized by dream psychologists (Antrobus, 1983; Foulkes, 1990, 1993,
1997; Moffitt, 1995). These similarities have been ascribed to brain activation processes that were thought
to be identical in the two states and this inference of
identity was supported by evidence from neurophysiology of 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
of amendment on physiological ground~.
Until now, the best available candidate mechanism for the differentiation of dreaming from waking
cognition has been the drastic reduction in the release
of the neuromodulators norepinephrine and serotonin
which drop from their steady high levels in waking to
almost zero in the REM sleep of cats and rats (Hobson,
1988, 1990, 1992, 1994, 1997a; Mamelak and Hobson, 1989; Hobson and Stickgold, 1994, 1995a). We
J. Allan Hobson
suggest that the newly described differences in regional 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).
Brain-Mind States and the Study of Consciousness
One of the strongest supports for the scientifically hypothesized unity of brain and mind comes from the
changes in conscious experience that we all experience 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 of fleeting hypnagogic images, the deeply unconscious oblivion of
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 of its own
physiological states (Hobson, 1994, 1997).
But whether or not they are accepted as firm
proof of brain-mind identity, these simultaneous subjective and objective events encourage the concept of
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 of the
neurophysiology and psychology of the events that
change, or remain the same, as the brain changes state.
It is within this paradigm of simultaneous conscious
state and brain-state change that I now review and
integrate data from three sources:
1. The formal and quantitative characteristics of consciousness 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 of the effect of
brain lesions and regional blood flow changes upon
the conscious states of humans.
REM Sleep Dreaming Defined

Formal Features of REM Sleep Dreams
REM sleep dreams have several distinctive formal features which the underlying brain state must somehow
The New Neuropsychology of Sleep

determine. They include: sensorimotor hallucinations;
bizarre imagery; the delusional belief that one is
awake; diminished self-reflective awareness; orientational instability; narrative structure; intensification of
emotion; instinctual behaviors; attenuated volition;
and very poor memory. Table 1 summarizes these feaTABLE 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 Donderi, 1998).
Bizareness Incongruity (imagery is strange, unusual, or impossible); 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; Revonsuo 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; Barrett, 1992; Kahan and LaBerge, 1994; Hobson, 1997b).
Self-reflection absent or greatly reduced relative to waking (Rechtschaffen, 1978; Barrett, 1992; Bradley, Hollifield, and
Foulkes, 1992).
Lack of orientational stability Persons, times, and places are fused,
plastic, incongruous, and discontinuous (McCarley and Hobson, 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; Blagrove, 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 quantification. Our discussion is based upon our
psychophysiological theory of brain-mind isomorphism. We assume that any enhancement (or impairment) 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.
Dream Motor Hallucinosis-Fictive Movement

The nature of the motor hallucinations of dreams deserves special comment because it suggests that brain
mechanisms subserving active motor behaviors are
brought into play during REM. Thus, even officebound 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 discussed below, REM sleep dream consciousness routinely 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 physiological processes which subserve internal visuomotor
activation. We would then predict selective activation
of the visual system, the basal ganglia, the motor cortex, or subcortical motor pattern generators. The neurophysiological studies and PET data from humans
confirm these predictions.
Dream 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
J. Allan Hobson
160
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 credentials, adequate equipment, or suitable clothing, to missing a train. These plots all satisfy the driving
emotion-anxiety-while being only very loosely associated with one another.
Dream Cognition
The distinctively discontinuous and incongruous nature of dream cognition can be measured as a construct
termed bizarreness (Hobson, Hoffman, Helfand, and
Kostner, 1987; Hobson, 1988). Bizarreness in turn reflects 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 individual and some of another. Even the sexual identity
of dream characters is fluid, and this ambiguity can
be anatomically explicit, not just psychological.
Dream Amnesia and Related Cognitive Deficits
The loss of memory in REM sleep makes dreaming

consciousness much more difficult to recall than waking consciousness. This phenomenological deficit logically implies a physiological deficit: some functional
process, present and responsible for memory in waking, 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,
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 subtraction of noradrenaline and serotonin from the varied
neuromodulatory mixture facilitating waking cognition, a mixture which, of course, includes acetylcholine (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 delusion that we are awake in our dreams) are two related 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 regular 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 associated with longer, more vivid, more motorically animated, and more bizarre accounts than NREM
(Foulkes, 1962,1982,1985,1993; Rechtschaffen, Verdone, and Wheaton, 1963; Goodenough, Lewis, Shapiro, 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
161
most strongly supports dream psychology (Kahn et aI.,

1997). For this reason, we restrict our integrative efforts to the neuropsychology of REM sleep dreaming.
A. Structural Model
The Reciprocal Interaction Hypothesis

The discovery of the ubiquity of REM sleep in mammals 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 widespread 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 system 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 neuromodulatory subsystems of the brainstem (Dahlstrom and
Fuxe, 1964; for reviews see Foote, Bloom, and AstonJones, 1983; Hobson and Steriade, '1986; Jacobs and
Azmita, 1992) and of their differential activity in waking (noradrenergic and serotonergic systems on,
cholinergic system damped) and REM sleep
(noradrenergic and serotonergic systems off, cholinergic system undamped) (Trulson and Jacobs, 1970; Chu
and Bloom, 1973, 1974; Hobson, McCarley, and Wyzinski, 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 cellular 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 neurobiological substrate of the conscious experience associated with these states. We now devote our careful
attention to a review of the cellular and molecularlevel details, in the context of the reciprocal interaction concept, to provide a basis for our discussion of
the new human imagery data in a later section.
B. Dynamic Model
t>-RIM..:.Q!!
NE,5HT
__
........ ......
"
"
'\
\
REM-On
',./
'""-----'
C. Activation Level (A)
1
Wake
---..Ir--4l
NREM
REM
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 noradrenergically (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 reciprocally waxes. At REM sleep onset aminergic inhibition is shut off and
cholinergic excitation reaches its high point. (C) Activation level: As a
consequence of the interplay of the neuronal systems shown in A and B,
the net activation level of the brain is at equally high levels in waking and
REM sleep and at about half this peak level in NREM sleep (Hobson,
1992).
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 neurobiological control system (Figure 1). In this section
we review subsequent work that has led to the alteration and elaboration (Figure 2) of the model.
Cholinergic REM Sleep Generation

Although there is abundant evidence for a pontine peribrachial cholinergic mechanism of REM generation
centered in the pedunculopontine (PPT) and laterodorsal tegmental (LDT) nuclei (for recent reviews see
Hobson, 1992; Hobson, Datta, Calvo, and Quattrochi,
J. Allan Hobson
162
REM Off
REM On
B.
Ach +0:
1
. - 5-HT
----...,
GABA
5.
:
---'----...-------,
mesopontine tegmentum
raphe
5-HT
3.
14
7. GL. AS
,1 ...
.;1-_ + 7. Ach
NE+Q 0
B.:
cholinergic non-cholinergic
PPT and LOT mPRF and Lea
+Ach
~ B.
GA!A
locus
coeruleus
+Ach
2.
-
Ach
+OAch -
'----~1.~
6.
NE
4.
GABAergic nuclei
................................... (e.g. substantia nigra pars reticulat8)

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 dynamic relationships are shown as dotted lines, and references are indicated
by numbers (see key below). The exponential magnification of cholinergic
output predicted by the original model (Figure 1) can also occur in this model
with mutually excitatory cholinergic-non-cholinergic interactions (7) taking
the place of the previously postulated, mutually excitatory cholinergic-cholinergic interactions. Therefore the basic shape of reciprocal interaction's
dynamic model (illustrated in Figure IB) and its reluctant alternation of behavioral 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. Excitatory cholinergic-non-cholinergic interactions utilizing ACh and the excitatory amino acid transmitters enhance firing of REM-on cells (6, 7) while
inhibitory noradrenergic (4), serotonergic (3) and autoreceptor cholinergic
(1) interactions suppress REM-on cells. ii. Cholinergic effects upon aminergic neurons are both excitatory (2), as hypothesized in the original reciprocal
interaction model and may also operate via presynaptic influences on noradrenergic-serotonergic as well as serotonergic-serotonergic circuits (8). iii.
Inhibitory cholinergic autoreceptors (1) could contribute to the inhibition of
LOT and PPT cholinergic neurons which is also caused by noradrenergic (4)
and serotonergic (3) inputs. iv. GABAergic influences (9, 10) as well as other
neurotransmitters such as adenosine and nitric oxide (see text) may contribute to the modulation of these interactions. Abbreviations: open circles, excitatory postsynaptic potentials; closed circles, inhibitory postsynaptic
potentials; mPRF, medial pontine reticular formation; PPT, pedunculopontine tegmental nucleus; LOT, laterodorsal tegmental nucleus; LCa, peri-locus coeruleus alpha; 5HT, serotonin; NE, norepinephrine; ACh,
acetylcholine; GL, glutamate; AS, aspartate; GABA, gamma-aminobutyric
acid. References: 1. Baghdoyan, Fleegal, & Lydic, 1997; EI Manseri, Sakai, & Jouvet, 1990; Kodama & Honda, 1996; Leonard & Llinas, 1990, 1994;
Luebke, McCarley, & Greene, 1993; Roth, Fleegal, Lydic, & Bagndoyan,
1996; Sakai & Koyama, 1996; Sakai, EI Manseri, & Jouvet, 1990. 2. Egan &
North, 1985, 1986.3. Horner, Sanford, Annis, Pack, & Morrison, 1997; Leonard & 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, Mamelak, Quattrochi, & Hobson, 1990a, b. 7. Greene & McCarley, 1990; Leonard & 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.
1993; Datta, 1995, 1997a; McCarley, Greene, Rannie,

and Portas, 1995; McCarley et aI., 1997), not all pontine 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 wakefulness as during sleep (Jasper and Tessier, 1971; Marrosu et aI., 1995; Jimenez-Capdeville and Dykes,
1996).
The original claim, that the medial pontine reticular formation (mPRF) was cholinergic, was clearly in
error. While many of the mPRF cells are excited by
acetylcholine as originally hypothesized, their own excitatory 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 brainstem cholinergic and aminergic neurons have recently
been questioned (Leonard and Llinas, 1994). Specifically, 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 hyperpolarize cell membranes in slice preparations of the rodent 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 reciprocal interaction model accurately describes essential
elements of REM sleep cycle control even though
some of its detailed synaptic assumptions need correction, as shown in Figure 2. Numerous findings confirm
the hypothesis that cholinergic mechanisms are essential to the generation of REM sleep and its physiological signs (for recent reviews see Hobson, Lydic, and
Baghdoyan, 1986; Hobson and Steriade, 1986; Sakai,
1988; Steriade and McCarley, 1990; Jones, 1991; Hobon, 1992b; Hobson et aI., 1993; Datta, 1995, 1997).
A selection of many recent examples follows.
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,

Rodrigo-Angulo, McCarley, and Hobson, 1987; Baghdoyan, Lydic, Callaway, and Hobson, 1989; VanniMercier, Sakai, and Lynn, 1989; Velazquez-Moctezuma, Gillin, and Shiromani, 1989; Yamamoto, Mamelak, Quattrochi, and Hobson, 1990a,b; Hobson et
aI., 1993). In addition to these short-term REM induction 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, Quattrochi, 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 of REM by muscarinic antagonists (Hobson et aI., 1986), the new presynaptic anticholinergic agents have also been shown to block
REM (Salin-Pascual and Jimenez-Anguiano, 1995;
Capece, Efange, and Lydic, 1997).
Cholinergic Neurons and REM Sleep
Cholinergic (type II and III) PPT and LDT neurons

have firing properties which make them well suited
for the tonic maintenance of REM (Leonard and Llinas, 1990), and both PPT and LDT neurons show specifically 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 of that state. Low amplitude
electrical stimulation of 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, glutamate, when microinjected into the cholinergic PPT,
increases REM sleep in a dose-dependent manner
(Datta, 1997b; Datta and Siwek, 1997).
Acetylcholine Release and REM sleep
Microdialysis studies show enhanced release of endogenous acetylcholine in the medial pontine reticular
formation during both natural (Kodama, Takahashi,
and Honda, 1990) and carbachol-induced (Lydic, Bagh-
163
doyan, and Lorine, 1991) REM sleep. Thalamic ACh
concentration of mesopontine origin is higher in both
wake and REM than in NREM (Williams, Comisarow,
Day, Fibiger, and Reiner, 1994), and a REM-specific
increase of ACh in the lateral geniculate body has
been observed (Kodama and Honda, 1996). Both muscarinic and nicotinic receptors participate in the depolarization of thalamic nuclei by the cholinergic
brainstem (Curro-Dossi, Pare, and Steriade, 1991).
Cholinergic 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 of mesopontine neurons induces depolarization of cortically projecting thalamic
neurons (Curro-Dossi et aI., 1991). Neurotoxic lesions
of pontomesencephalic cholinergic neurons reduce the
rate of PGO spiking (Webster and Jones, 1988) and
PGO waves can 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 overwhelming and so widely accepted that this tenet of the
reciprocal interaction model is an established principle.
Aminergic Inhibition of the Cholinergic REM
Generator
At the heart of the reciprocal interaction concept is

the idea that cholinergic REM sleep generation can
only occur when the noradrenergic and serotonergic
mediators of waking release their inhibitory constraint
of the cholinergic generator. The evidence for inhibitory serotonergic and noradrenergic influences on cholinergic neurons and REM sleep is now also quite
strong.
Decreased Serotonin Release in Natural REM Sleep
In the cat, extracellular levels of 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-dependent pattern is observed in the hypothalamus of the rat
(Auerbach, Minznberg, and Wilkinson, 1989; Imeri,
164
DeSimoni, Giglio, Clavenna, and Mancia, 1994).
Moreover, reduced extracellular serotonin concentration in REM sleep has recently been demonstrated in
the human amygdala, hippocampus, orbitofrontal cortex 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 Cholinergic Systems and

REM Sleep
Serotonergic neurons from the dorsal raphe have been

shown to synapse on LDT and PPT neurons (Honda
and Semba, 1994). Serotonin has been shown to hyperpolarize 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 Davies, 1996; Okabe and Kubin, 1997).
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 (noradrenergic) 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 et aI., 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-suppressive 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, norepinephrine, or both (Vogel, 1975; Nicholson, Belyavin, and
Pascoe, 1989; Vogel, Buffenstein, Minter, and Hennessy, 1990).
Like cholinergic enhancement, aminergic suppression 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).
Suppression of REM by Serotonin Agonists
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 suppresses REM (Monti et aI., 1994). Simultaneous unit
recording has shown that microinjection of 8-0HDPAT 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 microdialysis of serotonin agonists into the dorsal raphe nucleus (DRN) decreased DRN levels of serotonin
(presumably via serotonin autoreceptors on DRN
cells) which in turn increased REM sleep percent (Portas, Thakkar, Rainnie, and McCarley, 1996). Mesopontine injection of a serotonin agonist depressed ACh
release in the lateral geniculate body (Kodama and
Honda, 1996).
Suppression of REM by Endogenous Norepinephrine
and its Agonists
Locus coeruleus neurons have been shown to become

quiescent during REM in the monkey (Rajkowski, Si-
Modification of the Reciprocal Interaction Model
Modifications of simple reciprocal inhibition or interaction models, which are consonant with recent findings, 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" 'indirect feedback' excitation via cholinergic inhibition of
an inhibitory input or cholinergic excitation of an excitatory input or some combination of the two could
replace direct feedback excitation in their model" (p.
327). A similar mutually excitatory or mutually inhibitory 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 following elaboration of reciprocal interaction has been proposed by Li et ai. in the McCarley laboratory (Li et
aI., 1997). During waking, presynaptic nicotinic facili-

tation of excitatory locus coeruleus noradrenergic inputs to the dorsal raphe enhances serotonergic firing.
During REM, when the locus coeruleus is silent, this
same presynaptic nicotinic input may facilitate serotonergic self-inhibition by the raphe neurons themselves. In vivo microdialysis studies of GABA in the
cat further postulate selective suppression of noradrenergic locus coeruleus neurons by GABAergic inhibition 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 possible, 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 activity (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; Baghdoyan et aI., 1997). In contrast to the hyperpolarization of some mesopontine cholinergic neurons by cholinergic 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 mesoand medial pontine sites (Hobson and Steriade, 1986;
Hobson et aI., 1986, 1993; Steriade and McCarley,
1990) may involve excitatory neurons which are noncholinergic. Such cholinergic self-regulation combined 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 mechanisms; (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 contributions 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 (McCarley et aI., 1997); or the neuropeptides (Bourgin et aI.,
1997). Nor do we exclude the contributions of numerous nonpontine structures such as the basal forebrain
(Szymusiak, 1995); hypothalamus (Saper et aI., 1997);
the amygdala (Sanford, Ross, Tejani-Butt, and Morrison, 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 necessarily restricted to data obtained in subhuman
models of REM sleep, an abundant psychopharmacological literature provides indirect evidence that the
same mechanisms operate at the cellular and molecular 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.
Human 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 analyze 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 identicalor, 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, experiments 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 (Doricchi and Violani, 1993; Solms, 1997). The remark-
166
J. Allan Hobson
TABLE 2
Imaging of Brain Activation in REM and the Effects of Brain
Lesions on Dreaming
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 Frontal Cortex
KEY:
1 Increase; 1 Decrease; -
1
1
!
1
1 (right)
!
No Change.
ably complementary results of these two approaches

are summarized in Table 2.
PET Imaging Studies of REM Sleep Dreaming
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 generation. 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, regionally 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 discoveries 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 hypothesized (Hobson and McCarley, 1977).
Maquet et aI. (1996) used an H2150 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 tegmentum, significant activation was seen in both amygdalae
and the anterior cingulate cortex (Table 3). Significantly, despite the general deactivation in much of the
parietal cortex, Maquet et aI. reported activation of
the right parietal operculum-a brain region thought
to be important for spatial imagery construction, an

important aspect of dream cognition. As Maquet (Maquet and Franck, 1997) emphasizes, those cortical areas activated in REM are rich in afferentation from
the amygdala (anterior cingulate, right parietal operculum) while those areas with sparse amygdalar afferentation (prefrontal cortex, parietal cortex, and
precuneus) were deactivated in REM. Maquet et al.
interpreted their data in terms of the selective processing, in REM, of emotionally influenced memories
(see also Braun et aI., 1997; Maquet and Franck,
1997).
In another H2150 PET study, Braun et aI. (1997)
replicated the Maquet group's findings of a consistent
REM-related brainstem, limbic, and paralimbic activation. When REM-sleep brain activity was compared
to brain activity in delta NREM, with presleep waking
and with postsleep waking, Braun et aI. showed relative 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.
1. The ascending reticular activation of REM
sleep may proceed relatively more via a ventral cholinergic route from the brainstem through the basal forebrain 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 neuronal activation causing fictive movement in dreams
(Leslie and Ogilvie, 1996; Hobson, Stickgold, PaceSchott, and Leslie, 1997).
3. The strong REM sleep-related activation of
the basal ganglia suggests that these subcortical structures may play an important role in ascending thalamocortical activation. The mediating network links
brainstem to the basal ganglia via the intralaminar thalamic nuclei and proceeds to the cortext via the ventral
anterior and ventromedial thalamic nuclei. Because
this network contains multiple regulatory back projections 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).
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
Technique
Maquet et aI., 1996

H2150
Braun et aI., 1997

H 2150
Braun et aI., 1997

H2150
increase (R*)
increase*
increase
increase
increase: A-POA
increase
increase: A-POA
increase*
increase
increase*
increase
increase
increase
increase
(vermis)*
increase
(vermis)
Nofzinger et aI., 1997

18PDG
Subcortical Areas
Brainstem
Pontine tegmentum
Midbrain
Dorsal mesencephalon
Diencephalon
Thalamus
Hypothalamus
Limbic system
Left amygdala
Right amygdala
Septal nuclei
Hippocampus
Basal ganglia/striatum
Caudate
Putamen
Ventral striatum (n. accumbens, sub.innominata)
Cerebellum
increase
increase
increase: L
increase: R, Lat
increase
increase
increase
increase
increase: A, I, L
increase
Cortical Areas
Frontal
Dorsolateral Prefrontal
decrease:
L: 10, 11,46, 47
R: 8, 9, 10, 11, 46
increase
increase: 11, 12
decrease: 11 *
increase
increase
increase
decrease: 40*
increase: R A 40
decrease: L 40
decrease: 39*
decrease
Temporal
Middle
Posterior superior
Inferior I fusiform
increase R
increase: 37, 19
(postsleep only)
Occipital
Postrolandic sensory
Limbic Associated
Medial (prelimbic) prefrontal
Anterior cingulate
Posterior cingulate
Infralimbic
Insula
Parahippocampal
Entorhinal
Temporal pole
decrease: 46*
decrease: 45*
Opercular
Paraolfactory
Lateral orbital
Caudal orbital
Gyrus rectus
Parietal
Brodmann area 40
(supramarginal gyrus)
Angular gyrus
Precuneus
increase
increase: 22
increase: 37, 19
increase
increase: 24
decrease: 31
increase
increase: R 32
increase: 24
dec: R sm. areas
increase: 25
increase: L
increase
inc. (in fusiform)
increase: 10
increase: 32*
decrease*
increase: 10
increase: 32
decrease-P
increase: 37*
increase: A I
increase: 37
increase: 38
Abbr: L-Ieft h~misphere; 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)
168
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 deactivation of heteromodal association areas in the frontal and
parietal cortices. Interestingly, the inferior temporal
cortex (Brodmann areas 19 and 37) contains the fusiform 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 prefrontal cortices). This medial area, which has the most
abundant limbic connections in the prefrontal cortex,
has been associated with arousal and attention. Disruption of this area has been shown to cause confabulatory 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 dreaming increases in vivacity and reality and dreaming become confused (Solms, 1997). From these findings as
well as primary visual cortex deactivation in REM,
the Braun group has recently suggested that REM constitutes, in the cortex, a unique condition of internal
information processing (between extrastriate and limbic cortices) functionally isolated from input (via striate 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) described increased glucose utilization in the lateral hypothalamic area and the amygdaloid complex using an
I8F-fluoro-deoxyglucose (FDG) PET technique (Table
3). Nofzinger et aI. note that, "The largest area of
activation is a bilateral confluent paramedian zone
which extends from the septal area into ventral striatum, 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 hypothalamic motivational and reward mechanisms.
An equally interesting H 2Is Q PET finding, relevant to the cognitive deficits in self-reflective awareness, 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 dorsolateral prefrontal deactivation during REM, however, was not replicated by the Nofzinger et aI. FDG
study and this discrepancy remains to be clarified. Using 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
"REM sleep may constitute a state of generalized
brain activity with the specific exclusion of executive
systems which normally participate in the highest order 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 'association' loop, connecting the caudate, dorsomedial thalamus and prefrontal cortices ... appears to be activated
only in a partial or fragmentary way" (p. 1191). Figure 3 integrates findings from these first three PET
studies comparing REM sleep to other states.
Loss of Dreaming After Cerebral Lesions

An entirely complementary set of findings and conclusions 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 apparently 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 (especially areas V3, V 3a, and V4 but not VI, Vs or V6 ).
Solms (1997) also-reports that his patients with pontine lesions continued to dream and concludes that the
pons is not necessary for human dreaming. Based
upon the difficulty of suppressing REM by experimental lesions of the pons in animals, we suggest an alternative explanation. It seems to us that any lesion
169
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 reported 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 schematically 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 eNS areas subserving similar
functions (e.g., limbic-related cortex, ascending activation pathways and
multimodal association cortex).
(Hong, Gillin, Dow, Wu, and Buchsbaum, 1995). Although these authors interpret this medial activity correlation 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; Nofzinger 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, Wilson, 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).
capable of destroying the pontine REM sleep generator mechanism would have to be so extensive as to
eliminate consciousness altogether.
Freud's Dream Theory Revised in the Light of

Modern Sleep and Dream Research
Dorsolateral
Prefrontal
Cortex
Activated in REM
~ Deactivated in REM
Emotionally Salient Memory 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 memory systems (Maquet et aI., 1996; Braun et aI., 1997;
Nofzinger et aI., 1997; Maquet and Franck, 1997). Additionally, both the Maquet and Braun groups suggest
the possible origin of dream emotionality in REMassociated limbic activation and dream-associated executive deficiencies in REM-associated frontal deactivation (Braun et aI., 1997; Maquet and Franck, 1997).
Additional findings support this proposed cortico-limbic interaction. First, as shown in Table 3, the cingulate cortex has consistently shown increased activation
in REM in other PET studies (Buchsbaum et aI., 1989).
Second, FDG PET activation of anterior medial structures, including the anterior cingulate and medial frontal cortex, was found to correlate with REM density
in the REM period during which FDG uptake occurred
There are five basic tenets to Freud's disguise--eensorship dream theory which can now be contrasted with
aspects of the activation-synthesis hypothesis.
The instigation of dreaming was, for Freud,
caused by the upsurge of unconscious wishes following suspension of their wake-state repression. We
would now say that dreaming is caused by brain activation 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 differentiated from waking.
The bizarre character of dreaming was, for
Freud, determined by the disguise and censorship of
the unconscious wishes. In order to protect consciousness 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"
170
that served to neutralize the impact of the unconscious
wishes on consciousness.
We would now say that dreaming is bizarre because of the distinctive neurophysiology of 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 pattern of the forebrain (with limbic, paralimbic, and parietal cortical regions taking precedence over the
dorsolateral prefrontal cortex), and the global shift in
the biochemical mode of information processing
(caused by the noradrenergic and serotonergic demodulation) also contribute to dream bizarreness.
The visual nature ofdreams is for activation-synthesis, not defensive as Freud asserted, but rather the
direct result of 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 mediate dream vision and the relative influence of subcortical--cortical vs. corticocortical activation processes
remains to be clarified. But the answers to these fascinating questions have no direct bearing on the disguise-censorship postulate which is the heart of the
Freudian dream theory.
While dreaming, we never sit and watch but are
constantly moving through dream space. Thus dreams
are not properly thought of as simply visual but more
accurately as visuomotor. This feature was not recognized by Freud even if he did correctly infer the necessity of inhibiting motor output to prevent the
behavioral enactment of the fictive movement of
dreams. This is a key point for activation-synthesis
(and any modern general theory of hallucinosis) because of 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 results from a feed-forward conveyance of data about
motor intentions to the sensory processors in the upper brain.
The emotional character ofdreams was not easily
dealt with by Freud's theory. He repeatedly sidestepped the obvious inconsistency between the presence of sleep-disruptive anxiety and his mechanistic
postulate of disguise and censorship of the psychonoxious dream content. The presence of dream anxiety
also inveighed against his "guardian of sleep" functional hypothesis. In other parts of Freudian theory
anxiety is viewed as a symptom of inadequate compromise 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 of limbic lobe
activation. This speculative hypothesis has now received powerful support from recent PET studies
(showing amygdala, parahippocampal cortex, and anterior 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 of the emotional salience of dreams. For the reform-minded psychoanalyst, this should be heard as brain-music of
divine inspiration because it suggests that dreaming is
a conscious state in which the impact of emotion upon
cognition is more clearly demonstrated than in waking. A major reason for this shift must be that, together
with the limbic lobe activation, the seat of the executive control of 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-censorship nor does it support any interpretive scheme that
carries any trappings of that dogma. On the contrary,
it favors the view that dreams are, in part, the transparent exposure of an individual's cognitive associations
to, and means of coping with, anxiety (where anxiety
is viewed as an inherent, existential emotion that is
designed to interact with cognition in an adaptive if
disruptive manner).
Amnesia for Dreams. Freud ascribed dream forgetting to repression. Why repression was needed if
the dreams had already been bowdlerized by disguise
and censorship was never made clear. Activation-synthesis says that both the dream forgetting following
awakening and the defective episodic memory that occurs within dreams is a simple, state-dependent amnesia compounded by the global aminergic demodulation
and the deactivation of working memory mechanisms
in the dorsolateral prefrontal cortex. Activation-synthesis further asserts that the reason that dream recall
is enhanced by spontaneous or stimulated awakenings
from REM sleep is because the aminergic demodulation and prefrontal cortical deactivation of REM are
suddenly reversed. As is well known, even these postarousal 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 lesion studies strongly suggest that the forebrain activa-
171

tion and synthesis processes underlying dreaming are
very different from those of waking. Not only is REM
sleep chemically biased, but the preferential cholinergic neuromodulation and aminergic demodulation are
associated with selective activation of the subcortical
and cortical limbic structures (which mediate emotion)
and with relative inactivation of the frontal cortex
(which mediates directed thought). A unifying neurobiological 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 of REM 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 of brain activation in REM sleep, we are
in a much stronger position to strengthen the brainbased theory of dreaming first proposed twenty years
ago (Hobson and McCarley, 1977). We will now attempt 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 of
dreaming? (2) Why are dreams cognitively distinctive? (3) Why are dreams forgotten? (4) What is the
function of dreaming?
The Origin of Dreaming
Dreaming is a state of consciousness arising from the

activation of the brain in REM sleep. The brain activation which underlies dreaming is, like that of waking,
a result of the excitation of forebrain circuits by impulses arising in the ascending activation systems of
the brainstem (e.g., pontine and midbrain reticular activating systems) and basal forebrain (e.g., cholinergic
Nucleus Basalis of Meynert). This activation process
prepares the forebrain to process data with associated
cognitive awareness. But REM-sleep brain activation
differs from that of waking in three important ways:
1. There is selective activation of occipital, parietal
and limbic zones with a selective inactivation of
frontal regions.
2. The mechanism of the brainstem triggering of forebrain activation involves the spontaneous excitation
of cholinergic neurons in the pontomesencephalic
LDT and PPT nuclei. This occurs as the inhibitory
restraint upon them declines with the near total arrest
of firing by noradrenergic neurons in the locus coerulus and serotonergic neurons in the raphe nuclei.
3. Besides the recruitment of the pontine and mesencephalic reticular formation (which mediate the
tonic thalamocortical activation) the disinhibited
cholinergic system appears to playa role in providing the activated forebrain with phasic activation
signals, the PGO waves, that have two targets of
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 presumed substrates of emotion and emotionally
salient dream memories.
The Distinctive Nature of Dream Cognition
The selective activation process described above may

account for such distinctive cognitive features of
dreaming as:
1. The intense and vivid visual hallucinosis, due to
autoactivation of the visual brain;
2. The intense emotions, especially anxiety, elation,
and anger, due to the autoactivation of the amygdala, and more medial limbic structures;
3. The delusional belief that we are awake, the lack
of directed thought, the loss of self-reflective
awareness, and the lack of insight about illogical
and impossible dream experience, due to the combined and possibly related effects of aminergic demodulation and the selective inactivation of the
frontal cortices;
4. The bizarre cognition of dreaming which is characterized by incongruities and discontinuities of
dream characters, loci, and actions, due to an orientational instability caused by:
(a) the chaotic nature of the pontine autoactivation process and its sporadic engagement of
association cortices,
(b) the absence of frontal cortical monitoring,
and
(c) the memory deficits.
172
J. Allan Hobson
Activation
Dream Forgetting
Parietal operculum
.. Visuospatial
imagery
Input Source
PGO system tumed on
Fictive visual &
motor data generated
~ SenSOlY input blocked

Real wortd data unavailable
Motor output blocked

Real action impossible
Cortex
Modulation
Aminergically demodulated
t Recent memory
tOrientation
Pons
Aminergic neurons off
tNE. t5HT
Chotinergic neurons on
tAch
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 attempt to comprehensively detail all the brain structures and their interactions which may be involved in REM sleep dreaming (see text, Table 3
and Hobson et aI., 2000 for additional anatomic details).
5. The emotional salience of dream imagery (due to

the activation of the paralimbic cortices by the
amygdala).
Figure 4 presents a schematic model for the generation of these cognitive dream features by combining the above findings on state-dependent regional
activation with a model of the neuromodulation of
conscious states (Hobson, 1990, 1992, 1997a; Hobson
and Stickgold, 1995a).
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 instantaneous 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 enhancement 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 discard-the information 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 probable, that a key aspect of memory consolidation involves emotional salience. But whether this aspect is
very different from that operating in the waking
state-as those psychologists who regard dreaming as
a privileged communication from the unconscious
mind still hold-remains to be established.
The Function of Dreaming
If dream bizarreness indeed arises from the chaotic

autoactivation process and the absence of top-down
control from the frontal cortex in REM sleep, the apparent nonsense of dreams is most likely just that and
not the result of disguise and censorship as Freud's
psychoanalytic dream theory proposed (Freud, 1895).
At the same time, the instigation of emotionally salient
memories is probably also just that. Hence dreams
may be both nonsensical (i.e., bizarre) and transparently meaningful (i.e., emotionally salient) (Hobson,

1988). They are therefore potentially informative,
both in clinical and personal terms if one discounts the
bizarreness and attends to the undisguised emotional
content. This approach, which is straightforward and
requires no interpretation, may be well undertaken
without mediation but it may also be facilitated by a
sympathetic interlocutor.
Because dreams are so difficult to remember it
seems unlikely that attention to their content could
afford much in the way of high-priority survival value.
Indeed, it might instead be assumed that dreaming is
an epiphenomenon of REM sleep whose cognitive
content is so ambiguous as to invite misleading or even
erroneous interpretation. From the neurobiological
point of view it seems more likely that it is REM sleep
itself, and not the subjective experience of dreaming,
which has a functional significance for cognition that
cannot easily be deduced from dream content. Among
the many interesting theories that have been put forth,
the restoration of cognitive capabilities such as attention and the enhancement of such learning processes
as memory consolidation are of particular interest
(Cai, 1995; Crick and Mitchison, 1995; Giuditta et
aI., 1995; Hennevin, Hars, Maho, and Bloch, 1995;
Hobson and Stickgold, 1995b; Smith, 1995, 1996; Kavanaugh, 1997; Askenasy, Karni, and Sagi, 1997). We
regard the testing of this memory consolidation hypothesis as a most promising area of ongoing research
on sleep and dreaming.
173
research must therefore be to test this hypothesis at
both the basic science and clinical levels.
A New View of Dreams and Nightmares Based

on Neurobiology
Freud said the ego wishes to sleep. It withdraws its
cathexis from the waking world and, in so doing, releases the unconscious from its repressive vigil. Activation-synthesis says that sleep and waking alternate
with a period of about 24 hours under the control of
the circadian oscillator in the suprachiasmatic nucleus
of the hypothalamus. With the onset of sleep, neuronal
activity through the brain's core activating system declines. With this decline, consciousness abates.
Dreaming at Sleep Onset
Mental activity during the immediate postsleep onset

period may be dreamlike because the upper brain is
still sufficiently activated to support visual imagery
and scenario construction but dream plots are neither
sustained nor dramatically bizarre and within minutes
give way to more perseverative thoughtlike mentation
and/or complete conscious oblivion.
Dreaming in NREM Sleep
Integrating the Cellular-Molecular and Regional

Blood Flow Differences in Sleep
The shift in regional blood flow discovered by recent

PET studies can now be integrated with the reciprocal
interaction model in a tentative way. Since they are
the central incarnation of the peripheral autonomic
nervous system, it seems quite likely that the noradrenergic, serotonergic, and cholinergic controllers of the
NREM/REM sleep cycle would affect blood flow as
well as neuronal excitability and second messenger
functions. If that were the case, then a combination
of the differential axonal distribution and differential
discharge profiles of these neuromodulation systems
could account for the redirection of blood flow away
from the dorsolateral prefrontal cortex and toward the
limbic and parietal regions of the upper brain. The
redirection of blood flow would shift the relative
weight of the forebrain participants in conscious state
determination as well as redirecting the flow of information between them. An important next step in our
Because Freud made no distinction between the kinds

of dreaming-or other sorts of mental activity-that
occur in sleep, this part of the story is, in part, supplemental, but it does challenge the naive reciprocity that
Freud postulated between the ego and the id in the
transition from wake to sleep because in NREM sleep
the brain regions subserving reason and instinct are
depressed in parallel. At the depths of NREM sleep,
when the ego's withdrawal of cathexis would be expected to be maximal there is thus likely to be little or
no conscious mental activity of any kind. Awakenings
from Stage IV sleep are difficult to achieve, subjects
are likely to awaken only partially, and as a result they
then evince a confusion akin to dementia or delirium.
The Occurrence of Nightmares and Night Terrors
The occasional occurrence of night terrors, classic

nightmares, and other manifestations of the motoric,
emotional, and autonomic storm that can arise in
174
NREM sleep might seem to be an exception to this
rule. True, it does mean that automatic processes of a
primitive and presumably subcortical origin can be
released in NREM sleep. But note, there is still no
evidence of disguise or censorship. On the contrary,
the experience of arousal from NREM sleep may be
one of unmitigated terror with little or no dreamlike
imagery. Freud was never able to deal with the problem of bad dreams. Now we see why. It is because
his basic theory was both wrong and incomplete.
Dreaming in REM Sleep
Periodically throughout sleep the brain self activates.

This self-activation is a complex, stereotyped process
that is now well understood at the cellular and molecular levels. Like the circadian rhythm of sleep and waking, the ultradian 90- to 100-minute alternation of
REM and NREM sleep is caused not by the ebb and
flow of desire but by a biological clock composed of
reciprocally interactive aminergic and cholinergic
brainstem neurons. This oscillator causes the brainmind to change its activation structure and both the
flow and mode of information processing are accordingly reversed. During REM sleep, dreaming assumes
its most intense, sustained, and distinctive character
because of the shift in the mechanism of activation
from aminergic-cholinergic (in waking) to exclusively
cholinergic (in REM sleep). We have already detailed
many of the implications of this finding for dream
theory, but two important implications remain to be
amplified.
The Functions of REM Sleep and Dreaming
Any functions of dreaming must be clearly distinguished from the functions of REM sleep, many of
which (like temperature control or immune function
maintenance) could never be inferred from dream consciousness and have little or nothing to do with dream
consciousness. In this sense it is already clear that
dreaming is epiphenomenal with respect to the most
fundamental biological adaptations of REM sleep.
What about more intermediate level functions,
like the regulation of neuromodulatory balance (via
shifts in the balance of synthesis and degradation of
crucial brain chemicals)? Such shifts could subserve
optimal waking function (including protection from
the breakthrough of REM-like psychotogenic processes). Here again, dream content might be quite ir-
J. Allan Hobson
relevant, telling us only what a subject's mental state
might be like if he or she were to become delirious.
In this sense, the interpretation of dreams in terms of
unconscious motives would make about as much sense
as interpreting the ravings of an alcoholic in the throes
of delirium tremens or the demented ramblings of an
Alzheimer's disease victim.
For the progressive psychoanalyst this point
might be reframed in a more general, heuristic manner:
REM sleep dreaming is didactic! It shows the doctor
and his patient what psychosis is like. It shows that
the propensity to psychosis is natural and universal. It
shows that all psychoses are both functional and organic. And it shows that all mental products have both
a meaningful (read emotionally salient) and nonsensical (read chaotic) aspect.
But it is at the cognitive level that the most intriguing reframings must proceed. Abundant evidence is
fast accumulating to indicate that both NREM and
REM sleep benefit learning and memory. As these
mental functions are the coin of the realm in any psychology, psychoanalysis, or psychotherapy the door is
open to an examination of dream content for direct
evidence of the kind of social and psychological learning that all therapies, including psychoanalysis, want
to promote.
Obstacles to Progress
Three fundamental problems must be overcome if psychoanalysis wants to counter its rapidly progressive
marginalization:
The first is the cult of Freud and the argument from authority. The reverence for Freud's self-styled heroism and
for his texts has held the field back from revision in the
light of modern cognitive neuroscience.
The second is the rigid institutional structure and rigid
adherence to methodological narrowness embodied by the
suggestion that the only dreams that matter are those that
are brought to the analyst and that the method of free
association is the only legitimate means of understanding
dreams and dreaming. This method, so clearly circular as
to be practically worthless if scientific validity is a goal,
must be seamlessly complemented by the vast range of
techniques from single-unit recording in cats to PET scans
in humans, and when the data are out of register, the
progressive analyst must be encouraged and supported
rather than punished for dissidence. The ad hominem argument that anyone who is skeptical of psychoanalytic
theory needs further analysis is one unfortunate offshoot

of this methodological argument.
The third is the socioeconomic parochialism of psychoanalysis which makes it appear to some as a parlor game
practiced by upper middle-class doctors upon each other
and their urban friends. To survive and to have any claim
to universality psychoanalysis needs to democratize as
well as to diversify. A corollary of this principle is that
it is unconscionable to claim, as did Freud, that psychoanalysis is a research tool and then charge people for it
as if it were medical treatment. And the joke of the century
must be the claim that psychoanalysis can only be effective if its cost is kept high! That is certainly not true of
the polio vaccine, or penicillin, or even lithium!
Conclusions
In my opinion the new dream theory is so different
from Freud's as to make the use of a word like revision
a euphemism. Because there is essentially nothing left
of the Freudian hypotheses, what is needed is not revision but complete overhaul. Instead, what we see is a
tenacious adherence to a faith in the interpretability of
dreams using vague and unscientific terms like metaphor and hermeneutics or, what is worse, we see recourse to the relativistic claim of narrative truth. This
limits psychoanalysis to a literary exercise with no
claim to the scientific legitimacy that Freud dreamed
of in his 1895 "Project for a Scientific Psychology."
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Commentary on The New Neuropsychology of Sleep
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74 Fenwood Road
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The New Neuropsycholog)r of Sleep

Commentary by Mark Solms (London)
Allan Hobson is the leading authority on the neurophysiology of REM sleep dreaming, and his work has
dominated this field for more than twenty years
(McCarley and Hobson, 1975; Hobson and McCarley,
1977). Recent findings concerning the neuropsychology of dreaming, however, as Hobson himself acknowledges, need to be reconciled with the old
physiological findings, and this is ushering in a new
era in this field.
In his paper, Hobson has covered a vast area of
knowledge. It will not be feasible for me to address
all of the points that he raised. I will focus selectively
on one or two things that I think are of central importance. This omits a lot else that is also of interest. I
am going to structure what I have to say around six
questions which I would like to pose to Professor
Hobson.
I don't have any disagreement with Hobson's understanding of the essential physiological mechanisms
underlying the sleep-waking cycle, including the
mechanism of REM sleep. However, I do disagree
with his understanding of the psychology of dreams
based on those physiological mechanisms. Obviously,
psychology is what interests psychoanalysts most.
There has always been an uncomfortable gap between
the psychological approach to dreams, as remembered
The present commentary is a lightly edited version of a discussion
of Hobson's presentation to the Neuro-Psychoanalysis Center of the New
York Psychoanalytic Institute, November 7, 1998:"The New Neuropsychology of Sleep: Implications for Psychoanalysis."
Mark Solms is Hon. Lecturer, Academic Department of Neurosurgery, S1. Bartholomew's and Royal London School of Medicine; and Associate Member of the British Psycho-Analytical Society.
subjectively by patients, and the physiological approach to dreams, as manifested objectively (apparently) by REM sleep. However, it is now possible to
bridge this gap, using the insights that modern neuropsychological methods and neuro-imaging techniques
can provide into the neural organization of all higher
mental functions.
REM sleep is a state with many components, including a forebrain component, but until recently, only
the brainstem component has been well understood.
The recent developments in the neuropsychology of
dreaming that I am going to refer to (clinico-anatomical studies of human patients and functional imaging
of the dreaming human brain)-which also form the
basis of Hobson's most recent revisions of his own
model-are beginning to elucidate the forebrain component, and thereby starting to bridge the uncomfortable gap just referred to (Madsen, 1993; Maquet et aI.,
1996; Braun et aI., 1997, 1998; Nofzinger, Minturn,
Wiseman, Kupfer, and Moore, 1997; Solms, 1997). In
this gap, new insights are now being gained into the
neural correlates of dreaming itself, and these insights
are casting a different light on the issues that confront
us (Solms, in press).
What, then, are the issues that confront us? Many
analysts might be tempted to dispute the accuracy of
Hobson's presentation of Freud's dream theory (or
indeed of his remarks about psychoanalysis as a
whole). I am not going to take up those polemics here.
I am going to recall just one aspect of Freud's (1900)
theory, one that brings us to what I think is the central
issue at stake in these deliberations. Freud believed
that there is an ongoing mental process during sleep.

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Neuropsychoanalysis: An Interdisciplinary Journal

The New Neuropsychology of Sleep: Implications for

Laboratory of Neurophysiology, Massachusetts Mental Health Center, 74 Fenwood Road,

PLEASE SCROLL DOWN FOR ARTICLE

The New Neuropsychology of Sleep: Implications

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Abstract: In his 1895 "Project for a Scientific Psychology,"

The New Neuropsychology and Psychoanalysis

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The demonstration that the human brain activation

REM Sleep Dreaming Defined

The New Neuropsychology of Sleep

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Hallucinations Especially visual and motoric, but occasionally in

Dream Motor Hallucinosis-Fictive Movement

dream narrative (Foulkes, Sullivan, Kerr, and Brown,

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The loss of memory in REM sleep makes dreaming

1987, 1989; Kandel, 1989; McGaugh, 1990, 1995;

REM Sleep Neurophysiology

The New Neuropsychology of Sleep

most strongly supports dream psychology (Kahn et aI.,

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The Reciprocal Interaction Hypothesis

C. Activation Level (A)

Figure 1. The Original Reciprocal Interaction Model of physiological

The reciprocal interaction hypothesis (McCarley

Cholinergic REM Sleep Generation

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................................... (e.g. substantia nigra pars reticulat8)

1993; Datta, 1995, 1997a; McCarley, Greene, Rannie,

Microinjection of cholinergic agonist or cholinesterase

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The New Neuropsychology of Sleep

Cholinergic (type II and III) PPT and LDT neurons

PGO input to the LGB is cholinergic (Steriade, Pare,

At the heart of the reciprocal interaction concept is

In the cat, extracellular levels of serotonin are higher

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Serotonergic Suppression of Cholinergic Systems and

Serotonergic neurons from the dorsal raphe have been

Suppression of REM by Serotonin Agonists

Microinjection of the serotonin agonist 8-0H-DPAT

Locus coeruleus neurons have been shown to become

Modification of the Reciprocal Interaction Model

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The New Neuropsychology of Sleep

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ably complementary results of these two approaches

Two very recent and entirely dependent PET studies

to be important for spatial imagery construction, an

The New Neuropsychology of Sleep

REM vs. all other stages REM vs. waking

REM vs. pre- (& post-*) REM vs. NREM 3&4

Maquet et aI., 1996

Braun et aI., 1997

Braun et aI., 1997

Nofzinger et aI., 1997

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Loss of Dreaming After Cerebral Lesions