2 the New Neuropsychology of Sleep: Implications for Psychoanalysis

This article was downloaded by: [Gazi University] On: 17 August 2014, At: 22:15 Publisher: Routledge Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK Neuropsychoanalysis: An Interdisciplinary Journal for Psychoanalysis and the Neurosciences Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/rnpa20 The New Neuropsychology of Sleep: Implications for Psychoanalysis J. Allan Hobson a a 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: 10.1080/15294145.1999.10773258 To link to this article: http://dx.doi.org/10.1080/15294145.1999.10773258 PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions 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 Hobson and Stickgold. Because the dream theory is so foundational. later. 1992. The formal and quantitative characteristics of consciousness in waking. 1994. and Hobson. 1995a). and dreaming. or remain the same. And they further encourage a detailed accounting in the separable analytic domains of the neurophysiology and psychology of the events that change. these simultaneous subjective and objective events encourage the concept of a unified system which we call the brain-mind (Kahn et aI. Steriade and McCarley. But whether or not they are accepted as firm proof of brain-mind identity. 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 . 1993. 1983. The neuropsychological analysis of the effect of brain lesions and regional blood flow changes upon the conscious states of humans.. 2. 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. 1986. and 3. 1997). The initial loss of contact with the outside world at sleep onset with its flurry of fleeting hypnagogic images. the consequences of such an avowal are profound and far-reaching. and to proclaim that the goals he set himself in that work are the very same goals we now see to be within reach. Pace-Schott. 1989. 1994. Until now. With that idea in mind let us now review the recent data. the deeply unconscious oblivion of sleep early in the night." which Freud abandoned in favor of the 1900 dream theory. it has been the cognitive similarities between waking and dreaming that have been emphasized by dream psychologists (Antrobus. The cellular and molecular level brain events that have been measured in awake. 1997a. 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.. Indeed. 1994. 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. 1995). We J. and. Moffitt. 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. and the gripping hallucinoid scenarios of late-night dreams. Foulkes. 1991). Besides being unable to account for the robust differences between wake and dream consciousness (Kahn. 1997). fall deeply asleep. sleeping. 1990. and REM sleeping animals. and in its light examine the current status of Freud's dream theory. It is within this paradigm of simultaneous conscious state and brain-state change that I now review and integrate data from three sources: 1. NREM. One face-saving approach is to revisit the 1895 "Project for a Scientific Psychology. 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. 1997). 1990. 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. Mamelak and Hobson. 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. 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.Downloaded by [Gazi University] at 22:15 17 August 2014 158 longer afford not to do so. dream. 1990. as the brain changes state. its renunciation forces a major reformulation upon the whole field. 1997). For some time. 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. this inference is now clearly in need of amendment on physiological ground~. 1988. . We have emphasized these formal aspects of dreaming because they are noted in all REM sleep dreams regardless of their specific narrative content. Pace-Schott. 1986. 1994. Cipolli. Hobson. Pace-Schott. Mullington. Jouvet. or analyzing data (Hartmann. Barrett. Merritt et aI. Rittenhouse. Mercier. places. 1995). Nielsen. Thus. Fumai. 1995). the motor cortex. Hobson and Stickgold. Kahan and LaBerge. and places are fused. Uncertainty (persons. 1988. Table 1 summarizes these feaTABLE 1 The Formal Features of REM Sleep Dreaming Downloaded by [Gazi University] at 22:15 17 August 2014 Hallucinations Especially visual and motoric.The New Neuropsychology of Sleep determine. Williams.. Hoffman.. and very poor memory. 1978. the basal ganglia. or play tennis in their dreams whether or not they have recently done any of these things in their waking lives. That dream emotion is usually consistent with the . orientational instability. 1992). or impossible). Stickgold. DoIhhoff. 1989. Narrative story lines Explain and integrate all the dream elements in a confabulatory manner (Foulkes. 1997). REM sleep). Williams. instinctual behaviors. 1985. We would then predict selective activation of the visual system.g. Deslauriers. 1995b. 1987. 1992. Nofzinger et aI. 1986). 1981. and discontinuous (McCarley and Hobson. Mamelak and Hobson. 1991. 1996. 1991. 1988. Baroncini. Gonthier. They include: sensorimotor hallucinations. Stickgold. and DeKoninck. Hobson. 1994. and Hobson. times. Dream Emotion Emotion is a subjective experience that is intensified in dreams. but occasionally in any and all sensory modalities (Snyder. 1994. and Donderi. McCarley and Hoffman. 1996). Cipolli and Poli. We expect that REM sleep neurobiology will be able to explain more about such features than it now can about specific dream content. and anger in dreams (Nielsen et aI. or subcortical motor pattern generators. appear. Fagioli. Instinctual programs (especially fight-flight) often incorporated (Hobson and McCarley. 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. 1988. 1992. 1986. and Hobson. 1997). 1989. Rittenhouse. 1992. In this case we must look for what has been added to brain function in REM. Roussy et aI. Roussy. Hobson. Revonsuo and Salmivalli. Hobson et aI. Bradley. Braun et aI. elation. 1994. 1992. To account for the documented prominence of anxiety-fear. bizarre imagery. We assume that any enhancement (or impairment) of any psychological function (e. 1988. Montangero. Bizareness Incongruity (imagery is strange. 159 tures and documents their identification and quantification. even officebound intellectuals never dream of what they do every day: sitting at their desks reading. and Salzaruo. and Hobson. diminished self-reflective awareness. Fagioli. 1991. Porte and Hobson. Revonsuo and Salmivalli. 1998). 1997b).. 1988.. wake-dream and dream-dream transitions (Cipolli. 1991. 1966. In contrast to the deficits in memory functions discussed below. or disappear rapidly). Emotions increased Intensified and predominated by fear-anxiety (Nielsen. narrative structure. 1996). Volitional control greatly attenuated (Hartmann. swim. 1992. and events are often bizarrely uncertain by waking standards) (McCarley and Hoffman. Williams et aI. and Foulkes. Stickgold. REM sleep dream consciousness routinely has more motor hallucinatory content than NREM consciousness and perhaps even more than most waking fantasy.. intensification of emotion. LaBerge. 1997. Hunt. 1992.g. Hobson.. 1999). Raymond. Merritt. 1994. 1996. and Baylor.b. unusual. plastic. Hobson. Lack of orientational stability Persons. Antrobus. 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. Rittenhouse et al. Barrett. attenuated volition. 1987. Moffitt. Memory deficits across dream-wake.. fly. Purcell et aI. 1970. Our discussion is based upon our psychophysiological theory of brain-mind isomorphism. Hobson et aI.. dreaming) will be mirrored by enhancement (or impairment) of its physiological substrate's function (e. 1987.. and Wollman. 1992). incongruous.. Hobson. We might expect to find an enhancement of those physiological processes which subserve internal visuomotor activation. and Tuozzi. and Hobson. 1981.. The neurophysiological studies and PET data from humans confirm these predictions. Delusion We are consistently duped into believing that we are awake (unless we cultivate lucidity) (Purcell. writing. Discontinuity (imagery and plot can change. Self-reflection absent or greatly reduced relative to waking (Rechtschaffen. and Pigea. 1994. 1992. Instead they ski. Merritt. the delusional belief that one is awake. 1981. Domhoff. Zadra. Goodenough.. 1997a. 1991. 1990. Reinsel. Hollifield. 1977. Blagrove. the plot may shift from feeling lost. Thus. and Geffen. 1999).1993. while some dreaming can occur in other stages of sleep (Foulkes. 1987. But we have wondered. and. Antrobus. 1986. Natale.1985. 1994.. This REM-related aminergic demodulation is best viewed as a subtraction of noradrenaline and serotonin from the varied neuromodulatory mixture facilitating waking cognition. person is a qualitatively unique feature of REM sleep dreams. of course. 1997. 1985. 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. 1992. 1985. Hasselmo and Bower.to 100-minute intervals they observed the spontaneous emergence of electroencephalographic (EEG) desynchronization. Ferrier. Other dream characters are true chimeras having some of the features of one individual and some of another. Kondo. 1992. in many human and animal studies. and Kostner. 1982. and Crow. Abel et aI. most strikingly. 1990. and Hobson. 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. 1989. 1983. Helfand. and Bertini. Cavallero. 1994). 1994. When subjects were awakened and asked to report their antecedent mental activity. 1993) which remains abundant during REM. Hobson. Bizarreness in turn reflects the hyperassociative quality of REM sleep dream consciousness. Braun et aI. 1962. These plots all satisfy the driving emotion-anxiety-while being only very loosely associated with one another. or clothing. 1987. At regular 90. Waterman. and Robbins. and Brown. Shapiro. 1995. Even the sexual identity of dream characters is fluid. more motorically animated.. Stickgold. Witte. Kerr. Rechtschaffen.. Occhionero. Weber. working in Chicago. and Sleser. 1997). and Wheaton. we look with interest at such functional deficits as the loss of noradrenergic and serotonergic modulation in REM sleep. 1983. 1963.J. 1983. Hobson. 1992. Kahn et aI. Jaret. and Kenemans. Sullivan. and Samahalski. 1988). and Zito. 1996. 1996. can be explained by viewing dream emotion as a primary shaper of plots rather than as a reaction to them (Seligman and Yellen. Sahakian. 1990.. Cahill. Eugene Aserinsky and Nathaniel Kleitman. Porte and Hobson. accompanied by clusters of rapid saccadic eye movements (or REMs) together with acute accelerations of heart and respiration rates. This is because these very neuromodulators have been shown. Allan Hobson 160 dream narrative (Foulkes. adequate equipment. Coull. Casagrande. discovered that the brian-mind exhibited periodic self-activation during sleep. 1982. Violani. and this ambiguity can be anatomically explicit. hairstyle.. 1965. The instability of time. and more bizarre accounts than NREM (Foulkes. 1987). Geffen. Kahn et aI. Middleton. and Marrocco. and McGaugh. Clark. 1992. Ogilvie. Cicogna. Verdone. for reviews see Foulkes. Quatermain. 1967. 1988) and bizarre incongruities between emotion and narrative are rarer than incongruities among other dream elements (Merritt et al. Elton. Cavallero et aI. Thus in a classic anxiety dream. Dowdy. it is REM neurophysiology which . Robbins and Everitt. REM sleep was associated with longer. 1994. more vivid. Nielson. is absent or at least greatly diminished in REM sleep. Hoffman. Antrobus. Buttinelli. Sawicki. 1995). Goodenough. Dream Amnesia and Related Cognitive Deficits The loss of memory in REM sleep makes dreaming consciousness much more difficult to recall than waking consciousness. Lewis. and Reinsel. a mixture which. This phenomenological deficit logically implies a physiological deficit: some functional process. A dream character may thus have the name of one of our friends but the wrong face. Foulkes and Schmidt. 1993. McGaugh. Pace-Schott. to missing a train. present and responsible for memory in waking. Kandel. Prins.. to not having proper credentials. place. or suitable clothing. Gordon-Lickey.. Hunt.1982.g. 1989. Lucidi. not just psychological. includes acetylcholine (e. In our attempt to explain dream amnesia. Downloaded by [Gazi University] at 22:15 17 August 2014 Dream Cognition The distinctively discontinuous and incongruous nature of dream cognition can be measured as a construct termed bizarreness (Hobson. REM Sleep Neurophysiology In 1953. 1962. 1995. 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. Frith.. 1997). Pontine REM-off cells are noradrenergically (NE) or serotonergically (5HT) inhibitory (-) at their synapses. The Original Reciprocal Interaction Model of physiological mechanisms determining alterations in activation level. Chu and Bloom. and AstonJones. 1959. Datta. Steriade and McCarley. Gomez. In this section we review subsequent work that has led to the alteration and elaboration (Figure 2) of the model. Structural Model Downloaded by [Gazi University] at 22:15 17 August 2014 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.. Morilak. Reiner. 1990). 1981). and REM must be the neurobiological substrate of the conscious experience associated with these states. 1981. 1964. . 1987. Hobson.. This spectrum of brain activity across the states of waking.Q!! NE.5HT __ .. Jacobs.Ir--4l NREM REM Figure 1. Faridi. Jacobs and Azmita. 1997). " " '\ \ REM-On I '. with NREM sleep holding an intermediate position (Figure 1).. Hobson.. Bloom. Jouvet. Activation Level (A) 1 Wake ---. '1986. we restrict our integrative efforts to the neuropsychology of REM sleep dreaming. Rasmussen. 1992). Aston-Jones and Bloom. During NREM sleep aminergic inhibition gradually wanes and cholinergic excitation reciprocally waxes. Hobson and Steriade. McCarley. McCarley and Hobson..:. and Ruckebusch. (B) Dynamic Model: During waking the pontine aminergic system is tonically activated and inhibits the pontine cholinergic system. A. 1983. and Quattrochi. 1973. - B. cholinergic system undamped) (Trulson and Jacobs.. Cespuglio. 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. 1987. Jouvet and Michel. 1992) and of their differential activity in waking (noradrenergic and serotonergic systems on. and Jouvet. 1981. Lydic.161 The New Neuropsychology of Sleep most strongly supports dream psychology (Kahn et aI. and Jacobs. McGinty and Harper. cholinergic system damped) and REM sleep (noradrenergic and serotonergic systems off. 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. The reciprocal interaction hypothesis (McCarley and Hobson.. 1992. 1986. NREM. and Lorinc. A conceptual breakthrough was made possible by the discovery of the chemically specific neuromodulatory subsystems of the brainstem (Dahlstrom and Fuxe. (C) Activation level: As a consequence of the interplay of the neuronal systems shown in A and B. At REM sleep onset aminergic inhibition is shut off and cholinergic excitation reaches its high point. . Toutain. for reviews see Foote. 1986. Dallaire. 1958. 1976. to provide a basis for our discussion of the new human imagery data in a later section. 1975. and Hobson. McCarley.. Snyder. 1983.. 1986./ '""-----' C. 1962. in the context of the reciprocal interaction concept. 1974). 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).. Calvo. and Wyzinski. 1975.. 1966.. (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.. 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... For this reason. Lydic. Dynamic Model t>-RIM. 1970. The resulting model of reciprocal interaction (McCarley and Hobson. Baghdoyan. 1974. We now devote our careful attention to a review of the cellular and molecularlevel details. While animal studies showed that potent and widespread activation of the brain did occur in REM sleep. 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. Leonard & Llinas. Greene & McCarley. ACh.. 1995.... 1996.. Sakai. Ach +0······················: 1 . McCarley et aI. EI Manseri. LOT. Sakai & Koyama. aspartate. 1997. Jones. & Morrison. 1996.. Porkka-Heiskanen. . Oakson. 1988. 1994. Annis. NE 4. 1993.. 1997a.. & Lin. 1997). Sanford. 1997. Sakai. Sakai. McCarley. McCarley. Specifically. mutually excitatory cholinergic-cholinergic interactions. serotonin. 1986. Strecker. A selection of many recent examples follows. 10) as well as other neurotransmitters such as adenosine and nitric oxide (see text) may contribute to the modulation of these interactions.. medial pontine reticular formation. & McCarley.. Mamelak. 1990. Roth. 1990a. Vanni-Mercier.. AS. Allan Hobson 162 REM Off REM On B.. and Portas.. was clearly in error.. While many of the mPRF cells are excited by acetylcholine as originally hypothesized... Sakai & Onoe. Leonard & Llinas. 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. not all pontine PPT and LDT neurons are cholinergic (Steriade et aI. 6. norepinephrine. & Koyama.. Leonard and Llinas. 1995). 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. McCarley. & Steriade. Hutcheson. gamma-aminobutyric acid. Kang and Kitai. & McCarley.. GABAergic nuclei . their own excitatory neurotransmitter now appears to be glutamate.3. 1990.. 1992b. 1988.1 . Luebke. iv. 5HT.~ 6. Strecker. 1996. 1997. 7. that the medial pontine reticular formation (mPRF) was cholinergic. Datta. Synaptic Modifications of the Original Reciprocal Interaction Model Based Upon Recent Findings. & McCarley.. Hobson and Steriade. 1994). Luebke. Steriade and McCarley. excitatory postsynaptic potentials. peri-locus coeruleus alpha. McCarley. reciprocal interaction (McCarley and Hobson. Horner. 1988) models for control of the REM sleep cycle by brainstem cholinergic and aminergic neurons have recently been questioned (Leonard and Llinas. . & McCarley. 1971...J.. NE. 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. glutamate. 1996.g.. 1975) and reciprocal inhibition (Sakai. Sakai. the self-stimulatory role of acetylcholine on pontine PGO-bursting neurons has not been confirmed in in vitro slice preparations (Leonard and Llinas. Jimenez-Capdeville and Dykes. & Hobson. 1986) LDT (Luebke. Much evidence remains.. GA!A ···t locus coeruleus +Ach 2.. AS . Leonard & Llinas. Hobson et aI.. & Bagndoyan.... 1995.. mPRF. . Lydic. 1990. LCa. Pack. GL. 1990. : ---'----. 1990). 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. Nitz & Siegel. acetylcholine. Hobon. Li. ACh has been shown to hyperpolarize cell membranes in slice preparations of the rodent parabrachial nucleus (Egan and North. 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). Sakai. 7) while inhibitory noradrenergic (4). & Jouvet. Pare. 1990. 1994. 1997.. 1993.. Datta. 9. PPT. 2. Leonard and Llinas. 1994) and PPT (Leonard and Llinas. 5. b. 1995. Thakkar. Rannie.. Portas. 1994. Curro-Dossi. Kodama & Honda. iii. 1997b. Egan & North. For example: i. 1990. Bjorkum. Datta. ? 14 7.. Datta.. Green. Cholinergic effects upon aminergic neurons are both excitatory (2). Abbreviations: open circles. as shown in Figure 2. Fleegal. Similarly. Semba... 8. 1985. References: 1. 1997). Greene. GABAergic influences (9. pedunculopontine tegmental nucleus. 1996.. For this and other reasons to be discussed below. Thakkar. 4. Quattrochi.. Kamondi. Sakai & Koyama. laterodorsal tegmental nucleus. Ach NE+Q 0 •••••••• B. 1990. & Jouvet. Yamamoto. 1992. (e... and Baghdoyan. 1986. 1993.-------. 1997a. ii. EI Manseri.: cholinergic non-cholinergic PPT and LOT mPRF and Lea +Ach ~ B. 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. The original claim. Baghdoyan.1-_ + 7. GL. 10. 1996. closed circles. Stenberg. Kamodi. Rannie. Williams. inhibitory postsynaptic potentials. 1992. Reported data from animal (cat and rodent) are shown as solid lines. 1996. and Greene. GABA ···i i • 5. 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.. that the reciprocal interaction model accurately describes essential elements of REM sleep cycle control even though some of its detailed synaptic assumptions need correction. Fleegal. Excitatory cholinergic-non-cholinergic interactions utilizing ACh and the excitatory amino acid transmitters enhance firing of REM-on cells (6. mesopontine tegmentum raphe 5-HT 3. 1997. and references are indicated by numbers (see key below). - Ach +OAch - Downloaded by [Gazi University] at 22:15 17 August 2014 '----~1. some of the recently proposed putative dynamic relationships are shown as dotted lines. GABA. 1989. Sakai & Koyama. 1993. not acetylcholine. 1991. & Reiner.. 1994. For example. 1991. Sakai and Koyama. and Reiner. & Lydic. 1997. however. 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. Greene. 1996) and cortical acetylcholine release may be as high during wakefulness as during sleep (Jasper and Tessier. Rannie. & Greene. 1996). 1995. serotonergic (3) and autoreceptor cholinergic (1) interactions suppress REM-on cells. 1986. 1994). substantia nigra pars reticulat8) Figure 2.5-HT ----. Marrosu et aI... Lydic. . glutamate. Pare. and McCarley. Datta and Siwek. 1997). and Steriade. Lydic. In rats. Day. The evidence for inhibitory serotonergic and noradrenergic influences on cholinergic neurons and REM sleep is now also quite strong. Acetylcholine Release and REM sleep Microdialysis studies show enhanced release of endogenous acetylcholine in the medial pontine reticular formation during both natural (Kodama. 1997). and Reiner. Callaway. Quattrochi. Ito. 1993). extracellular levels of serotonin are higher in waking than in NREM and higher in NREM than REM in the dorsal raphe (Portas and McCarley. and McCarley. and Deschenes. and Hobson. 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. and Smith. Velazquez-Moctezuma. Datta. Takahashi. Low amplitude electrical stimulation of the LDT enhances subsequent REM sleep (Thakkar. 1990). Neurotoxic lesions of pontomesencephalic cholinergic neurons reduce the rate of PGO spiking (Webster and Jones. 1988). 1994).. and Lydic. Baghdoyan..b. Winston. Datta. 1986). 1980). and Wilkinson. Winston. Minznberg. and both PPT and LDT neurons show specifically c-fos and foslike immunoreactivity (Fos-LI) following carbachol-induced REM sleep (Shiromani. In addition to these short-term REM induction sites. The excitatory amino acid. it has been difficult to enhance REM sleep with carbachol (Deurveiller. 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. 1988). In addition to the well-known suppression of REM by muscarinic antagonists (Hobson et aI. and can be antidromically traced to pontine PGO-burst neurons (Sakai and Jouvet. and Hobson. Mamelak. Decreased Serotonin Release in Natural REM Sleep In the cat. 1990a. Cholinergic Mediation of PGO Waves PGO input to the LGB is cholinergic (Steriade. This same state-dependent pattern is observed in the hypothalamus of the rat (Auerbach. and Lorine. 1996) suggesting that they participate in the genesis of that state. 1997). Portas. 1995. and McCarley. 1996). Gillin. Malik. Datta. and McCarley. 1989. Matsuyama.Downloaded by [Gazi University] at 22:15 17 August 2014 The New Neuropsychology of Sleep Rodrigo-Angulo. Quattrochi. 1996). Imeri. and Mori. 1994) and the medial pontine reticular formation (Iwakiri. 1991) REM sleep. 1992. Steriade. McCarley. and Hobson. the new presynaptic anticholinergic agents have also been shown to block REM (Salin-Pascual and Jimenez-Anguiano. 1996). carbachol injection into a pontine site in the caudal peribrachial area has been shown to induce long-term (over seven days) REM enhancement (Calvo. 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. Bagh- 163 doyan. 1995. and Lynn. 1991). 1989. Hobson et aI. Calvo. Hans. 1989.. Capece. and Hobson. Efange. Quattrochi. 1988) and PGO waves· can be blocked by cholinergic antagonists (Hu. Bouhassira. 1987. Pare. and Hobson. and Honda. Thalamic ACh concentration of mesopontine origin is higher in both wake and REM than in NREM (Williams. and Hobson. 1993). but rat strains which are genetically supersensitive to ACh show enhanced REM sleep (Benca et. when microinjected into the cholinergic PPT. Yamamoto. Parent. . increases REM sleep in a dose-dependent manner (Datta. Dauphin. and Hennevin. VanniMercier. 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. Stimulation of mesopontine neurons induces depolarization of cortically projecting thalamic neurons (Curro-Dossi et aI. 1990) and carbachol-induced (Lydic. Quattrochi. Comisarow. 1989. 1993). and Shiromani. Shiromani. Fibiger. 1991). Both muscarinic and nicotinic receptors participate in the depolarization of thalamic nuclei by the cholinergic brainstem (Curro-Dossi. Sakai. and a REM-specific increase of ACh in the lateral geniculate body has been observed (Kodama and Honda. aI. 1992. 1997b. and Morrison. Mesopontine injection of a serotonin agonist depressed ACh release in the lateral geniculate body (Kodama and Honda. Sanford.. Reignier. Vogel. 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. 1995). and Aston-Jones. 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. 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. 1997). 1997). 1990). et aI. 1997). Allan Hobson lakov. 1997) as well as in the cat and rat (Hobson and Steriade. 1997) while the alpha-l receptor may be the most important site for adrenergic REM suppression (Ross. Pack. and Mancia. 1975. 1996). norepinephrine. 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. Gentili et aI. Sanford. reduced extracellular serotonin concentration in REM sleep has recently been demonstrated in the human amygdala. 1996). presynaptic nicotinic facili- . Annis. 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. and Morrison. 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. Like cholinergic enhancement. 1989. J. 1992.. Serotonin has been shown to hyperpolarize rat cholinergic LDT cells in vitro (Luebke et aI. in the McCarley laboratory (Li et aI. Gresch... Kubin. 1994). the following elaboration of reciprocal interaction has been proposed by Li et ai. or both (Vogel. have been proposed for the brainstem control of REM sleep. hippocampus. 1997). 1997). and Cirelli. Buffenstein.. it can be inferred that the human limbic system is turned on but demodulated during dreaming. Clavenna. and McCarley. 1994). 1996) and the cat (Tononi. Giglio.. Minter. which are consonant with recent findings. Rainnie. and Davies. Moreover. 1994). Suppression of REM by Endogenous Norepinephrine and its Agonists Locus coeruleus neurons have been shown to become quiescent during REM in the monkey (Rajkowski. 1994). 1991. and Pascoe. Nicholson. 1994) and to reduce the proportion of REM sleep in vivo (Horner. All such modifications retain one or both of the major tenets of the reciprocal interaction model: cholinergic facilitation and adrenergic inhibition of REM. Electrical stimulation of the pons in the vicinity of the (noradrenergic) locus coeruleus reduced REM sleep in rats (Singh and Mallick. From recent in vitro studies in the rat. 1996). 1986). Serotonin has been shown to counteract the REM-like carbachol-induced atonia of hypoglossal motoneurons (Kubin. 1991) while the noradrenergic antagonist idazoxan increases REM when injected into the pontine reticular formation of cats (Bier and McCarley. Okabe and Kubin. Tojima. Downloaded by [Gazi University] at 22:15 17 August 2014 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. During waking. Such a mechanism is depicted in Figure 2. Si- Modification of the Reciprocal Interaction Model Modifications of simple reciprocal inhibition or interaction models. Thakkar. Leonard and Llinas. Reignier. 1996.. 327). and Hennessy. Pompeiano.. aminergic suppression of REM sleep is now an established principle. 1994) and systemic injection of 8-0H-DPAT into serotonin-depleted rats also suppresses REM (Monti et aI. The alpha-2 noradrenergic agonist clonidine suppresses REM in human subjects (Nicholson and Pascoe. Ivanova. Belyavin. Pack. orbitofrontal cortex and cingulate cortex (Wilson et aI. 1994) and LDT (Sanford et aI... 1996). 1994. Ball. 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. Since most of these structures show selective activation in PET images of REM sleep.164 DeSimoni. 1978a. At the same time. 1993. This suggests that the exponential self-stimulatory activation which can be triggered by cholinergic stimulation in diverse mesoand medial pontine sites (Hobson and Steriade. It seems possible. Steriade and McCarley.... 1995). 1989. 1993. and Jouvet. Sakai and Koyama. Hobson. Hobson and Steriade. 1996. central gray area (Sastre. 1997). 1990.. Wyatt. 1990. 1988. we do not exclude the contributions to the modulation of behavioral state of other neuromodulatory systems such as GABAergic systems (Nitz and Siegel. adenosinergic systems (McCarley et aI.. 1997). and Morales. Steriade and McCarley. 1995). Solms. In contrast to the hyperpolarization of some mesopontine cholinergic neurons by cholinergic agonists. 1976. glycinergic systems (Chase. when the locus coeruleus is silent. Soja. and Gillin. By restricting our discussion to cholinergic and aminergic mechanisms. for example.. 1997). 1991. the experimental study of human REM sleep dreaming has been limited on the physiological side by the poor resolving power of the EEG. While the studies we have reviewed here are necessarily restricted to data obtained in subhuman models of REM sleep. in the form of strokes. Luebke et aI. 1990. 1994. Human Neuropsychology Until recently. 1975. and Elmquist. We now turn our attention to new. glutamatergic systems (Qnoe and 165 Sakai. Such cholinergic self-regulation combined with cholinergic-noncholinergic mutual excitation is schematized in Figure 2. Hobson et aI. EI Manseri et aI.. 1997). 1986. Gillin. 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. The remark- . this same presynaptic nicotinic input may facilitate serotonergic self-inhibition by the raphe neurons themselves. Roth et aI. Sherin. 1986. Nor do we exclude the contributions of numerous nonpontine structures such as the basal forebrain (Szymusiak. Kodama and Honda. Nicholson et aI.b. and Stickgold. 1995. Moore. 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.. 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. Sakai and Koyama. Ross. the amygdala (Sanford. Sutton. 1994. Sakai. 1989).. 1997. have allowed the locale of brain lesions to be correlated with deficits or accentuations of dream experience in patients (Doricchi and Violani. Buda. 1993. very similar. 1996). or the medulla (Chase and Morales.. experiments of nature.Downloaded by [Gazi University] at 22:15 17 August 2014 The New Neuropsychology of Sleep tation of excitatory locus coeruleus noradrenergic inputs to the dorsal raphe enhances serotonergic firing. 1990. This limitation has probably reinforced the erroneous idea that the brain activation picture of REM sleep and waking are identicalor. 1997). Tejani-Butt. 2000). hypothalamus (Saper et aI. 1986. Vogel et aI. and Ruiz. During REM. Baghdoyan et aI. Fortunately. an abundant psychopharmacological literature provides indirect evidence that the same mechanisms operate at the cellular and molecular level in the human brain (Sitaram. 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. 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. 1986. Sakai et aI. Kitahama. 1990) may involve excitatory neurons which are noncholinergic. histaminergic systems (Saper. and Morrison. Rather. 1996). 1990. 1996. more direct evidence supporting the assumptions of cross-species homology. 1990). 1997). 1995). 1996. 1995). nitroxergic systems (Leonard and Lydic. thalamic nuclei (Mancia and Marini. at least. or the neuropeptides (Bourgin et aI. 1997). It is important to realize that many of the studies questioning reciprocal interaction (Egan and North... (2) cholinergic mechanisms are essential to REM sleep and come into full play only when the serotonergic and noradrenergic systems are inhibited. 1997). 1990). Datta. These other systems are reviewed elsewhere (Kahn et aI. 1990). and Gillin. Pace-Schott. we emphasize here those aminergic and cholinergic mechanisms associated with the executive control of REM sleep in reciprocal interaction/inhibition models (McCarley and Hobson. Leonard and Llinas. 1992) have been carried out on in vitro rodent models. in vitro studies have shown the majority of medial pontine reticular formation (mPRF) neurons' to be depolarized by carbachol (Greene and McCarley. 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). 1997). Sitaram.. Dawson. Perry and Perry. a possible role for the basal ganglia in the rostral transmission of PGO waves is suggested. 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. 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. showed relative activation of the pons.. those cortical areas activated in REM are rich in afferentation from the amygdala (anterior cingulate. the Braun group offered the following speculations which are relevant to the neurology of dreaming. the caudate. parahippocampal.. (1996) used an H2150 positron source to study REM-sleep activation in their subjects who were subsequently awakened for the solicitation of dream reports. 1997). 3. 1. the midbrain. the hippocampus. The strong REM sleep-related activation of the basal ganglia suggests that these subcortical structures may play an important role in ascending thalamocortical activation. 1997. In addition to the pontine tegmentum. 1988. and inferior temporal cortices in REM sleep as compared to each of the above three conditions (Table 3). 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. for the first time. Based on these observations. 2. and Leslie. PaceSchott. Stickgold. the anterior hypothalamus. 1997) emphasizes. in REM. Braun et aI. Maquet et aI. Maquet et al. 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 Downloaded by [Gazi University] at 22:15 17 August 2014 KEY: 1 Increase.. significant activation was seen in both amygdalae and the anterior cingulate cortex (Table 3). Nofzinger et aI. Maquet et aI. Maquet and Franck. despite the general deactivation in much of the parietal cortex. 1996). right parietal operculum) while those areas with sparse amygdalar afferentation (prefrontal cortex. . 1997. 1977). 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. Braun et aI. - 1 1 ! 1 1 (right) ! No Change. (1997) replicated the Maquet group's findings of a consistent REM-related brainstem. and precuneus) were deactivated in REM.. Porte and Hobson. 1997.. The basal ganglia may initiate motor activity and be related to the ubiquity of hallucinated motion in dreams (Hobson. anterior cingulate. 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. Maquet et aI. of emotionally influenced memories (see also Braun et aI.. Hobson. ably complementary results of these two approaches are summarized in Table 2. caudal orbital. 1997). When REM-sleep brain activity was compared to brain activity in delta NREM. reported activation of the right parietal operculum-a brain region thought to be important for spatial imagery construction. Instead of the global. and the medial prefrontal. interpreted their data in terms of the selective processing. 1 Decrease. In another H2150 PET study. As Maquet (Maquet and Franck. and paralimbic activation. an important aspect of dream cognition. parietal cortex. 1997).166 J. limbic. 1996. regionally nonspecific picture of forebrain activation that had been suggested by EEG studies. with presleep waking and with postsleep waking. Maquet et aI. the experimental animal data on the critical and specific role of the pontine brainstem in REM-sleep generation. This is an important advance because it validates. Significantly. 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. At the same time these new studies also provide important new data for our understanding of dream synthesis by the forebrain. 1996). I. 1997) .46. 47 R: 8. 11. 1996 H2150 Braun et aI. 9. Lat increase increase increase increase increase: A. R-right hemisphere.innominata) Cerebellum increase increase increase: L increase: R. 19 increase increase: 24 decrease: 31 increase increase: R 32 increase: 24 dec: R sm.-lateral. S-superior. sub. NREM 3&4 sleep waking Study Technique Maquet 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. all numerals = Brodmann's area *Change relative to both pre.and postsleep waking (Braun et aI. 10. A-POA anterior preoptic area. L increase Cortical Areas Frontal Dorsolateral Prefrontal decrease: L: 10. 11. all other stages REM vs.. A-anterior. (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. 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.(& post-*) REM vs. Lat. I-inferior. 1997 18PDG Downloaded by [Gazi University] at 22:15 17 August 2014 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. 46 increase increase: 11. waking REM vs. P-posterior. pre. areas increase: 25 increase: L increase inc. C-caudal.167 The New Neuropsychology of Sleep 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.. 1997 H 2150 Braun et aI... 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. M-medial.. we suggest an alternative explanation. Pawlik. Gore. 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. 1191). and Truett. Vs or V6 ).. a similar decrease in cerebral blood flow to frontal areas during REM J. An equally interesting H 2Is Q PET finding. This dorsolateral prefrontal deactivation during REM. orientation. FDG study and this discrepancy remains to be clarified. Figure 3 integrates findings from these first three PET studies comparing REM sleep to other states. 1997). anterior thalamus and paralimbic cortices. Puce. 1997) this area of research can be expected to provide more detail in the near future. the Braun group has recently suggested that REM constitutes.. 1997). This medial area. Confirming the widespread limbic activation of the human brain in REM. Solms. 1996. Ives et aI. and memory during dreaming was significant deactivation.. 1997). 1997) another common. appear to be activated during REM sleep. Disruption of this area has been shown to cause confabulatory syndromes formally similar to dreaming (Braun et aI. Using the finer time-resolution offered by functional MRI (fMRI) imaging (Huang-Hellinger et aI.. relevant to the cognitive deficits in self-reflective awareness. dream feature. Allan Hobson had earlier been noted (Madsen et aI. With respect to the visual imagery aspect. 5. in the cortex. the inferior temporal cortex (Brodmann areas 19 and 37) contains the fusiform gyrus. and V4 but not VI. often result in a distinctive syndrome in which dreaming increases in vivacity and reality and dreaming become confused (Solms. The fact that considerable portions of executive and association cortex are far less active in REM than in waking led Braun et aI. cited the much earlier single subject report of a PET glucose activation of limbic and prelimbic structures in REM (Heiss. and Wienhard. 1991). V 3a. however. prelimbic. Braun et al. 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. Based upon the difficulty of suppressing REM by experimental lesions of the pons in animals. Nofzinger et aI. has been associated with arousal and attention. "The largest area of activation is a bilateral confluent paramedian zone which extends from the septal area into ventral striatum. The authors suggest that an important function of REM sleep is the integration of neocortical function with basal forebrain hypothalamic motivational and reward mechanisms.. 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. 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. appears to be activated only in a partial or fragmentary way" (p. Sutton et aI. who was apparently unaware of the recent PET studies. Braun et aI. of a vast area of dorsolateral prefrontal cortex (Maquet et aI. Interestingly. infralimbic. which has the most abundant limbic connections in the prefrontal cortex. especially the neighboring anterior cingulate.. the prefrontal or 'association' loop. was not replicated by the Nofzinger et aI. Interestingly. orbitofrontal and anterior cingulate cortex" (p. 1985). Nofzinger et aI. connecting the caudate. 1998). However. lesions of the anterior limbic cortex. in REM. Herholz. a structure known to be involved in human face recognition (McCarthy. note that.Downloaded by [Gazi University] at 22:15 17 August 2014 168 4. 1190). Using SPECT. Solms (1997) also-reports that his patients with pontine lesions continued to dream and concludes that the pons is not necessary for human dreaming. dorsomedial thalamus and prefrontal cortices .. 1997).... Wagner. 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. From these findings as well as primary visual cortex deactivation in REM. 1995. It seems to us that any lesion . if often bizarrely uncertain.. suggest further that "the 'limbic' loop connecting ventral striatum. 1997. 192). (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. In terms of cortical-subcortical networks.. 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).. (1997) described increased glucose utilization in the lateral hypothalamic area and the amygdaloid complex using an I8F-fluoro-deoxyglucose (FDG) PET technique (Table 3). in turn. 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. FDG PET activation of anterior medial structures. ascending activation pathways and multimodal association cortex). 1997). Additionally. Braun et aI. (Hong. Such processing may.. The instigation of dreaming was. 1996... and cortical..g.. Nofzinger et aI.. 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. 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. including the anterior cingulate and medial frontal cortex. capable of destroying the pontine REM sleep generator mechanism would have to be so extensive as to eliminate consciousness altogether. 1989). Dow. Even the visual hallucinosis of dreaming was viewed by Freud as a "regression to the sensory side" . 1996. the cingulate cortex has consistently shown increased activation in REM in other PET studies (Buchsbaum et aI. 1997. In order to protect consciousness from disruption (which would otherwise lead to awakening). residual brain activation is at a low level hence dreaming is less intense and less sustained. Braun et aI. and Braun studies (Maquet et aI. Maquet and Franck. Additional findings support this proposed cortico-limbic interaction. 1997). caused by the upsurge of unconscious wishes following suspension of their wake-state repression. 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. Braun et aI. 1988. 1997. whereas in REM the brain activation is as vigorous as that in waking but that activation is both biochemically and regionally differentiated from waking. 1997.. and symbolization were called into play. We would now say that dreaming is caused by brain activation during sleep.. 1997). Second. determined by the disguise and censorship of the unconscious wishes. 1997. Nofzinger et aI. Freud's Dream Theory Revised in the Light of Modern Sleep and Dream Research Dorsolateral Prefrontal Cortex Downloaded by [Gazi University] at 22:15 17 August 2014 • Activated in REM ~ Deactivated in REM Emotionally Salient Memory Processing Concerning the functional significance of the imaging results. limbic-related cortex.. In NREM sleep. The depicted areas in this figure are thus most realistically viewed as representative portions of large eNS areas subserving similar functions (e. Wilson. 1997). Maquet.. 1997). 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... 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. 1996... Nofzinger et aI. Gillin. 1997. limbic structures for the adaptive processing of emotional and motivational learning (Maquet et aI. account for the emotionality and psychological salience of REM sleep dreams (Hobson. Engel. and Buchsbaum. Braun et aI. Nofzinger et aI. 1991). 1995). Wu. all three of the image study authors assign REM sleep a role in the processing of emotion in memory systems (Maquet et aI. and Bragin. it is equally possible that activation of these structures reflects the limbic and paralimbic activity in REM suggested by the Nofzinger. 1995). as shown in Table 3. condensation. Finally. The regional activation during REM may reflect a specific activation of subcortical. for Freud.. The bizarre character of dreaming was.The New Neuropsychology of Sleep 169 Figure 3. 1997). Note that considerably more extensive areas of activation are reported in the individual studies and these more detailed findings are given in Table 3. 1996. such defensive processes as displacement. Some support for this comes from a PET (glucose) study showing correlation between content-analyzed dream anxiety and medial frontal activation (Gottschalk et aI. Simmons. 1997). Convergent Findings on Relative Regional Brain Activation and Deactivation in REM Compared to Waking.. Maquet and Franck. for Freud. First.. state-dependent amnesia compounded by the global aminergic demodulation and the deactivation of working memory mechanisms in the dorsolateral prefrontal cortex.. these new neuroimaging and brain lesion studies strongly suggest that the forebrain activa- . 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. dream hallucinosis results from a feed-forward conveyance of data about motor intentions to the sensory processors in the upper brain. This cortex vs. As is well known. For the reform-minded psychoanalyst. Activation-synthesis says that both the dream forgetting following awakening and the defective episodic memory that occurs within dreams is a simple. Amnesia for Dreams. and means of coping with. Freud ascribed dream forgetting to repression. 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 strong implication is that far from being a feedback regression to the sensory side. A major reason for this shift must be that.Downloaded by [Gazi University] at 22:15 17 August 2014 170 that served to neutralize the impact of the unconscious wishes on consciousness. 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. 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. 1996]) as the primary product of limbic lobe activation. not defensive as Freud asserted. Merritt et aI. In this sense anxiety (and the two other prominent dream emotions. J. and anterior cingulate gyrus activation in human REM sleep). While dreaming. parahippocampal cortex. it favors the view that dreams are. together with the limbic lobe activation. The emotional character ofdreams was not easily dealt with by Freud's theory. Thus dreams are not properly thought of as simply visual but more accurately as visuomotor. 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. and parietal cortical regions taking precedence over the dorsolateral prefrontal cortex). 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. but rather the direct result of both bottom-up activation processes (which also convey information about brainstem/eye movement commands). corticocortical activation processes remains to be clarified. in part. The visual nature ofdreams is for activation-synthesis. elation and anger) can be seen as major dream plot organizers and shapers of the emotional salience of dreams. The presence of dream anxiety also inveighed against his "guardian of sleep" functional hypothesis. Allan Hobson Activation-synthesis has always regarded anxiety (which is the leading emotion in all dreams and all dreamers [Nielsen et aI.. and the global shift in the biochemical mode of information processing (caused by the noradrenergic and serotonergic demodulation) also contribute to dream bizarreness. the seat of the executive control of cognition in the dorsolateral prefrontal cortex is deactivated in REM! But let us make no mistake. anxiety (where anxiety is viewed as an inherent. the transparent exposure of an individual's cognitive associations to. 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. even these postarousal recollections are evanescent probably because it takes several minutes to reinstate waking cognition. 1991. 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. The distinctive regional activation pattern of the forebrain (with limbic. The degree to which primary vs. From the Neuron to the Dream: Freud's Project Realized Taken together. limbic system construct in no way vindicates disguise-censorship nor does it support any interpretive scheme that carries any trappings of that dogma. secondary unimodal and multimodal cortices mediate dream vision and the relative influence of subcortical--cortical vs. This speculative hypothesis has now received powerful support from recent PET studies (showing amygdala. 1994. existential emotion that is designed to interact with cognition in an adaptive if disruptive manner). we never sit and watch but are constantly moving through dream space. On the contrary. Domhoff. Why repression was needed if the dreams had already been bowdlerized by disguise and censorship was never made clear. paralimbic. 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. 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). the PGO waves. 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. cholinergic Nucleus Basalis of Meynert). 2. The mechanism of the brainstem triggering of forebrain activation involves the spontaneous excitation of cholinergic neurons in the pontomesencephalic LDT and PPT nuclei. and (c) the memory deficits. volition. The Distinctive Nature of Dream Cognition The selective activation process described above may account for such distinctive cognitive features of dreaming as: 1. 3. The intense and vivid visual hallucinosis.g. The intense emotions. and (b) Limbic and paralimbic structures. these findings greatly enrich and inform the integrated picture of REM sleep dreaming as emotion-driven cognition with deficient memory. a result of the excitation of forebrain circuits by impulses arising in the ascending activation systems of the brainstem (e. 4. the presumed substrates of visual imagery in dreaming. due to the combined and possibly related effects of aminergic demodulation and the selective inactivation of the frontal cortices. parietal and limbic zones with a selective inactivation of frontal regions. 1977). The brain activation which underlies dreaming is. due to an orientational instability caused by: (a) the chaotic nature of the pontine autoactivation process and its sporadic engagement of association cortices. 3. 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. elation. This activation process prepares the forebrain to process data with associated cognitive awareness. like that of waking. 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.. 2. the lack of directed thought. But REM-sleep brain activation differs from that of waking in three important ways: 1. that have two targets of particular relevance to dream theory: (a) The lateral geniculate body and posterolateral cerebral cortex. the loss of self-reflective awareness. and actions. we are in a much stronger position to strengthen the brainbased theory of dreaming first proposed twenty years ago (Hobson and McCarley. especially anxiety. Whatever the link between the neuromodulatory and regional blood flow data. (b) the absence of frontal cortical monitoring. and the lack of insight about illogical and impossible dream experience. 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. The bizarre cognition of dreaming which is characterized by incongruities and discontinuities of dream characters. due to the autoactivation of the amygdala. There is selective activation of occipital. loci. A unifying neurobiological hypothesis is that the regional blood flow changes are causally linked to the neuromodulatory dynamics in the following way.. pontine and midbrain reticular activating systems) and basal forebrain (e. the presumed substrates of emotion and emotionally salient dream memories. and anger. The delusional belief that we are awake. Not only is REM sleep chemically biased. orientation. due to autoactivation of the visual brain.171 Downloaded by [Gazi University] at 22:15 17 August 2014 The New Neuropsychology of Sleep tion and synthesis processes underlying dreaming are very different from those of waking. and more medial limbic structures. and analytic thinking.g. . 1985. t5HT Chotinergic neurons on tAch Figure 4. Table 3 and Hobson et aI. it is also quite possible. memory consolidation mode. But if we recall that it is consolidation. McCarley. and dopamine (Flicker.... emotionally salient) (Hobson. Input Source (I). 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. Hobson and Stickgold. Frith et aI. The emotional salience of dream imagery (due to the activation of the paralimbic cortices by the amygdala).e. On this view. 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. Of course. Physiological Signs and Regional Brain Mechanisms of REM Sleep Dreaming Separated into the Activation (A). At first glance. and M during REM sleep dreaming are noted adjacent to each figure. especially serotonin. 1982. bizarre) and transparently meaningful (i. 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. Kandel.. At the same time. 2000). 1981. not acquisition that is hypothetically enhanced..172 J. 1983. that a key aspect of memory consolidation involves emotional salience. Visuospatial imagery Downloaded by [Gazi University] at 22:15 17 August 2014 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. 1995). 1992a. 1997a. Quartermain. 1986. I.. Libet. 1990. and Modulation (M) Functional Components of the AIM Model (see Hobson.e. . 1992. Abel et aI. Kandel and Schwartz. the dream is the often meaningless sometimes meaningful noise that is made when the brain enters its active.. 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. Allan Hobson Activation Dream Forgetting Parietal operculum . 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. 1989. the instigation of emotionally salient memories is probably also just that. 2000 for additional anatomic details). 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. Cellular and molecular level studies of learning and memory all concur in supporting a role for the aminergic neuromodulators. Hobson et aI. this failure to record intercellular transactions would seem to be at odds with the enhancement of learning hypothesis advanced in the next section. 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. 1895). 1995a). and even probable. Dynamic changes in A. Montarolo et aI. and Hobson. Without their mediation. Hence dreams may be both nonsensical (i. norepinephrine. 5.. 1984. 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. and cholinergic controllers of the NREM/REM sleep cycle would affect blood flow as well as neuronal excitability and second messenger functions. in so doing. 1995b. 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. 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. With the onset of sleep. and other manifestations of the motoric. 173 research must therefore be to test this hypothesis at both the basic science and clinical levels. the restoration of cognitive capabilities such as attention and the enhancement of such learning processes as memory consolidation are of particular interest (Cai. 1997. classic nightmares. With this decline. consciousness abates. in part. Awakenings from Stage IV sleep are difficult to achieve. and Bloch. 1996. This approach. it seems quite likely that the noradrenergic. both in clinical and personal terms if one discounts the bizarreness and attends to the undisguised emotional content. It withdraws its cathexis from the waking world and. 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. 1995. 1995. The Occurrence of Nightmares and Night Terrors The occasional occurrence of night terrors. 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. 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. If that were the case. which has a functional significance for cognition that cannot easily be deduced from dream content. A New View of Dreams and Nightmares Based on Neurobiology Freud said the ego wishes to sleep. Hars. Crick and Mitchison. At the depths of NREM sleep. Giuditta et aI. Hennevin. and as a result they then evince a confusion akin to dementia or delirium. 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.. Askenasy. Karni. Smith. 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. serotonergic. releases the unconscious from its repressive vigil. subjects are likely to awaken only partially. and Sagi. 1995. From the neurobiological point of view it seems more likely that it is REM sleep itself. which is straightforward and requires no interpretation. and not the subjective experience of dreaming. and autonomic storm that can arise in . 1995. 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. We regard the testing of this memory consolidation hypothesis as a most promising area of ongoing research on sleep and dreaming. supplemental. emotional. Among the many interesting theories that have been put forth. 1995. Maho. Kavanaugh. Since they are the central incarnation of the peripheral autonomic nervous system. They are therefore potentially informative.Downloaded by [Gazi University] at 22:15 17 August 2014 The New Neuropsychology of Sleep 1988). 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. Indeed. 1997). 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. neuronal activity through the brain's core activating system declines. this part of the story is. Hobson and Stickgold. may be well undertaken without mediation but it may also be facilitated by a sympathetic interlocutor. But note. Abundant evidence is fast accumulating to indicate that both NREM and REM sleep benefit learning and memory. And it shows that all mental products have both a meaningful (read emotionally salient) and nonsensical (read chaotic) aspect. and when the data are out of register. the ultradian 90. For the progressive psychoanalyst this point might be reframed in a more general. telling us only what a subject's mental state might be like if he or she were to become delirious. 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. 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. sustained. stereotyped process that is now well understood at the cellular and molecular levels. The Functions of REM Sleep and Dreaming Any functions of dreaming must be clearly distinguished from the functions of REM sleep. it does mean that automatic processes of a primitive and presumably subcortical origin can be released in NREM sleep. 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. True. The ad hominem argument that anyone who is skeptical of psychoanalytic . the progressive analyst must be encouraged and supported rather than punished for dissidence. Like the circadian rhythm of sleep and waking. want to promote. 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). dream content might be quite ir- J. It shows that the propensity to psychosis is natural and universal. On the contrary. What about more intermediate level functions. It shows that all psychoses are both functional and organic. This oscillator causes the brainmind to change its activation structure and both the flow and mode of information processing are accordingly reversed. This self-activation is a complex. This method. But it is at the cognitive level that the most intriguing reframings must proceed. In this sense it is already clear that dreaming is epiphenomenal with respect to the most fundamental biological adaptations of REM sleep. • 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. and distinctive character because of the shift in the mechanism of activation from aminergic-cholinergic (in waking) to exclusively cholinergic (in REM sleep). Downloaded by [Gazi University] at 22:15 17 August 2014 Dreaming in REM Sleep Periodically throughout sleep the brain self activates.174 NREM sleep might seem to be an exception to this rule. psychoanalysis. It is because his basic theory was both wrong and incomplete. so clearly circular as to be practically worthless if scientific validity is a goal. As these mental functions are the coin of the realm in any psychology. 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. During REM sleep. Now we see why. heuristic manner: REM sleep dreaming is didactic! It shows the doctor and his patient what psychosis is like. Allan Hobson relevant. We have already detailed many of the implications of this finding for dream theory.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. 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. 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. there is still no evidence of disguise or censorship. Here again. but two important implications remain to be amplified. including psychoanalysis. dreaming assumes its most intense. In this sense. must be seamlessly complemented by the vast range of techniques from single-unit recording in cats to PET scans in humans. & Wilkinson.. & Kleitman.. R. Varga. 414:245-261.. Baldwin. as did Freud. 77:351-360. G. O. S.. A.. Acetylcholine (ACh) release in the medial pontine reticular formation is regulated by M2 muscarinic autoreceptors. B. . C. M. 1:876-886. ed. M.. (1992).. • 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. A. Neuropsychopharmacol. A. (1953).Rodrigo-Angulo. REM and NREM sleep reports: Comparison of word frequencies by cognitive classes. Hamon. Brain. Auerbach. Belenky. M. A. 2:67-69. D. ed. Y. what is needed is not revision but complete overhaul.. J. (1997)... (1998). 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. (1997). Belenky. F. & Reinsel. Neuropsycholog. L. Increased basal REM sleep but no difference in dark induction or light suppression of REM sleep in Flinders rats with cholinergic supersensitivity. A.... C. Askenasy. Balkin. M. Lebrand. Antrobus. 175 Hayaishi & S. & McCarley. Minznberg. D. M.. Brain Res.. M.... 20:562-568. Huang. Gaultier.. (1997). N. that psychoanalysis is a research tool and then charge people for it as if it were medical treatment. Overstreet.. Vasoactive intestinal polypeptide microinjections into the oral pontine tegmentum enhance rapid eye movement sleep in the rat. Dreaming. N. J. & Adrien. F. D. Escourrou. & Obermeyer. S. 2:221-228. Hollifield. (1983). 4:275-299. J. Abstr...Gwady. H. R.. Baghdoyan. . M.. . 279:91-95. Science. Scripts and the structuralist analysis of dreams. Because there is essentially nothing left of the Freudian hypotheses. M. Brain Res. Ghirardi. Consciousness & Cognit. Extracellular serotonin and 5 hydroxyindolacetic acid in hypothalamus of the unanaesthetized rat measured by in vivo dialysis coupled to high performance liquid chromotography with electrochemical detection: Dialysate serotonin reflects neuronal release. Regularly occurring periods of ocular motility and concomitant phenomena during sleep. Alberini. 499:281-290.. Brain Res. P. & Herscovitch. P. R.. J. L. T. M. (1987). (1996). Pharmacol. we see recourse to the relativistic claim of narrative truth.. & Foulkes. Dreaming.Lydic. R. Nguyen. 15:45-51. P. O. J.. Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle. 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. Braun. Franc. Carson. 118:361-375. B. A neuroanatomical gradient in the pontine tegmentum for the cholinoceptive induction of desynchronized sleep signs. Bergman. J.. T. . R.. 634:333-338. A. Soc. Russell. REM-enhancing effects of the adrenergic antagonist idazoxan infused into the medial pontine reticular formation of the freely moving cat. H. Wesensten. (1992). W.. Dissociated pattern of activity in visual cortices and their projections during human rapid eye movement sleep. D. D. & Kandel. Science. J. Fleegal. Carson. 2:23-37. M.. A corollary of this principle is that it is unconscionable to claim. The carbachol induced enhancement of desynchronized sleep signs is dose dependent and antagonized by centrally administered atropine. M. E. W. J. Selbie. To survive and to have any claim to universality psychoanalysis needs to democratize as well as to diversify." References Abel... 298-325.. Visual skill consolidation in the dreaming brain. M. (1997). G... P.. pp. & Hobson. J. New York: Academic Press.. Steps toward a molecular definition of memory consolidation. R. (1981).. Aserinsky. R. J... A. pp. L. Reflection during REM dreaming. & Sagi. In: Sleep and Sleep Disorders: From Molecule to Behavior. & Lydic.. Neurosci. An H2150 PET study. Neurosci. R. Karni. (1989). W. In: Memory Distortion. B. R. E. what is worse. Bradley.. C. E. Schacter. E. Gilliland.. . E. Suggested further readings are indicated by an asterisk (*).. S.. 23:2131. Varga.... J. L. (1995). Baldwin. 2:161-166. Dreaming in the late morning: Summation of REM and diurnal cortical activation. P... M.. McCarley. (1994). 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Thakkar. Soc. Soc. Stickgold. Sakai. T. L.. however. 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. including the mechanism of REM sleep. Quattrochi. M. I don't have any disagreement with Hobson's understanding of the essential physiological mechanisms underlying the sleep-waking cycle.. I am not going to take up those polemics here. J.. it is now possible to bridge this gap. Braun et aI. D. only the brainstem component has been well understood. However. MA 02115 The New Neuropsycholog)r of Sleep Commentary by Mark Solms (London) Allan Hobson is the leading authority on the neurophysiology of REM sleep dreaming. & Hobson. Soc. using the insights that modern neuropsychological methods and neuro-imaging techniques can provide into the neural organization of all higher mental functions. and Associate Member of the British Psycho-Analytical Society. I am going to recall just one aspect of Freud's (1900) theory. as manifested objectively (apparently) by REM sleep. C. REM sleep is a state with many components. A. I do disagree with his understanding of the psychology of dreams based on those physiological mechanisms.. Neurosci.. and his work has dominated this field for more than twenty years (McCarley and Hobson.. J. Nofzinger. Freud believed that there is an ongoing mental process during sleep. Prevalence of auditory. November 7. olfactory and gustatory experiences in home dreams. Solms. Gordon-Lickey. 1998. Minturn. 1997). in press). 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.. Yamamoto. In this gap.. A cholinoceptive desynchronized sleep induction zone in the anterodorsal pontine tegmentum: Spontaneous and drug-induced neuronal activity. K. 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). E. J. R. I am going to structure what I have to say around six questions which I would like to pose to Professor Hobson. Mamelak. & Donderi. Nielsen... 1975. A. (1990a). L. & Marrocco. Obviously. However. 1998:"The New Neuropsychology of Sleep: Implications for Psychoanalysis. A. 1993. & Motor Skills. (1992). . Kupfer.. 1996. Zadra. Lecturer. What. Pharmacological depletion of catecholamines modifies covert orienting in rhesus monkeys. Percep. T. A cholinoceptive desynchronized sleep induction zone in the anterodorsal pontine tegmentum: Locus of the sensitized region. 18:537. . There has always been an uncomfortable gap between the psychological approach to dreams. I will focus selectively on one or two things that I think are of central importance. 39:279-293. as Hobson himself acknowledges.(1990b). subjectively by patients. one that brings us to what I think is the central issue at stake in these deliberations. 39:295-304... Neurosci. Hobson and McCarley." Mark Solms is Hon. A. Hobson has covered a vast area of knowledge. and this is ushering in a new era in this field. 1997. A. and thereby starting to bridge the uncomfortable gap just referred to (Madsen. Allan Hobson Laboratory of Neurophysiology Massachusetts Mental Health Center 74 Fenwood Road Boston. This omits a lot else that is also of interest. Abstr.... N. S1. Neurosci. and these insights are casting a different light on the issues that confront us (Solms. Maquet et aI. Recent findings concerning the neuropsychology of dreaming. E. psychology is what interests psychoanalysts most... new insights are now being gained into the neural correlates of dreaming itself. but until recently. then. It will not be feasible for me to address all of the points that he raised. T. Wiseman. including a forebrain component. Bartholomew's and Royal London School of Medicine. In his paper.. 87:819-826. and the physiological approach to dreams. Academic Department of Neurosurgery. 1977).. J. 1997.183 Commentary on The New Neuropsychology of Sleep Downloaded by [Gazi University] at 22:15 17 August 2014 Witte. (1998). need to be reconciled with the old physiological findings. and Moore.