Dream Bizarreness As the Cognitive Correlate of Altered Neuronal Behavior in Relm Sleep

Dream Bizarreness as the Cognitive Correlate of Altered Neuronal Behavior in RElM Sleep

Adam Mame&& and J. Hobson

N. Allan Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/1/3/201/1755575/jocn.1989.1.3.201.pdf by guest on 18 May 2021 Laboratory of Neurophysiology Harvard Medical School

Introduction Perhaps the best known theory is attributed to Freud (1900) who argued in the Interpretation of Drams that One of the most pronounced and distinctive features of dream bizarreness reflects a motivated effort to disguise our dreams is the occurrence of impossible, improbable, subconsci~conflicts in symbolic constructs. and illogical phenomena which are collectively referred With the discovery of rapid eye movement (REM) sleep to as dream bizarreness. Over the centuries many the- (Aserinsky and Kleitman 1953) and the conskquent corre- ories have attempted to explain the nature and signif- lation of REM sleep with dreaming (Dement and Kleitman icance of dream bizarreness (Lavie and Hobson 1986). 1957), a neurobiological basis of dreaming was estab-

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Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1989.1.3.201 by guest on 30 September 2021 lished. This neurobiological approach was embodied in ble or impossible dream events as real, the emotional the activation-synthesis hypothesis (Hobson and McCar- spectrum of dreaming, and our dimculty with dream re- ley 1977) which argued that dreaming was the cognitive call (unless we awaken from REM sleep). In light of byproduct of a physiological state, REM sleep, in which these parallel developments we can now attempt to con- the major source of input or “drive”was not, as Freud had struct a more con@eteand formal model of the dream suggested, psychological dissonance but rather “random” synthesizing process, focusing specifically on those neu- neural activity.’ ral processes which may contribute to the bizarreness of The activation-synthesis hypothesis of dreaming was dream mentation. the first theory which accounted for dream formation Our reason for concentrating on the bizarreness of

from a well-supported neurophysiological viewpoint, the dreams is twofold. (1) While dream content is unique Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/1/3/201/1755575/jocn.1989.1.3.201.pdf by guest on 18 May 2021 reciprocal interaction model of sleep cycle control (Hob- to an individual dream, dream bizarreness is a formal son et al. 1975; McCarley and Hobson 1975; McCarley property shared by all of them (Hobson et al. 1987; Hob- and Massaquoi 1985). By describing how the inhibition son 1988). As such, we can analyze the physiological of certain neuronal populations was coupled with the basis for the process without considering the highly vari- excitation of others to produce the behavioral and elec- able content of individual dreams. (2) While many de- trographic signs of REM sleep, it suggested that the hu- tails of human REM sleep are not fully understood, two man mental correlate of REM sleep, dreaming, could like- physiological correlates of this mammalian brain state are wise be explained neurophysiologically. The activation- relatively undisputed: (a) the near complete cessation of synthesis hypothesis relied upon physiological arguments nucleus locus coeruleus (LC) and dorsal raphe nucleus to explain distinctive features of dreaming such as hallu- (DRN) neuronal discharge and (b) the appearance of cinosis, emotionality, and amnesia. Unfortunately, not pontogeniculooccipital (PGO) waves. Since evidence ex- enough was then known about either the cognitive pro- ists to support the view that these processes also charac- cesses themselves or the changes in underlying neuronal terize human REM sleep (McCarley et al. 1983; Miyauchi activity across behavioral states to test some of the hy- et al. 19871, we have good reason to expect them to potheses of the activation-synthesis model. directly contribute to the unique aspects of dream men- Since the original formulation of the activation-synthesis tation. hypothesis, neurophysiological advances have been made which help us to better understand the neuronal basis of DefhhgDreamBluUreness REM sleep. In addition, computer simulations of theoreti- To focus our discussion of the physiological systems cal neural systems have provided insight into such cogni- that we think may underlie distinctive aspects of dream tive processes as learning and memory (MacGregor 1987; cognition, we first define what we mean by “dream Kanerva 1984; Kohonen 1984; Hopfield 1982; Harth et al. bizarreness.” In their initial investigation of 40 dream 1987; Ackley et al. 1985; Anninos et al. 1984; McClelland reports, McCarley and Hoffman (1981) loosely defined and Rumelhart 19861, and some of these have been sub- bizarreness as “any event that was unlikely or improba- stantiated in biological systems (Crow 1988; Abrams et ble.” Acknowledging the inherent subjectivity in terms al. 1988; Shepherd 1979). such as “improbable”or “unlikely,”Hobson et al. (1987) The study of dreams has also advanced. By comparing next developed a quantitative bizarreness scoring system the characteristics of home-based reports (in which indi- that, when applied to 110 dream reports, was able to viduals record their recollected dreams in bedside jour- group all bizarre items into three major classifications: nals or on tape recorders) with those collected in sleep (a) discontinuity (i.e., times, persons, places, and actions laboratories, it can be confidently concluded that most may suddenly change without notice), (b) incongruity long and detailed narratives of mental experience with (i.e., aspects of persons, places, and activities do not fit distinctive formal features described below are the cog- together), and (c) cognitive abnormalities (i.e., non se- nitive experiences of REM sleep. This means that much quiturs, ad hoc explanations, and explicit vagueness or more extensive, more naturalistic, and more inexpensive uncertainty of dream thoughts). This scoring system for data is now available for analysis. dream bizarreness is outlined in Table 1. Coinciding with this shift in data source is a shift In one sample of 60 dreams, 465 bizarre items were in analytic paradigm from the second-to-second cross- identified (inter-rater reliability 0.90); of these, 9.3%were correlation model of sleep lab physiology (where, for ex- plot discontinuities while 44.5%were plot incongruities. ample, the relationship of gaze direction in the dream can These two features could affect the plot itself or the be correlated with eye movement direction as recorded dreamer’s thoughts about the plot. on the polygraph) to a more global state-testate cross- An example of a plot discontinuity, taken from a scored correlation approach (where the intensity of visual hal- sample of 72 NREWREM paired dream reports (Antrobus lucinosis in a dream can be correlated with the rapid 1983a1, is the following scene shift: eye movement density in REM sleep). Other formal features of dreaming that are amenable to analysis in this “. . .which I also throw behind a bush and for paradigm include the uncritical acceptance of improba- some reason he takes off his jacket, the detec-

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Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1989.1.3.201 by guest on 30 September 2021 Table 1

TWO STAGE SCORING SYSTEM FOR DREAM BIZARRENESS

Stage I identifies items as bizarre if they are physically impossible or improbable (probability of occurrence < 0.05) aspects of: Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/1/3/201/1755575/jocn.1989.1.3.201.pdf by guest on 18 May 2021 A. the plot, characters, objects or action B. the thoughts of the dreamer or dream character C. the feeling state of the dreamer or dream character

This stage establishes the dream domain or report locus of each item of bizarreness.

Stage II then characterizes the item as exhibiting:

1. discontinuity (change of identity, time, place, or features there00 2. incongruity (mismatching features) 3. uncertainty (explicit vagueness)

This stage establishes the character of each item of bizarreness.

tive does, and puts it down somewhere . . .and cognitive feature which is highly state specific. at this point the whole thing is switched to some- As mentioned above, plot incongruity was the most where else with different Characters so I think it‘s common (44.5%) source of dream bizarreness found by the whole, you know, different thing, urn -some- our earlier analysis. It may be flagrant as in the following thing, to a street, or a street with a lot of rubble description (see again Figure 1 and item 19, Table 2): piled on each side - the street sort of - a desolated kind of street, and there was a car going “As we wandered aimlessly about we suddenly down the street. . . ” saw the Customs Building, straight in front of us. It was a three-story building of white stone This scene change is an example of a global discon- with “ramps” on the outside apparently to en- tinuity in which place, time, and characters all suddenly able animals to reach the upper stories.” change without apparent reason. But more subtle and partial discontinuities also occur. For example, in the While physically possible, such ramps are a distinctly following dream excerpt, the dreamer’s nephew is de- incongruous architectural feature and this item is scored scribed as follows: as a plot incongruity. More subtle, but still definitely bizarre is the peculiar association of the Customs Build- “. . .no one in sight except my companion, a ing, usually specialized in controlling imports, with an child of perhaps 6 to 8 years, who later turned animal pound (item 10, Table 2). For example: into Jason, but who, at first, seemed like a stranger.” “It was at the Customs Building where all animals (except small ones such as cats) must be This example, taken from the dream journal report il- registered or declared, weighed, and the proper lustrated in Figure l and entered as item 4 in Table 2, tax paid.” is typical in its reflection of the loss, in dreaming, of the orientational unity that characterizes wake state menta- Dream incongruities occur more frequently than dis- tion. Even in fantasy (or day dreams) characters rarely continuities but are somewhat less striking, since the change identity. We therefore regard discontinuity as a narrative thematic constancy of the dream is typically

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Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1989.1.3.201 by guest on 30 September 2021 In this example the "littleJewish memorial candle" and the "black light that you use for psychedelic art" are perhaps logically linked as ceremonial objects but distinctly incongruous in the context of a camping trip. Since ev- eryone is asleep it is not clear why candle light would be needed, and one would certainly not use a Jewish memorial candle or a black light for heat. Thus the candle incongruity is not resolved by the dreamer's ad hoc explanation of their utility. In a related example, in an

effort to explain why he is having trouble locating the Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/1/3/201/1755575/jocn.1989.1.3.201.pdf by guest on 18 May 2021 Customs Building, the dreamer states:

"I remember thinking it was probably in some other part of town."

Likewise, the explanation for the use of the "ramps" in the example given earlier is both ad hoc and improbable (it being far more likely that an elevator would be used to reach the upper stories). But the use of the term "apparently" by the dreamer makes it unclear whether this explanation was established during the dream or upon reflecting about the purpose of these bizarre ramps while Figure 1. Ph&phic repduction of a page in a dream awake. We regard these cognitive aspects of bizarreness, journal giving a narrath and a pictorial account of a which are scored as uncertainties, as secondary in that dream about a Customs Bdldhg which the dream- and his nephew seek, and- in downtown Washhgton. As they constitute either illogical or explicitly vague and in- illustrated in Table 2,24 separate items of bhrreness adequate attempts by the dreamer to explain the bizarre were scored in the podon of the text shown, including plot events which we regard as primary and emphasize in the sudden transformation of the dreamers nephew (plot discontinuity), the ramps (plot incongruity), and the ad this paper. Because it is unclear to us whether these cog- hocexplanationfortheiruse(cognitiveincongruity). See nitive uncertainties are intrinsic to REM sleep, or rather text for dlscussioa CReprodUcad with permission &om represent ad hoc explanations advanced in the wake state Hobson 1987.1 et al. reporting of the dream, we do not specifically address this type of bizarreness in our present physiological model. Nonetheless, it should be emphasized that thought pro- maintained (Rechtshaffen 1978). In the following exam- cesses can be every bit as deranged in dreaming as our ple, the objects listed as candles don't really fit together perceptual and orientational faculties. in the context of a camping trip.

" ...I was, ah, holding a match, eh, I was ly- ing in bed and I was holding a match . . .wait, Neumcogdtive Models: Basic Premtses in the it was in a tent, it wasn't in bed, it was in Brain-Mind Isomorphism a tent and some of my friends were there So that our model may be properly interpreted, it is im- and we were all in sleeping bags - we were portant to make clear the connection we draw between camping out and, eh, I was looking at all brain activity and mental activity. We explicitly assume the different candles that we had . . . eh, to that the isomorphism between brain and mind is com- give off heat and light the tent - everybody plete, so that any form of mental activity - such as a was asleep except for myself and the can- memory, thought, motor response, or sensation - can dles were next to me and one was a . . .one be equivalently represented at the brain level by some of the candles was a memorial candle ...it aspect of neuronal activity. We admit that this is a large was a little Jewish memorial candle another assumption, but it is a widely accepted working paradigm one was, eh . . .another one was, eh, wasn't among cognitive neuroscientists, and one we feel is es- a candle - it was a black light that you sential to make if we are to begin to explain the physio- use for the psychedelic art which Emily had logical basis of the complex mental activities which con- brought who was there and Emily is this girl- tribute to dream bizarreness. friend of mine from like three years back who In beginning to build a bridge between dream bizarre- was, eh . . . " ness and REM-sleep neurophysiology, we note certain

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Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1989.1.3.201 by guest on 30 September 2021 isomorphisms - or similarities of form - between prevented from enacting motor commands due to the the psychological and the physiological domains. muscular atonia induced during REM. This cognitively First, we are struck by the fact that although dream active, environmentally isolated, and demodulated brain bizarreness is a constant feature of REM sleep dreams, it is further stimulated by frequent volleys of PGO neuron is seldom noticed by the dreamer who appears to have input, as evidenced by the appearance of PGO waves lost the self-critical, supervisory control of waking cog- throughout the forebrain. nition. The constancy of bizarreness suggests an equally Associated with these electrographic and neuronal constant change in brain function and the inability to changes are the bizarre images of our dreams. The detect this bizarreness further suggests that the change uniqueness of REM dreams is evidenced by the obser-

represents a loss of some wake state brain function. In vations that non-REM (NREM or slow-wave sleep) men- Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/1/3/201/1755575/jocn.1989.1.3.201.pdf by guest on 18 May 2021 addition to the obvious loss of external data that occurs tation reports are much shorter and lack the detailed in sleep generally, we are struck by the almost total loss imagery present in wake or REM mentation (Antrobus of aminergic neuromodulation in REM sleep and will de- 1983b). At the same time, they are less bizarre even when velop below our reasons for considering this neurobio- the lower word count is taken into consideration (Porte logical defect to be isomorphic with the cognitive defects and Hobson 1986) so that deactivation alone cannot be of dreaming. the main cause of bizarreness. Wake-state day dreams or Second, most individual bizarre elements or events ap- fantasies exhibit less bizarreness than REM dreams (Hob- pear to be embedded in the plot itself, at or near what son, unpublished preliminary data). we might call the sensorimotor level. For example, in the Of the various neurophysiological features of wake- Customs Building dream we consider the perception of sleep states, only three - the muscular atonia, the ces- the dreamer’s companion initially as a stranger and later sation of LC/DRN discharge, and the intense PGO burst- as his nephew, their ”wandering aimlessly about,” and ing - are unique to REM sleep. Since muscular atonia their sudden appearance in front of a stone building with is effected by post-synaptic inhibition at the level of the ramps to be sensarimotor events. To explain these sen- spinal cord, it is unlikely to influence cortical processes sorimotor aspects of dreaming we suggest that an inter- directly, and we therefore assume it is not a major influ- nal mechanism such as the activated reticular formation ence upon dream bizarreness. Conversely, because the of the brain stem and its PGO wave system provide the other two systems constitute significant sources of input sensorially deafferented forebrain with a constant stream and/or modulation to the cortex, it is reasonable to sug- of excitation, which in some way mimics the role of ex- gest that these systems may constitute the physiological ternal data in wake-state information processing. basis of dream bizarreness. Third, we are impressed with the loss of orientational stability illustrated by many bizarre items, perhaps most Neurobioloey of Aminergic Demodulation notably in discontinuities such as the examples listed ear- In this section we discuss the neurobiology of the nor- lier. The unities of time, place, and person that charac- adrenergic and serotonergic systems, with special refer- terize wake state mentation are given in part by environ- ence to the hypothesis that aminergic demodulation is mental constancy, but derive also in part from the internal a root cause of diminished neuronal predictability and continuity of memory, attention, and thought. Since all that this physiological feature in turn contributes to in- these cognitive functions are deficient in dreaming, we congruities and related features of dream bizarreness at postulate deficits in their neuronal underpinnings. This the cognitive or psychological level. psychophysiological assumption is indirectly bolstered A summary of the properties and functions of the nor- by the classic clinical observation that disorientation of adrenergic and serotonergic systems is shown in Table the sort seen in dreaming is also seen in organic mental 3. Because of their central location in the pontine brain syndromes caused by toxicity or dietary deficiency (Ka- stem (Aghajanian et al. 1968; Foote et al. 1983), their plan and Sadock 1985). widespread projection to the forebrain and spinal cord (Foote et al. 1983; Sakai et al. 19771, and their chemical specificity (Aghajanian et al. 1975; Aston-Jones and Neurophysiology of the Sleepwake Cycle Bloom 1981; Lydic et al. 1987a, 1987b), the noradrenergic Figure 2 reviews the major behavioral, electroencephalo- locus coeruleus and the serotonergic raphe systems have graphic, and neuronal changes that occur during the been called “a brain within the brain,” signalling their in- sleep-wake cycle. To summarize these features, REM ternal regulatory functions. NE has been implicated as a is a behavioral state in which the cortex is at least as modulatory factor essential to hippocampal and cortical electrically active as it is during waking, but operates in learning Uarbe et al. 1986; Sara 1985; Everitt et al. 1983 the absence of the modulatory neurotransmitters nore- Flicker et al. 1981; Bear and Singer 1986) and to atten- pinephrine (NE) and serotonin (5HT), as evidenced by tional mechanisms (Schmajuk and Moore 1985; Carli et al. decreased locus coeruleus and dorsal raphe nucleus dis- 19831, and to faithful information transfer from thalamus charge rates. It is deprived of external stimuli by a va- to cortex (McCormick and Prince 1988). NE has been riety of sensory inhibitory mechanisms, and is in turn shown to facilitate the generation of long-term potentia-

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BIZARRENESS SCORING IN ONE DREAM

Item Bizarrephrase BizamenessClass score

1 none of which seemed large plot incongruity A-2 2 seemed large cognitive uncertainty B-3 3 perhaps 6 or 8 years cognitive uncertainty B-3 Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/1/3/201/1755575/jocn.1989.1.3.201.pdf by guest on 18 May 2021 4 who later turned into Jason plot discontinuity A- 1 5 [companion]who, at first, seemed like a stranger plot incongruity A-2 6 seemed like a stranger cognitive uncertainty B-3 7 thinking that it . . . was in some other part of town cognitive incongruity B-2 8 thinking that it . . . was in some other part of town cognitive discontinuity B- 1 9 very probably was in some other part of town cognitive uncertainty B-3 10 Customs Bldg. where all animals . . . declared plot incongruity A-2 11 (except small ones such as cats) plot incongruity A-2 12 (Customs Bldg.) . . . (animals) . . . weighed plot incongruity A-2 13 (Customs Bldg.) . . . (animals) . . . proper tax paid plot incongruity A-2 14 train stopped . . . animals must be brought . . . taxed plot incongruity A-2 15 some person cognitive uncertainty B-3 16 some ‘person we were looking for plot discontinuity A-1 17 had brought an animal from train to the Customs Bldg. plot incongruity A-2 18 we suddenly saw the Customs Bldg. . .. in front of us plot discontinuity A- 1 19 Bldg. of white stone with “ramps”on outside plot incongruity A-2 20 apparently cognitive uncertainty €3-3 21 apparently to enable animals to reach the upper stories cognitive incongruity B-2 22 (though . . . clear that all weighing . . . basement) cognitive incongruity B-2 23 We entered Bldg. somehow (not by means of ramps) plot incongruity A-2 24 somehow cognitive uncertainty B-3

tion (LTP) of synaptic efficacy in hippocampal pyramidal rate of neurons (Aghajanian and Van der Maelen 1986). cells (Hopkins and Johnston 1988) and may thus be an But again, as with NE, there are instances in which 5HT important modulator of synaptic plasticity. We consider can evoke increases in neuronal discharge rates (McCall the loss in REM sleep of these neurotransmitter substrates and Aghajanian 1979; Aghajanian and Van der Maelen of wake state attentional and mnemonic functions as pos- 1986). Decreased DRN discharge typically results in a sibly isomorphic with the cognitive defects of dreaming, reciprocal increase in spontaneous activity of brain ar- especially the inability to remember dreams. eas receiving DRN input (Haigler and Aghajanian 1974; In many instances NE acts as an inhibitory neurotrans- Lydic et al. 1987a, 1987b; Ruch-Monachon et al. 1976a, mitter (Foote et al. 1983) but NE can also facilitate neu- 1976b; Hobson et al. 1983). For example, DRN neurons ronal discharge if a neuron is receiving sufficient excita- project to the area identified as a PGO wave output center tory input (Hopkins and Johnston 1988; Bjorklund and (Sakai et al. 1977; Vivaldi et al. 1980). As DRN discharge Lindvall 1986). On these grounds, Segal (1985) has ar- decreases, PGO neurons spontaneously burst and PGO gued that the LC, by way of inhibiting spontaneous ac- waves can be recorded in the EEG of cats. tivity while potentiating the responses of “relevant”activ- The psychotomimetic drug lysergic acid (ED) is a ity, acts to increase the signal-to-noise WN) ratio during structural analog to 5HT which depresses the firing be- learning. In the hippocampus, for example, NE enhances havior of DRN neurons (Aghajanian et al. 1968; Haigler responses to stimuli that predict reinforcement, while ex- and Aghajanian 1974). Studies support the view of Jacobs tinguishing responses which represent background activ- et al. (1976) that, in the absence of serotonergic modula- ity (Segal and Bloom 1976). tion, activity in visual, limbic, and other brain structures Serotonin is also considered to be an inhibitory neu- becomes disinhibited. This disinhibition results in hal- rotransmitter in that it diminishes the spontaneous firing lucinatory episodes (Aghajanian et al. 1975; Ferguson et

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F@UW 2. Behavi~ral,-qmphic, and neuiOnal chnnSes p88odBtcd with the Sk wake cycle. (A) a- iorallywake is chrvactcnlzed byfreqwnt movement, logical thoughts, and acauate percepL of externnl stirnull. NREM is chra&&dbyepisodic poaure shifra and limb movements, aogicalbut nonpmgressive Wnking, and a sparsenessofimagery. REMsleepis-bythenearcom leteabsenceofbodymovtments,anddrcamswhkh areascomp~and-asw-stoee~ugh~,bptwith~thinLlnPandMzBmpercep*s. [Adnptcdftom Hobson and Steriade 1986.1 (B) phicchmgescomlateweJlwithbehavioralchangceocrossstrrtes. Muscle tone, as meamredbye-WG), is -tin- and absent in- with= in-, come- SPnZwith the ivelossofmovementseenh.omw&ngtoREM.CortkalEEGisas~inREM asin (Hobson!* 1986), correlating with the complexity of thought and vividness of hnqery obsemed in both states. During NREM high amplitude delta (1-4 Hz)waves which are comlatedwithdecreadmean neuronal fLrins rates appear in the cortex (Hobson and Steriade 19861, as do s indle complexes, 7-14 Hz odlhtbm prodpced whenthe thalamus is functionallydisconnectedfromcortex(Surlpd:etd 1987). These~onscomlstcwell with the low kvel of mental activity and lackof dream imageryqxnted in NREM. EOG potentials arc common to bothREMand~butare~absentinNREM.Inwake,theseEoGsieprrsenteye~~~external stimult, while! in REM they appear to be gendintemaUy(NeES0n et al. 1983). PGO waves are absent in NREM and can be tecordedinwake in assodntlonwithastartle response. In contrast, chistas of PGOwaves can be ircofded in the brain stem, thalamus, cortex, and some subadd structws (Cahwayet at 1987) during REM. Since few environmental stimuli reach the brain, it is udkelythat these PGO waves represent a redkive compomst ofthe startle response (Bowker and Morrison 1976), but ratha operate in REM as a8ouire of exdtptfontothe forrbiafa Wpted ftom callnway et aL 1987.1 (C) At the nem0nal-h coetuleus (ILC), the principal source patine (NE) to the forebinin and the dol.sal raphenuclerrs 0,the princllwlaourceof semtenh(5Ifi) bothOf =3z t their highest rates of tonic dsbchryp inwake. During NREM LC andDRNfirinsrates aredemeamlto 50% ofwake state kvcls, but inREM theLC andDRN cease fivinsalmostcompletely,mnovingthe In&Knas of NE and 5HT ftom forebmh processes (McGinty and Harper 1972; McGinty and Harper 1976Xm1974; Hobson et at 1986). Vertical axis is mean neuronaldidwge rate per minute. Spike traine are recotdedfiroma single cat DRN neuron. [Adapted fhmHobson et aL 1983.1

al. 1969). The qualitative similarity between REM sleep that the hallucinatory and disinhibited nature of dreams dreams and ED-induced hallucinosis, and the correlation may be related to the withdrawal of 5HT from the fore- of both with decreased serotonin in the brain, suggests brain during REM.

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AMXNERGIC NEUROMODULATORY SY!TIXW

Norepinephrine Locus Substantia Cerebral Learning Wake: High Tonic Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/1/3/201/1755575/jocn.1989.1.3.201.pdf by guest on 18 May 2021 (NE) Coeruleus Nigra Cortex Discharge Memory Increased Spinal cord Hippo- phasic campus Attention discharge in presence Fastigial hYgaa of noxious Cerebellar Increased stimuli Nucleus Cerebellar signal-noise Cortex ratio Central NREM: 50% drop Gray Area Thalamus Facilitate in discharge LTP gener- from wake Hypothalamus Hypothalamus ation in levels Hippocampus Contralateral REM cease firing Lc Inhibit REM sleep Stria Terminalis Inhibit PGO generation hygdaloid Complex

Insular Cortex

Serotonin Dorsal Other raphe Hypothalamus Inhibit Wake: High "pacemaker" (5HTl Raphe Nuclei "spontaneous discharge rate, Some Thalamic activity not influenced Locus Nuclei of forebrain by =-ry Coeruleus circuits stimuli Globus (especialy Pontine Pallidus motor NREM: 50%dropin Central Gray and visual) discharge from Striatum wake levels Substantia Nigra Hippocampus Inhibit REM REM: cease firing sleep Hypothalamus Neocortex Inhibit PGO Lateral Mammillary generation Habenular MY Nucleus

Madeling the Effects of Aminergic Demodulation and cognitive psychology. Such a model is suggested While the correlation of aminergic withdrawal with hal- by evaluation of a computer simulation by Clarke et al. lucinatory cognition and/or increased spontaneous neu- (1985) in which the spontaneous or stochastic behavior ronal activity suggests that at least some elements of of neuron-like elements (or "neuromimes") is explicitly dream bizarreness may be attributed to the cessation of modeled, thereby allowing us to assess postulated varia- LC and DRN firing, we need a more formal model of this tions in response caused by state-specific fluctuations in process if we are to attempt to integrate neurophysiology catacholamine levels.

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Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1989.1.3.201 by guest on 30 September 2021 Imagine a neuron i (Figure 31, which can be in one of of neuronal responses reflects the quanta1 release of two states at any time, “firing”or “silent.” Let si(t) be the neurotransmitter, leakage of neurotransmitter from pre- state of the neuron at time t: synaptic terminal boutons, spatial and temporal integration of post-synaptic potentials, local ionic concentra- si(t) = 1 if neuron i is firing tions, threshold variation via accommodation and refrac- toriness, and other such dynamic variables (see Ganong si(t) = 0 if neuron is silent i 1977 for a review of the properties of ~ynapticcommuni- cation). For stimuli that produce membrane potentials far This reflects the all-or-none action potential response (> 10 mv) above or below threshold, responses of post- exhibited by neurons. A neuron receives input from synaptic neurons are generally very predictable on the Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/1/3/201/1755575/jocn.1989.1.3.201.pdf by guest on 18 May 2021 N,presynaptic afferents (labeled 1,2,3.. .j . . . N> and a basis of statistically averaged values of synaptic weight, measure of the synaptic coupling strength between any threshold potential, and refractory period length. But re- two neurons can be stored as the value of the synaptic sponses to stimuli that produce near-threshold potentials weight Wij from neuron j to neuron Let pi repre- are more difficult to predict owing to the uncertainties sent the membrane potential (relative to the threshold inherent in neural dynamics. potential, Voi, a model neuron develops at time t). The It should be stressed that we do not intend to imply membrane potential pi(t + 2’) is defined as: a rigorous link between the specific model neuromimes presented here and the role of aminergic demodulation in dream bizarreness. Other realistic neural simulations that are equally amenable to modeling the effects of aminergic demodulation on neuronal responses could be constructed (see MacGregor 1987). We choose these particular neuromimes for illustration purposes, simply because they exhibit greater similarity to biological neurons than most simulated neuron-like elements in which synaptic weight from j to i, < 0 for the influences of noise have been investigated (Keeler inhibitory synapse, > 0 for excitatory synapses decay constant of membrane; exp[-t/~oil = residual charge on neuron i from past excitations action potential firing threshold function that prohibits the neuron from firing more frequently than its absolute refractory period R time step between updates in the computer simulation

Note that if neuron j is silent, it cannot exert any synaptic influence on neuron i because then Wijsj = 0 regardless of the value of Wij . Whether a neuron fires in response to a value of b is Figure 3. A schematic view of a single idealized neuron (or neuromime) with three synaptic afferent inputs used determined by the explicit form of an activation function to model the influence of aminergic modulation on neu- which reflects the dynamics of action potential genera- ronal interactions. A neuron s, receives afferent input tion in a simplistic sense because membrane ion conduc- from N input neurons s,, where denotes the index of a particular input. The strength of the synapse between tances, dendritic interactions, etc. are ignored. Clarke neurons, which reflects an average value of the amount of et al. (1985) suggest a probabilistic activation function, neurotransmitter released with each depolarization of J, meaning that for a given membrane potential pj, there is is stored in the value of the synaptic ”weight” W,,. The response of s, is determined by the value of its “membrane an associated probability pi that a neuron will fire: potential” pl,which is determined by the sum weight of all active synaptic inputs, the residual membrane potential on 8% from past events, exp[-t/q,,l, and a threshold value Kt. The value of the membrane potential is then used to determine the probability of a neuron firing, according to the spectfic shape of the activation function used in the A probabilistic activation function mirrors the behav- model (see text and Figure 4B). Since the membrane potential determines only probabilities of firing, the system ior of neurons in that neurons exhibit variability in their has stochastic dynamics and is thus amenable to studying moment-to-moment responses. The probabilistic nature the effects of aminergic modulation across states.

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Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1989.1.3.201 by guest on 30 September 2021 et al. 1989; McClelland and Rumelhart 1986). Critical determined by pre-synaptic input. Output patterns in to this discussion is only the use of a probabilistic ac- these neural circuits will represent "true" responses to tivation function such as the one demonstrated in equa- afferent stimulation because there is little chance that tion (1.21, in which the sigmoid shape of that func- potentials slightly below threshold will cause firing, and tion is varied by a scale factor (or function) that reflects likewise little chance that potentials slightly above thresh- the level of catacholaminergic neurotransmitter present. old will not cause firing. The system is very "predictable" All other aspects of the model are purely descriptive in at the neuronal level and the concomitant associations are function. "tight" at the cognitive level. The scale factor a used in this discussion is analo- If, on the other hand, the response to near-threshold

gous to the role of temperature employed in the study synaptic input is less predictable due to the absence of Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/1/3/201/1755575/jocn.1989.1.3.201.pdf by guest on 18 May 2021 of thermodynamic systems. Many connectionist models aminergic modulation during EM, then the chance of use thermodynamic temperature and energy as an anal- a neuron firing or not firing "accidentally" is substan- ogy to study network responses to probabilistic behavior. tially increased. A single neuron firing in response to With regard to cognitive neuroscience, perhaps the best subthreshold stimuli, or not firing in response to above- known of these are the Boltzmann Machine (Hinton et threshold stimuli, is equivalent to making a mistake at al. 1984) and Smolensky's Harmony Theory (1986). Since some level in the net. Distributed over thousands of our model is significantly distinct from these thermody- neurons in a net, some of which are output neurons, namic models in both form and function, we use the the overall response pattern produced at any given time term a in this discussion to avoid confusion with such in a dream could be different from the response of the approaches. net to identical afferent stimulation in a well-controlled, How might the modulatory influence of the aminer- aminergically modulated regime simply because the per- gic systems affect neuronal responses so as to determine centage of neurons responding incorrectly increases in the quality of dream mentation? Although the full de- the absence of NE and/or 5HT. The cognitive equivalent tails of the mechanism(s) governing aminergic modula- of this result could be a loosening of associations as ob- tion still elude us, its influence upon neural dynamics served in dream incongruities. A schematized view of is suggested by the shape of the activation function in this process is shown in Figure 4D. equation (1.2) (Figure 4B). For any membrane potential From a slightly more mathematical point of view, one there is an associated probability pi that neuron i will fire could imagine associating each possible output response (pi(si = 1)). This probability is dependent on the value of a network with a numeric probability which reflects of pi and a modulatory scale factor a. The value of a the likelihood that a given output will be generated in determines how sharply sloped the activation function response to a specific input. When aminergic modula- response curve is in the vicinity of the threshold poten- tion is high (wake), there are most likely only one or two tial, and a can therefore be considered a scalar quantity output patterns with high probability for each input. In that determines the reliability of neuronal behavior. If a REM sleep, these output probabilities are altered due to is a very small value (e.g., a = 0.5) then for pi just slightly the state-specific loss of aminergic modulatory control so above or below threshold, the neuronal response is eas- that many output patterns are generated with equal prob- ily predicted with a high degree of reliability. As a gets ability for a given input. Some of these outputs would larger, the mid-portion of the curve takes on a more hor- presumably seem bizarre in the context of the remainder izontal slope, and so the responses of neurons are much of the dream imagery. harder to predict on the basis of membrane potentials Returning now to the topic of dream bizarreness, in- alone, which in turn is largely determined by the synap- congruity is favored by a brain state in which neuronal tic weights of afferent inputs. network output responses are less tightly associated with, One can visualize aminergic demodulation as a means but not unrelated to, the incoming afferent neuronal ac- of shifting the explicit shape of the probability curve from tivity. A reported image such as the Customs Building deeply sloped to flattened (e.g., in Figure 4C a shift from with "ramps" on the outside could well reflect the physi- a = 0.5 in wake to a = 8 during REM). Thus for mem- ological response of the networks which, upon receiving brane potentials that are near threshold, the behavior of a an input pattern that during wake typically generate an neuron would become less predictable during REM sleep image of a white stone building with a first floor ramp, than during waking, with NREM intermediate. exhibit a greater degree of error in the absence of NE We now consider how withdrawal of aminergic modu- and/or 5HT. This results in some output neurons failing lation could account for the incongruities found in dream to "properly" fire in response to above-threshold stim- reports by influencing neural responsiveness at the level uli, while other neurons fire "erroneously" in response to of local circuit neurons. If the behavior of a localized subthreshold inputs. Cognitively this is manifested as the brain network or circuit is well controlled by aminergic bizarre image of a ramp that has two levels and reaches modulation (as in waking), then the probability that a incongruously up to the third floor of the Customs post-synaptic neuron will fire is determined almost en- Building. tirely by the membrane potential, which in turn is largely This effect is likewise observed in our second example

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Figure 4. (A) Semtonergic innervation of the rat forebrain. Noradrenergic innervation from LC is similarlywidespread. [Reproduced with permlapion from Hobson and Steriade 1986.1 (B) During wake, high levels of 5HT and NE function to ensure that neuronal responses reliably reflect &rent input and not spontaneous behavior. A sigmoid-sha prdwbiustic advation function can be used to model how predictably computer-simulated neurons will respon8" to afferent stimuli. "his advation function (see text) changes shape by varying the value of a. We hypothesize that a inversely reflects the level of aminergic modulation present in the forebrain, and is therefore lowest in wake and highest in REM. (C) The effect that varying levels of NE and 5HT might have on neuronal behavior is -ted by a computer simulation in which 41 neurons were given a supra-threshold (+lo mv) and subthreshold (-10 mv) input stimulus and tested to see if they fired, For a = 2 (wake-&; te., hi& predictability) all neurons above threshold fkred and only one of those below threshold tired resulting in a 97% (81/82) reliability. For a = 10 (REM-like; Le., low predictability) 10 supra-threshold neurons Wed to fire while 12 sub-threshold neurons fmd, resulting in 74% (70/82) reliability. We propose that this failure to exhibit the same fidelity of response as a increases is the neuronal equhlent of cognitive incongruities reported in dreams, and explains why such incongruities are more Erequent in REM dreams than in waking thought or htasies. (D)A dhgmmmic view of how such aminergic demodulation results in incongruities is suggested by considering a four-unit input pattern presented to a sim le connectionist network. For the input presented, let us assume that output pattern 2 (heavy arrow) is most bnrOreBt0 be produced if behavior of the neurons is entirely -tic (a = 0). because synaptic connection strengths favor that output for the given input. In REM, where a is high because aminergic modulation is absent, neuronal behavior would be less predictable on the basis of input alone. Therefore, if only one neuron in the output failed to respond correctly, pattern 1 could be produced instead of pattern 2. Note that pattern 1 is similar but not identical to the correct res nse. We view this increase in spontaneous neuronal discharge as Isomorphic with the increase in incongruity found'& dreams.

of incongruity, this time demonstrating incongruity in se- Another one was, eh . . . another one was, eh, quential thought wasn't a candle, it was a black light that you use for the psychedelic art which Emily had brought "I was looking at all the different candles that who was there . . . we had . . .eh to give off heat and light - the tent, everybody was asleep except for myself The dreamer is having an associative train of thought, and the candles were next to me and one was but those associations are more loosely coupled than is a .. .one of the candles was a memorial can- typical in wake or day dreams. The perception of be- dle . ..it was a little Jewish memorial candle. ing in a camping tent may serve as contextual input that

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Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1989.1.3.201 by guest on 30 September 2021 produces the response pattern for an image of candles, some reason or other and someone else is there because candles are commonly used while camping. But - I don’t know - I’m not sure if it’s my wife a Jewish memorial candle and a black light are contex- or not - seems that it is - but way down the tually associated in a very different way, and neither is road there’s a truck.. . typically associated with a camping tent. It seems that secondary network responses that subserve “ceremonial A discontinuity represents a rapid transition from one objects” rather than “camping supplies” have been spon- thought, action, image, or dream setting to a completely taneously activated, perhaps because candle light is a unrelated one. Our model of aminergic demodulation feature common to both these types of responses in this predicts more loosely associated neuronal responses and

dreamer’s brain. Again, our model of aminergic demod- a resulting increased amount of incongruity. The asso- Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/1/3/201/1755575/jocn.1989.1.3.201.pdf by guest on 18 May 2021 ulation in REM sleep can explain such incongruities as ciative quality of these incongruities is understandable a natural consequence of cortical activity during a be- because even in the complete absence of aminergic mod- havioral state in which neuronal responsiveness is less ulation, an ensemble of neurons will exhibit a finite reliably a function of afferent stimulus, and more prone amount of predictable behavior. Some predictability is to error because of the loosening of predictable neuronal assured simply because pre-synaptic activity that induces behaviors caused by aminergic withdrawal. membrane potentials far above or below threshold will One forebrain structure, the hippocampus, deserves be largely unaffected by aminergic demodulation. In ad- special mention at this point. In the absence of cata- dition, not every error in a network will directly translate cholamines (as in EM), spontaneous hippocampal neu- into an error at the output of the network. This is because ronal discharge is very high (Elazar and Hobson 1985) so each neuron typically receives input from a multitude of that the spatial and contextual information which is prob- sources, so that the effect of each synaptic contact may ably mapped in the hippocampus (O’Keefe and Nadel be small. These facts suggest that the output responses 1978; Eichenbaum and Cohen 1988) might be expected of most networks should retain at least some of the asso- to enter into dream mentation with a higher degree of ciational qualities of the information carried by the input unpredictability than with amine present. Indeed, spatial patterns. That discontinuities are so common in REM disorientation and contextual confusion are prominent sleep dreams suggests the activation of a specific physio- features of dream bizzareness (see Hobson and Schma- logical system which could produce this aspect of dream juk 1988 for a more detailed discussion of hippocampal bizarreness. We now consider the PGO system as the activity in REM sleep). possible neurobiological isomorph of this cognitive fea- The hippocampus is also of interest because synapses ture and show how bifurcation theory can be used to in the hippocampus demonstrate a form of synaptic plas- model this process. ticity referred to as long-term potentiation (LTP). Since synapses at which LTP is established are more synapti- Neurobioloey of PGO Waves and Acetylcholine cally effective than those without LTP (McNaughton 1982; PGO burst neurons are located in the lateral pontomes- McNaughton and Morris 19871, input from these neurons encephalic brain stem (Brooks and Bizzi 1963; Nelson et and circuits would be expected to contribute prominently al. 1983) and project to the thalamus and cortex (Brooks to the spatial and contextual aspects of dreams. This may 1967; Callaway et al. 1987). PGO waves, the phasic EEG explain why dreams often contain elements of events that potentials correlated with PGO neuron bursting (McCar- occurred during recent periods of wake (e.g., what Freud ley et al. 1978; McCarley and It0 19831, are most promi- called the “day residue” of dreams), especially if these nent in the posterolateral cortex, with decreasing activa- events were novel or emotionally charged experiences tion of more anterior regions of the cortex (Brooks 1968; (Hopkins and Johnston 1988; Svensson 1987). Sakai 1980). PGO-like waves have also been recorded in the hippocampus and amygdala (Calvo and Hernandez- PGO waves, Bifurcation Theory, and Dream Guardiola 1984). There is strong evidence that the PGO Discontinuity system conveys information about eye movement direc- While the absence of aminergic modulation offers a plau- tion from the brain stem to the forebrain (Monaco et al. sible neurophysiologic basis for the prevalence of in- 1984; Callaway et al. 1987). congruities in dreams, it has more difficulty explaining The postulated mechanism for PGO burst cell activa- discontinuities, the second and more specific aspect of tion is withdrawal of aminergic inhibition by decreased dream bizarreness. Consider the following example: LC and DRN discharge, with a reciprocal cholinergic excitation via REM-on cells. The PGO generator system . . .and, ah, my father made the comment as we is cholinoceptive (Lea,responsive to acetylcholine [AChl walked by that, ah, much of the, ah, money - agonists such as carbachol) (Vivaldi et al. 1980), and ev- the city is, ah, held by that man, and then there idence suggests that its principal neurotransmitter is ACh seems to be a lapse and then, ah, I seem to be as well (Hobson and Steriade 1986; Steriade and Llinis on another road, sort of standing in the road for 1988). Therefore, a basic understanding of the neurobiol-

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Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1989.1.3.201 by guest on 30 September 2021 ogy and actions of ACh is essential to an understanding A. of the role the PGO system may play in the dreaming process. Forebrain The presence of cholinoceptive neurons throughout Activity the cortex, hippocampus, and thalamus is well docu- I mented (Olivier et al. 1970; Bear and Singer 1986; Ste- riade et al. 1988; Pa& et al. 1988; Metharate et al. 1988a, 1988b; Mesulam et al. 1983). It appears that a principal PGO-induced EPSP action of ACh is to facilitate the firing of neurons receiv-

ing excitatory afferent input, but that ACh is not by itself A A A IOm”. Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/1/3/201/1755575/jocn.1989.1.3.201.pdf by guest on 18 May 2021 an excitatory neurotransmitter. This means that ACh will not typically generate action potentials in the absence of other stimuli (Hobson and Steriade 1986). For example, Metharate et al. (1988a, 1988b) demonstrated that ACh facilitates the selective firing of cat somatosensory cortex neurons in response to forearm skin tapping, but has no Effect Induced Subthreshold effect on spontaneous discharge rates (Figure 5C). Simi- lar results have been obtained in hippocampus (Ben-Ari et al. 1981) and visual cortex (Sillito and Kemp 1983). B. The basic mechanism of cholinergic facilitation (Km- jevic et al. 1971) is a long-lasting increase in membrane resistance via a reduction in potassium conductance. In . *-%/Set ofOutputs all Possible accord with this mechanism is the observation that ACh Input PGO-induced 5 applied to cells af the nucleus reticularis thalami (nRl9 Bifurcation Point induces hyperpolarization and bursting (McCormick and ).

Bifurcation Theory and PGO Waves Assuming that the PGO system is indeed cholinergic, then bursting PGO neurons supply the forebrain with a source of cholinergic facilitation that may also mimic an internal sensory stimulus during REM sleep when there is an absence of external stimuli to help orient the dreamer. How such cholinergic input or modulation could serve as a source for bizarre dream discontinuities can be understood by applying a model based on bifurcation theory to the properties of PGO neurons and cognitive processing. A rapid and discontinuous “jump” from one set of neuronal responses into a second set of responses that are independent from the original response pattern is called a bifurcation, and bifurcation theory is a branch of mathe- matics that explains how dynamical systems can produce these rapid transitions. Freeman and colleagues (Freeman and Skarda 1985; Skarda and Freeman 1987) observed that during inspiration, the entire rabbit olfactory bulb EEG oscillates at a patterns of the olfactory bulb to each scent that was fixed wavelength, but the amplitude and phase of the os- established during conditioning trials. Using a model of cillation varies from point to point in the bulb, depending the olfactory bulb‘s neural circuitry, Baircl (1985) then upon the particular scent presented to the rabbit. They argued that when a particular scent was presented to argued that this spatial variation in EEG amplitude and the rabbits, the observed rapid and almost discontinuous phase reflected the different learned neuronal response switch from a non-specific pattern of EEG amplitudes

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Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1989.1.3.201 by guest on 30 September 2021 into a specifically learned, and therefore predictable, duce an EPSP that always increases the membrane poten- response pattern could be mathematically detailed using tial, pi, of post-synaptic neurons by exactly Q millivolts the theory of multiple Hopf bifurcations. (mv) (i.e., variations in synaptic efficacy and quanta1 re- Of central importance to Bairds model is the functional lease of neurotransmitter are ignored). If a neuron is fir- role of chaotic neuronal activity. In his view, chaotic os- ing, the PGO input will have no influence on the state of cillation of the entire olfactory bulb during inspiration that neuron at that instant. But if the neuron is not firing, serves to “clear” the olfactory circuitry so that the pre- is not in its absolute refractory period, and its membrane sented scent stimulus can be processed using only those potential is less than Q millivolts below threshold, the contextual cues present at that moment, resulting in rapid PGO neurons’ release of ACh will depolarize the mem-

bifurcations to learned activation patterns. Chaotic activ- brane enough to cause firing. Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/1/3/201/1755575/jocn.1989.1.3.201.pdf by guest on 18 May 2021 ity increases the amount of energy in the bulb circuitry, Now let us re-consider our earlier example. Imagine thereby allowing the network to rapidly transition out that at some time in the dream the activity at the level of an existing but unassociated pattern of output into a of a visual cortex net is such that the image of a detec- learned response pattern. tive removing his jacket is synthesized. We will call this Accepting Bairds work as conceptually valid, it is rea- the presentation pattern. Superimposition of cholinergic sonable to hypothesize that brain stem-generated PGO PGO activity would result in the firing of all visual cortex activity may be able to exert a similar effect on the entire neurons less than Q mv below threshold, even though forebrain during dreaming. In REM, the highly activated their discharge may be unrelated to the information en- networks of the brain could bifurcate from one set of coded by the presentation pattern’s synaptic connection activation patterns into entirely new and unrelated ones strengths. The result could be the activation of a re- when phasically bombarded with a source of excitatory sponse (resultant pattern) entirely unrelated to the orig- facilitation, the PGO system. The cognitive equivalent inal input or image. The visual imagery could therefore of these discontinuous changes in activation would be discontinuously shift to a street scene. Schematically this discontinuous mental imagery. This would be reported is represented by the following situation: as a shift in scene, plot, action, or image. Consider our original example of a dream discontinuity: Presentation Pattern .. .lOOO.. ..1100. .. PGO Pattern ... 1111.... 1111 ... “. . .which I also throw behind a bush and for Resultant Pattern ...1011 ....1111 ... some reason he takes off his jacket, the detec- t tive does, and puts it down somewhere . . .and at this point the whole thing is switched to In this example, all neurons except one (arrow) fire somewhere else with different characters so I as a result of phasic PGO activity because either they think it’s the whole, you know, different thing, were already activated or were less than Q mv below um - something, to a street, or a street with threshold. The result, distributed over millions of neu- a lot of rubble piled on each side - the street rons, is a pattern of activity that is substantially different sort of - a desolated kind of street, and there and largely unassociated from the pattern prior to the was a car going down the street. . . ” PGO burst. Since the facilitatory effects of ACh appear to last for several seconds, while neural action potentials It is our contention that the sudden, rapid, and un- are only a few milliseconds in duration, a single cluster explained shift in the dream scene and plot represents of PGO waves could result in several seconds of uncon- the cognitive equivalent of a PGO-induced bifurcation at trolled cortical activity, and the activity in networks after the level of the thalamus and the visual and association the PGO effect has subsided could reflect a set of out- cortices. puts unrelated to those inputs present prior to the PGO To understand more clearly how this process might activity. Physiologically bifurcation has been produced. take place at the local circuit and neuronal level, we de- Cognitively, there is a discontinuity because of the sud- velop the following simplified model of the process. As den change in associative trains of thought that are the before, we represent the firing behavior of each neuron cognitive correlates of sequential activation of neural net- in a network as a set of binary values. Each neuron can works. This process is schematically outlined in diagram either be a 1 (firing) or 0 (silent), so that the activity pat- form in Figure 6. tern for an entire ensemble of neurons could be listed: Note that our postulated role for PGO activity in dream bizarreness is entirely consonant with the association ...111010111o0000111 ...... 001111m1 ... noted between PGO activity and the startle response seen during waking (Bowker and Morrison 1976). When an Phasic PGO neuron bursting can now be viewed as a animal is startled by an unexpected stimulus in the envi- template of facilitatory activity that is superimposed on ronment it rapidly shifts its attention toward that stimulus the activated forebrain circuits and networks during REM. source. This sudden attentional shift has much the same Let us assume that PGO neurons releasing ACh pro- quality of a REM dream discontinuity, and the fact that

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Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1989.1.3.201 by guest on 30 September 2021 to external stimuli (so that discontinuities are generated more frequently and spontaneously). We note that our model of PGO activity in REM sleep is somewhat analogous to simulated annealing algorithms used in connectionist models (Kirkpatrick et al. 1983; Hinton and Sejnowski 1986; Smolensky 1986). Simulated annealing algorithms use a probabilistic activation function which is dependent upon the “temperature” of the system to decide if a unit in the network should change

state. Learning and recall in these networks follows a Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/1/3/201/1755575/jocn.1989.1.3.201.pdf by guest on 18 May 2021 “cooling” schedule. At first the temperature is high; the system behaves more randomly but avoids committing to one particular memory or energy configuration. As the temperature is lowered (the annealing process), the network becomes more predictable and settles into a single equilibrium position. This annealing process prevents nets from “getting stuck” in incorrect memory configu- rations early on in a learning or recall task. Because the activation functions used in simulated annealing al-

Out8ide gorithms and our model of aminergic demodulation are * nearly identical, one might consider aminergic demodulation more analogous to simulated annealing. However, it is actually the KOsystem which bears the greater re- semblance, at least with respect to REM sleep. This is because while aminergic demodulation in REM sleep is RECOVERY tonic (and therefore persists throughout the dream), PGO + activity is phasic. The discontinuous bursts of cholin- STIMULUS m ergic facilitation throughout REM sleep are thus analogous to increases in temperature in simulated annealing, while the quiescent periods between clusters of PGO Figure 6. PGO activity as a source of dream dis- waves would correspond to cooling phases. It should continuity. (A) In this shpU5ed schematic, PGO be stressed that this comparison between the PGO sys- fadlltatory input is viewed as a source of phasic EPSRP super-imposed upon forebrain neuronal activity. tem and simulated annealing is strictly metaphorical. Whenappliedto already active neurons (farlefttradne), or neurons far below threshold (farrlght tracins), PGO input has no influence. However, in neurons that are only slightly subthreshold cholinergic facilitation by PGO in- Dream Bizarreness and the Nafiatfve Thematic put may induce in a neuron that would not 0th- C0nstancyof Dreams U”hM!h(dddkrradns). (B)The~ktiOflS~pbetWeen How can our model of error-filled neuronal activity con- PGO WaVe-indUCed- bifurcptions and dream dfscontinuity isdialp-ammaticallyoutlinedbyconsideringthedevelop tend with the fact that most dreams do maintain a narra- ment of a dream as a series of sequential input-output re- tive thematic constancy filled with wake-like images and sponses by the brain’s neuronal networks. For a @ve!nin- happenings? If our model is correct, one might expect put, a set of outputs rangins fromimprobable to likelyex- ists, and the eventsthat occur in adream reflect the actual completely disordered mentation with little if any the- out uts that are generated (dark arrows). PGO input may matic development and kaleidoscopic imagery. While dtatethe spontaneous of enough neurons the solution to this paradox remains speculative, some such that the resultant pattern of activity present when this fadutatfonstopsis entirelyunrelatedtotherange of suggestions may provide insight into this apparent in- possible or expeckd ou uts or to the PGO input. consistency. nitively,thissuddensar or ifwcatloninactivityco 3 In the model systems we present, all units are identical represent a dream dtscontinuty such as a scene shift. and symmetric interactions between units take place at every level. The brain, on the other hand, shows tremen- dous heterogeneity in both morphology and connectivity PGO waves are tightly associated with both events further (Shepherd 1979; Brodal 1981). Such heterogeneity di- strengthens our physiological model of the PGO system rectly influences discharge properties. Thus it would not as a contributor to dream bizarreness. The major differ- be surprising to find that aminergic demodulation and/or ence is that during waking, the PGO waves are elicited phasic PGO stimulation differentially affect the behavior by external stimuli and the waves rapidly habituate (sug- of cortical neurons, thereby influencing the amount of gesting a specific event-related role), while in REM sleep bizarreness seen at a cognitive level. Indeed, it would be PGO bursting is both disinhibited and entirely unrelated surprising if this were not the case. Despite the fact that

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Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1989.1.3.201 by guest on 30 September 2021 LC and DRN project widely and diffusely to cortex and A facilitatory effect resulting in patterns of activity un- subcortical structures with little evidence of a highly or- related to pre-PGO activity would be predicted by our ganized or laminar pattern of innervation, the influence hypothesis. of NE and 5HT may be variable across neuronal types and subtypes such that decreased aminergic neuromod- Connectionist ModeLs and Computer Simulations: ulation may have little influence on dream coherence un- There are numerous dficulties in testing the neurophys- less certain critical neurons are affected by this demod- iological basis of a subjective human mental experience ulation. For example, changes in ensembles pf cortical like dreaming. Both ethical and practical considerations pyramidal cells may be a more important contributor to preclude many types of experiments in humans. Given

bizarre dream imagery than similar alterations in cortical these restrictions, perhaps the easiest way to test the hy- Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/1/3/201/1755575/jocn.1989.1.3.201.pdf by guest on 18 May 2021 granule cells. An alternative way of viewing this is that potheses of the model is to study the effects of behavioral while all neurons may be near-equally demodulated by state changes on realistic computer simulations of neural the loss of amine in REM, the effect on overall cogni- and/or cognitive processes (Traub et al. 1987a, 1987b; tive processing may be negligible unless certain critical Clarke et al. 1985; MacGregor 1987). The more accu- neurons involved in information processing and image rately the model neurons resemble biological neurons, generation are specifically affected by such demodula- the more accurately cholinergic and aminergic modulation at a given instant of a dream. An entirely analogous tory influences can be modeled. argument can be made for the role of the PGO system in Computer-simulated neural networks with realistic discontinuity production. properties could be “trained“ to learn a series of out- In support of this view is the observation that, in pa- put patterns in response to a set of inputs. The networks tients with Alzheimer’s dementia, neuronal loss is selec- could then be linked together in such a way that the tive for large neocortical cells such as those found in output patterns from one net would serve as the input layer 111. Despite the fact that approximately 90% of all patterns to a second and third net (as well as feeding cortical neurons are spared in Alzheimer patients (Katz- back upon itself). This linking of outputs and inputs is a man 19861, memory loss and disorientation can be pro- very simple way to model the sequencing of patterns in a found. Similar effects have been reported in computer “train of thought” and has been suggested by many mod- simulations of artificial neural networks with hierarchical elers (Hopfield 1984; Kanerva 1984; Keeler 1987; Clarke memory storage capabilities (Sutton et al. 1987). Con- et al. 1985). In an aminergically modulated (wake-like) sidering the implication of catacholaminergicand cholin- regime, the response patterns of the networks should ex- ergic mechanisms in dream bizarreness and the selec- hibit a high degree of reliability and predictability, but in tive loss of neurons containing these neurotransmitters the demodulated (REM-like) regime, outputs should be- in Alzheimer’s dementia (Henderson and Finch 19891, it come less predictable but still remain loosely associated might be worthwhile to focus attention on layer III corti- with the responses typically produced in wake, support- cal cells in attempting to validate some of the hypotheses ing the modulatory role attributed to aminergic systems presented here with neurophysiological tests. in our model. More recent attempts to model the effects of noise on neural networks have yielded results consis- Testing the Model tent with this hypothesis, and should encourage further Neurophysiology Neurophysiological and pharma- investigation (Keeler et al. 1989). cological studies of higher brain function - which sub- PGO activity could be simulated by phasically alter- stantiate the physical assumptions of this theory - con- ing the membrane response characteristics of the neu- stitute one of the strongest tests of its validity. One logi- rons such that excitatory responses are facilitated. This cal but technically sophisticated study in this vein would should cause bifurcations to outputs which are unrelated be to show that a specific afferent input to a well-defined to pre-existing afferent input. By varying the properties cortical area produces an equally well-defined and repro- of the simulation neurons, and connecting these units in ducible output response in the presence of NE or 5HT, networks consistent with neuroanatomical data, different but a less predictable one in its absence. Since Free- types of neurons and networks that exist in the forebrain man has demonstrated reproducible spatial patterns of could be modeled, leading to a better understanding of EEG amplitude across the rabbit olfactory bulb after clas- the roles each neuronal type and circuit may play in pro- sical conditioning experiments, this system seems well ducing bizarre imagery in dreams. suited for such a test. The complex receptive fields of the visual cortex (Szentagothai 1973; Szentagothai 1978) Dream Bizarreness and the Functional Significance are likewise attractive targets for such hypothesis testing of REM sleep and some preliminary work by Singer (1987) is highly As is so often the case in science, answering the ques- suggestive of the type of result to be expected. The ef- tion of how something might work is often easier than fects of PGO input could be assessed by either electrically answering the question of why it works that way. While stimulating the PGO burst cell zone or by iontophoreti- we feel our model offers a plausible neurophysiological cally applying ACh to the olfactory bulb or visual cortex. basis for the bizarre imagery common to all dreams, it

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Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1989.1.3.201 by guest on 30 September 2021 says nothing about the functional significance this sort of night to night? Perhaps most importantly, there is no psy- process has for the brain - either biologically or psychological, physiological, or developmental evidence to chologically. In particular, it does not attempt to explain support this notion. the sort of learning or information processing functions A third and most intriguing view is that the purpose of that dream bizarreness or REM sleep may serve. Sad to RFM sleep is a developmental one, in which the activa- say, at present not enough is known about the neuro- tion of neural circuits in REM serves to strengthen, rather physiology of either REM sleep or cognitive function to than weaken, synaptic contacts (Roffwarg et al. 1966). address this issue in a scientifically adequate manner. We For example, the fetus developing in the womb receives review here some more recent and computationally ori- all of its oxygen from its mother, yet at the instant of

ented theories regarding the function of REM sleep in the its birth it must begin to breath with incredible regular- Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/1/3/201/1755575/jocn.1989.1.3.201.pdf by guest on 18 May 2021 hope that it may suggest to others some links between ity if it is to continue to receive oxygen. Somehow the dream bizarreness and REM sleep that are not presently neural circuits which control the muscles of breathing apparent to us. must be prepared for this event, and it has been pos- Numerous investigators (Crick and Mitchison 1983; tulated that the role of REM sleep is to automatically Hinton and Sejnowski 1986; Clarke et al. 1985; Davis and stereotypically excite these brain circuits such that 1985) have suggested that REM sleep, and consequently synaptic strengthening occurs before these connections dream bizarreness, is needed for efficient cortical func- are needed. Failure of these circuits to develop may ex- tioning. Crick and Mitchison argue that if computational plain such phenomena as the sudden infant death syn- neural networks become overloaded with memory pat- drome (SIDS) (Watabe et al. 1983). In support of this terns, they either fail to produce any correct responses view is the observation that a fetus will spend 70430% of or recall only one memory regardless of the input. Pe- total sleep time in REM and the newborn will spend 50% riodically retraining these networks with random inputs of total sleep time in REM (Roffwarg et al. 1966; Anders serves to dampen synaptic connection strengths, result- 1976). Adults spend approximately 20% of total sleep ing in a reverse learning process that allows the net to time in REM, despite the fact that the total amount of perform better on subsequent training trials. Hopfield NREM sleep remains nearly constant throughout life. et al. (1983) demonstrated this result in a connectionist At the theoretical level, Linsker (1987) has demon- network model. Crick and Mitchison postulate that REM strated that networks which use a Hebbian learning al- sleep serves an analogous reverse learning function for gorithm to modify synaptic weights and are connected in the cerebral cortex. They further predict that, in the ab- a “center-surround configuration similar to the cells of sence of REM sleep, mammals deprived of this reverse the visual system, will, when activated by random input learning should develop pathological and/or obsessive patterns, adjust synaptic weights such that orientation- behaviors. At present there is little physiological data to selective output units spontaneously emerge. This model suggest that this sort of process is ongoing in sleep. Peo- demonstrates that random input to a network with a simple deprived of REM sleep for long periods of time do ple pattern of connectivity can lead to the emergence of not appear to develop significant cognitive deficits (Al- higher-order information processing, and thus seems to bert 1975; Vogel 1975; Webb and Cartwright 1978) and support an ontogenetic argument for REM sleep. rats deprived of REM sleep likewise do not behave abnor- While no single theory has gained clear-cut accep- mally although they do lose the ability to thermoregulate tance, the notion that dream bizarreness is the cognitive and control metabolism (Kushida et al. 1989). result of neural activity required for the efficient function- Hinton and Sejnowski (1986) postulate that in a Boltz- ing of the brain’s neural networks does seem to be gain- mann Machine network, the “phase negative (-1’’ com- ing wider acceptance. At the very least, our model of- ponent of learning, in which a network is allowed to fers a plausible neurophysiological explanation of dream run freely with no external input, could be possibly iso- bizarreness, and consequently a way to test these “net- morphic with REM sleep. They suggest that the random work hypotheses about REM sleep. co-activation of pre- and post-synaptic units during this phase can be used to calculate an average measure of Summary and Conclusions the degree of synaptic plasticity in a network. This average value then establishes a baseline from which synaptic In an effort to further specify the ways in which REM weight changes are to be “subtracted during wake, when sleep neuronal dynamics could be related to distinctive environmental cues serve as the principal inputs to the dream cognition, we have considered how two robust networks (“phase positive (+I”). This process serves to neurophysiological processes could contribute to dream stabilize behavior by helping units deep inside the net- discontinuity and incongruity. We first propose that the work decipher the influences of other units from influ- withdrawal of aminergic neuromodulation seen in REM ences due to environmental input. There are many obvi- sleep results in a shifi in neural dynamics. This shift, ous difficulties with this view. How is this average value which can be described mathematically, makes neural measured? Where and how is it stored? Why should networks of the forebrain more prone toward unpre- this baseline be different from person to person or from dictable response patterns, which are reflected cogni-

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Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1989.1.3.201 by guest on 30 September 2021 tively by loose associations and incongruity. We next Antrobus, J. (1983a). REM and NREM pairs collected on first propose that PGO activity serves as a source of ACh to lab nights in which reports were elicited from native English the forebrain which facilitates bifurcations in network re- speakers. Department of Psychology, C.C.N.Y., New York, NY. sponse patterns; these could be experienced cognitively Antrobus, J. (1983b). REM and NREM sleep reports: Compari- as dream discontinuities. Our model thus offers a more son of word frequenciesby cognitive classes. Psychophysiology, formal and precise description of the physiological sys- 20(2), 562i568. tems which underlie bizarreness in dreams. Future ef- forts must proceed on two fronts: (1) detailing the dy- Aserinsky, E. & Kleitman, N. (1953). Regularly occuring periods of eye motility and concurrent phenomena during sleep. namics of such neuronal interactions in physiologically Science, 118, 273274. and anatomically realistic networks and (2) demonstrat- Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/1/3/201/1755575/jocn.1989.1.3.201.pdf by guest on 18 May 2021 ing results consistent with our hypotheses in network and Aston-Jones, G. & Bloom, F.E. (1981). Activity of norepine- animal models which are altered by simulating aminergic phrinetontaining locus coeruleus neurons in rats anticipates demodulation and input. fluctuations in the sleepwaking cycle. Journal of NeuIoscience, PGO I, 876-886.

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