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

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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- Mamelak and Hobson 201 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 fea- tures 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- 202 Journal of Cognitive Neuroscience Volume 1, Number 3 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 des- olated 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 ani- mals (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.
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