The Neuropsychology of Sleep and Dreaming

John S. Antrobus, Mario Bertini

• Publisher: Psychology Press
• Year: 2013
• ISBN:
  9781134764334
• Edition: 1
• Topic: Psychology
• Subtopic: History & Theory in Psychology
• Index: Psychology

This volume describes how the conceptual and technical sophistication of contemporary cognitive and neuroscientific fields has enhanced the neurocognitive understanding of dreaming sleep. Because it is the only naturally-occurring state in which the active brain produces elaborate cognitive processes in the absence of sensory input, the study of dreaming offers a unique cognitive and neurophysiological view of the production of higher cognitive processes. The theory and research included is driven by the search for the most direct relationships linking the neurophysiological characteristics of sleepers to their concurrent cognitive experiences. The search is organized around three sets of theoretical models and the three classes of neurocognitive relationships upon which they are based. The contributions to this volume demonstrate that the field has begun to move in new directions opened up by the rapid advances in contemporary cognitive science, neuropsychology, and neurophysiology.

1

Introduction

John Antrobus

City College of the City University of New York

Mario Bertini

University of Rome, La Sapienza

The theories, reviews, and research findings presented in this volume, together with their supporting evidence, describe our current views of how the rhythmic oscillations in the activation of the sleeping brain are associated with shifts in information processing, and with how the cortex creates the fascinating imagery and thought during sleep that popularly goes by the name dreaming. This chapter introduces the reader to the basic research issues and themes that drive sleep neuropsychologists to monitor sophisticated electronic apparatus and study sleeping subjects in grueling, 12-hour, all-night shifts. The passion that sustains this effort derives from the baffling mystery of the dream experience, from the dramatic changes in neurophysiological states during sleep, and from the high degree of covariation between the two. In no other area of neuropsychology has the search for the links between body and mind been so intense and so sustained. The chapters that follow describe our successes (and some failures) in locating these links. For the reader who is unfamiliar with the technical procedures of EEG and REM recording and the elicitation of imagery and thought reports, the opening pages of Armitage, Hoffman, and Moffitt (Chap. 2) will provide an excellent introduction.

The explanatory value of a theory or model is constrained by how well its concepts or terms can be translated into empirically defined operations. This constraint is particularly apparent in the neuropsychological study of dreaming where characteristics of the dream can only be inferred from the often inarticulate verbal report of a disoriented individual who has just been awakened from sleep. Unlike the report of a visual perception, whose accuracy can be checked against the public visual stimulus, there is no way to check the accuracy of the “public” dream report against the sleeper’s private dream experience. For this reason, the discovery of a close relation between the dream report and the cortical EEG by Aserinsky and Kleitman (1953) was welcomed as a potentially more reliable way to determine when dreaming was taking place. In 1962, Roffwarg, Dement, Muzio, and Fisher also claimed that measures of eye movement direction under the lids indicated the direction of the dreamer’s visual gaze. The strong form of this assertion was not supported by subsequent experiments, but a more modest relationship does appear to exist (see Chapter 14). But despite the technical sophistication of accuracy of the physiological instrumentation used in sleep and dreaming research, it has provided us with little additional indication about the characteristics of the dream experience.

The ability of neurophysiological measures to identify the cognitive characteristics of dreaming cannot be better than the cognitive criteria employed to validate those measures. The description of the relations between the characteristics of the sleeping brain and the cognitive characteristics of the dream are ultimately constrained by the quality of the measurements of the characteristics of the imagery and thought that make up the dream experience.

The Measurement of Imagery and Thought Produced During Sleep

Although there is general agreement that the term dreaming is defined by a cluster of variables such as bizarreness, hallucinatory quality, vivid visual imagery and a story-like quality, it is entirely possible that different neurophysiological processes may be associated with each of these quite different properties. If so, the magnitude of these qualities may vary somewhat independently across different conditions within sleep. But if dreaming is defined as some composite of these qualities, the linkages between cognitive (image and thought) and neurophysiological concepts will be visible only when all of the qualities covary. For example, if bizarreness is high and hallucinatory quality low in condition A, and the reverse on condition B, the value of the dream variable will be the same in both conditions, and the possible relation of A to bizarreness and B to hallucinatory quality will be obscured. Moreover, the visual qualities of spatial relationships, clarity of form, surface texture, and color may be controlled by different neurophysiological sites. Again the relations will be obscured if visual images are scaled on a single variable, such as vividness.

Support for this multivariate conception of sleep mentation from the finding that reports from Stage 1 Rapid Eye Movement (REM) sleep can be distinguished from those of Stage 2 (NREM) sleep 92.5% of the time by their greater length (Total Recall [word] Count: TRC; Antrobus, 1983). On the other hand, the length of the report is no help in discriminating Stage 1 REM from waking reports, where the latter are obtained from subjects lying in bed in a dark room, that is, under identical laboratory conditions. But if the mentation reports are divided into thematic units, the units are significantly longer in Stage 1 REM sleep than they are in awakening. Put another way, there are more, and shorter, thematic units per report in waking, especially in a noisy environment, than there are during REM sleep, despite their similar report length.

In the domain of visual imagery, Antrobus (1983) separated the imagery variable into four word-count variables: visual nouns, verbs, modifiers (adjectives and adverbs), and spatial prepositions. But all four behaved similarly in discriminating REM from NREM reports and so were combined to create a Visual Imagery Count for all further analyses. As with the dreaming variable, when the REM–NREM difference was statistically corrected for differences in TRC, there was no significant residual REM–NREM difference in Visual Imagery Count.

Investigators have long been concerned about the error that is inevitably incurred when the dreamer translates the predominately visual dream into a verbal description or report. In response to the problem, Rechtschaffen and Buchignani (chapter 7) have created several visual scales based on variations on a single photograph. The technique yields measures of independent visual dimensions such as hue saturation, clarity or focus, and brightness. Rechtschaffen et al. show that one set of visual variables may discriminate REM from NREM reports, whereas a second set may discriminate Phasic from Tonic REM reports. The relation between visual imagery scales that are based on the traditional verbal report and those based on a modification of this photograph technique (Antrobus, Hartwig, Rosa, & Reinsel, 1987) is currently being studied in our lab. At this point, the new visual imagery scales developed by Rechtschaffen et al. show considerable promise for identifying semi-independent visual-neurophysiological relationships.

At least three distinct bizarreness classifications have been identified thus far. In the chapter by Reinsel, Antrobus, and Wollman, the authors found that a variable that is the conceptual converse of Topic length, and is commonly considered to be a component of bizarreness, namely temporal Discontinuities, is at least as common in waking as in REM reports. This Waking-REM Sleep similarity was also true for Improbable Combinations of visual attributes, a second subclass of Bizarreness. Only Improbable Identities, the least frequent class of Bizarreness, were more typical of REM than Waking reports. All three classes were more typical of REM than NREM reports, but again, statistical correction for TRC eliminates the REM-NREM distinction in Bizarreness, defined as the sum of the three measures.

In summary, the effort to identify relations between the neurophysiological and cognitive variables within sleep is greatly enhanced when the global variable dreaming is separated into components that have potentially different neurophysiological origins. As new and more sharply defined relationships are uncovered it becomes possible to build more precise neurocognitive theories and models of sleep imagery and thought.

Models of Sleep Imagery and Thought

The theory and research described in this volume is driven by the search for the most direct relationships that link the neurophysiological characteristics of the sleeper to his or her concurrent cognitive experience. The neuropsychology, or more precisely the neurocognition, of dreaming sleep is therefore an example par excellence of a body-mind problem. The search is organized primarily around three sets of theoretical models and the three classes of neurocognitive relationships upon which they are based. For the purposes of this introduction, the three sets of models are (1) the cerebral hemisphere asymmetry models first suggested by Ornstein (1972); (2) the Activation-Synthesis model introduced by Hobson and McCarley in 1977, and Hobson’s new Activation level, Input source, and Mode of processing (AIM) model (Chap. 12), and (3) Antrobus’ DREAMIT model (Antrobus, 1991; Antrobus, Chapter 10). The empirical domains of inquiry that overlap, but do not coincide, with the models are, Tonic Distributed Activation, Hemisphere Asymmetry, and Phasic Activation.

Tonic Distributed Activation

The tonic activation relationships to dreaming was first introduced by Zimmerman in 1970. He proposed a direct link between cortical arousal and dreaming. His concept of cortical arousal is a mixture of sensory thresholds, motor activity within sleep, and other spontaneous psychophysiological activity during sleep. Most of his measures of cortical arousal, however, are associated more with disturbed than with normal sleep and are not part of the cluster of neurophysiological variables that are now considered typical of the contrast REM and NREM sleep. As evidence for the subcortical control of cortical activity during sleep became clearer, Hobson and McCarley (1977) introduced a neurophysiological Activation-Synthesis model of dreaming sleep in which general cortical activation was associated with general cognitive activation which, in turn, led to the production of dreaming in Stage 1 REM sleep. The cognitive activation side of this model has subsequently been elaborated by Antrobus (1990; in press).

Hobson and McCarley (1977), Hobson, Lydic, and Baghdoyan (1986), McCarley and Massaquoi (1986) and Hobson and Steriade (1986) describe a sleep control model in which pontine centers oscillate back and forth to produce the REM and NREM sleep. The medial reticular formation controls a set of cholinergic/cholinoceptive neurotransmitter pathways that activate the association and motor cortex during REM sleep. This activation is characterized by a tonic desychronization of the cortical EEG, a defining criterion of REM sleep, so that the REM EEG is quite similar to that of the waking state. This similarity has persuaded a broad consensus of opinion that the cerebral cortex is similarly activated in REM sleep and waking.

Additional support for this position is provided by two measures that respond to changes in cerebral metabolism. Townsend, Prinz, & Obrist (1973), Sakai, Meyer, Derman, Karacan, and Yamamoto (1979), and Meyer, Ishikawa, Hata, and Karacan (1987) found that cerebral blood flow during REM sleep was higher than during NREM sleep, and equal or higher than during waking. Franck et al. (1987) reached similar conclusions using positron emission tomography (PET).

The concept of cortical activation is derived in part from the concept of cognitive activation, and both concepts rest on the testable assumption that performance on a broad class of perceptual-> cognitive-> motor tasks is associated with a widespread shift in cortical state. There is, however, no simple relationship between any measure of cortical neuronal activity and information processing within the cerebral cortex. The neural activity that is identified by the cortical EEG is produced by the outermost layer of cortical cells, which do not themselves participate directly in information processing (Hobson & Steriade, 1986). Nor does an increase in cerebral metabolism, or total neural metabolic rate, necessarily identify a state of increased cognitive activity. Information processing involves a rapid sequence of delicately patterned activity within large networks of neurons. Increased neural metabolism may indicate an increased rate of processing the information represented in the networks, but it is quite possible that metabolic rates either higher or lower than those of the alert waking brain are incompatible with information processing. The assumption that increased cerebral blood flow indexes increased neural metabolism and thus increased cognitive activity is also vulnerable because blood flow is only indirectly related to neural oxygen consumption. Thus, the high rate of cerebral blood flow in REM may be attributed to a relaxation of arterial wall tonus that is quite unrelated to neural metabolic requirements.

The assumption of a cortical to cognitive activation function, therefore, requires empirical support that links the body-mind domains. Conventional measures of information processing are out of reach during sleep because of the high sensory thresholds of the sleeper. This inaccessibility is acute during REM sleep because of the powerful suppression of motor efferent control. The cortex may be active, but it receives relatively little information from the outside world and is incapable of making a motor response without moving marginally out of the REM sleep state. Cognitive measures must, therefore, be obtained in the postsleep state. Bertini, Violani, Zoccolotti, Antonelli, and DiStephano (1984), Bertini and Violani (Chapter 3), and Lavie and Tzischinsky (1984) have reported considerable success with sensory-motor performance tests designed to evaluate hemisphere asymmetry in prior sleep states, although Lavie (personal communication, 1988) has recommended caution in extrapolating from waking performance to prior sleep states.

Even the assumption that mentation reports obtained following awakening from sleep describe imagery and thought that occurred during the prior sleep interval has been questioned from time to time. In 1896, Goblot (Hall & Raskin, 1980) proposed that the production of the dream report begins at the moment the sleeper begins to awaken and ends after the report is completed. The hypothesis was discredited when Dement and Wolpert (1958) found that the time between the presentation of an external stimulus, such as a spray of water, and the time of being awakened from sleep matched the duration of the dream report, which in turn, equaled the time required to act out the narrative. But in an unpublished, privately circulated, critical review of the evidence for and against the Goblot hypothesis, Hall and Raskin (1980) pointed out that the duration of the stimulus interval in the Dement and Wolpert experiment was a constant 30 s in all cases. Evidence against the Goblot hypothesis would require a design where the stimulus-to-awakening interval was varied over some range and that the time to act out the narrative covaried with the duration of the stimulus-to-awakening interval. They argued that the Dement and Wolpert findings were equally compatible with the Goblot hypothesis. To date, no one has carried out such a study.

Closely related to the Goblot hypothesis is the question of whether the greater amount of information in the REM relative to NREM report is a cognitive production or an attention-memory-retrieval effect. Rosenblatt, Antrobus, and Zimler (Chapter 11) showed that the increased cognitive activation of REM sleep carries over to the postawakening mentation report period. Their subjects were presented with six brief audiovisual cartoon sequences just prior to going to bed. Upon subsequently being awakened from REM and NREM sleep and given a brief audiovisual cue, they were able to recall significantly more information following REM than NREM awakenings. Therefore the cortical activation of subjects is greater upon awakening from REM than NREM sleep. But the effect was small relative to that of the extremely large REM-NREM mentation report effect. Therefore, only a rather small part of the REM-NREM mentation report difference may be attributed to an improved ability of the subject to retrieve and translate into words the sleep mentation of REM sleep. The major part the REM-NREM mentation difference must be attributed to the subject’s ability, while asleep, to generate actually more thought and imagery in the REM interval. In this sense, the ...

Table of contents

• Cover Page
• Half Title page
• Title Page
• Copyright Page
• Dedication
• Contents
• Preface
• 1. Introduction
• I. Dreaming and Cortical Hemisphere Asymmetry: Pro and Con
• II. Visual Imagery and Cognitive Processes across Waking and Sleep States
• III. Tonic and Phasic Activation Models
• IV. Lucid Dreaming
• Author Index
• Subject Index