The popular view that behavioral quiescence is the predominant sign of sleep may be valid for the full-blown state of resting sleep, but not for the preparatory period during which many animal species display complex motor behaviors directed at finding a home for sleep. However, this aspect of behavioral immobility alone cannot differentiate sleep from wakefulness since humans and other mammals are motionless at increasing levels of vigilance, especially during expectancy and hunting conditions associated with characteristic bioelectrical rhythms. The defining signs of the period when one falls asleep are peculiar changes in brain electrical activity (electroencephalogram, EEG) produced by network operations in the thalamus and cerebral cortex. These changes are the cause, rather than the reflection, of a quiescent behavioral condition. Indeed, the brain oscillations that define the transition from wakefulness to sleep are associated with long periods of inhibition in thalamocortical cells, with the consequence that the incoming messages are blocked and the cerebral cortex is deprived of information from the outside world. Following the appearance of these initial signs, other oscillatory types mark the late stage of resting sleep and they further deepen the unresponsiveness of thalamic and cortical neurons, disconnecting the brain from the external world.

In this chapter, I discuss the neuronal properties and network mechanisms underlying the behavioral and bioelectrical signs of waking and two major sleep stages: sleep with high-amplitude, synchronized slow waves (SWS), and sleep with rapid eye movements (REM sleep).

The understanding of neuronal mechanisms underlying different states of sleep and epilepsy requires a detailed exposé of various neuronal types and networks in the major brain structures that generate these behavioral conditions, that is, neocortex, archicortex and related systems (rhinal cortices and amygdala), thalamus, and generalized systems that modulate the excitability of forebrain structures. Despite the innumerable neurons located in these structures and their diverse temporal patterns of repetitive firing, unifying principles can group individual neurons into a limited number of classes. This chapter deals with neuronal types and with local and distant connections among neurons, placing emphasis on peculiar neuronal features that may play a role in certain aspects of sleep and seizures.

One of the conclusions resulting from data presented in this chapter is that synaptic activities within complex neuronal networks modulate, and often overwhelm, intrinsic neuronal properties. In the absence of rich synaptic activity, as is the case in brain slices and isolated cortical slabs in vivo, neuronal properties mainly result from a host of voltage-dependent and transmitter-gated conductances. Analyses of the same neuronal types in the intact brain, under anesthesia and especially in naturally alert preparations, demonstrate that intrinsic neuronal properties display dramatic alterations with changes in membrane potential and increased synaptic activity during behavioral states.

The intrinsic properties of cortical and thalamic neurons were first revealed in brain slices.

This monograph is a synthesis of the ongoing efforts toward the understanding of neuronal mechanisms underlying sleep stages and different forms of paroxysmal (epileptiform) activities that preferentially occur during the states of drowsiness and slow-wave sleep. I have been interested in the neurophysiological basis of electrographic seizures since the 1960s, and this interest intensified during the early 1970s when I investigated spike-wave seizures during light sleep in behaving monkeys. This work inspired my idea that such seizures originate within the neocortex and set the scene for our recent intracellular work in vivo, throughout the 1990s. The journey continues this century, along the same conceptual lines, with new collaborators who have joined my team.

The two major topics of my laboratory are the neocortical and thalamic neuronal bases of sleep and of paroxysmal activities that mimic different forms of epilepsy in humans, more particularly absence seizures and Lennox–Gastaut syndrome. This is why sleep and these two forms of paroxysmal activities found a place of choice in the present monograph. Nonetheless, I have also attempted to relate these topics with a series of other forms of epilepsy. There are some edited volumes in which many authors express their views, sometimes discrepant, on sleep and/or epilepsy, but I decided to write a monograph because this may allow an expression of coherence, even if the views in this book might be, of necessity, biased by my ideas and personal experimental data.

Abstract: Sleep researchers in different disciplines disagree about how fully dreaming can be explained in terms of brain physiology. Debate has focused on whether REM sleep dreaming is qualitatively different from nonREM (NREM) sleep and waking. A review of psychophysiological studies shows clear quantitative differences between REM and NREM mentation and between REM and waking mentation. Recent neuroimaging and neurophysiological studies also differentiate REM, NREM, and waking in features with phenomenological implications. Both evidence and theory suggest that there are isomorphisms between the phenomenology and the physiology of dreams. We present a three-dimensional model with specific examples from normally and abnormally changing conscious states.

Keywords: consciousness, dreaming, neuroimaging, neuromodulation, NREM, phenomenology, qualia, REM, sleep

Introduction

Dreaming is a universal human experience that offers a unique view of consciousness and cognition. It has been studied from the vantage points of philosophy (e.g., Flanagan 1997), psychiatry (e.g., Freud 1900), psychology (e.g., Foulkes 1985), artificial intelligence (e.g., Crick 1994), neural network modeling (Antrobus 1991; 1993b; Fookson & Antrobus 1992), psychophysiology (e.g., Dement & Kleitman 1957b), neurobiology (e.g., Jouvet 1962) and even clinical medicine (e.g., Mahowald & Schenck 1999; Mahowald et al. 1998; Schenck et al. 1993). Because of its broad reach, dream research offers the possibility of bridging the gaps in these fields.

We strongly believe that advances in all these domains make this a propitious time to review and further develop these bridges. It is our goal in this target article to do so.

Abstract: The paradigmatic assumption that REM sleep is the physiological equivalent of dreaming is in need of fundamental revision. A mounting body of evidence suggests that dreaming and REM sleep are dissociable states, and that dreaming is controlled by forebrain mechanisms. Recent neuropsychological, radiological, and pharmacological findings suggest that the cholinergic brain stem mechanisms that control the REM state can only generate the psychological phenomena of dreaming through the mediation of a second, probably dopaminergic, forebrain mechanism. The latter mechanism (and thus dreaming itself) can also be activated by a variety of nonREM triggers. Dreaming can be manipulated by dopamine agonists and antagonists with no concomitant change in REM frequency, duration, and density. Dreaming can also be induced by focal forebrain stimulation and by complex partial (forebrain) seizures during nonREM sleep, when the involvement of brainstem REM mechanisms is precluded. Likewise, dreaming is obliterated by focal lesions along a specific (probably dopaminergic) forebrain pathway, and these lesions do not have any appreciable effects on REM frequency, duration, and density. These findings suggest that the forebrain mechanism in question is the final common path to dreaming and that the brainstem oscillator that controls the REM state is just one of the many arousal triggers that can activate this forebrain mechanism. The “REM-on” mechanism (like its various NREM equivalents) therefore stands outside the dream process itself, which is mediated by an independent, forebrain “dream-on” mechanism.

Overview

It is important that persons seeking to theorize on the neural bases of dreaming be grounded in the most current findings on the neurobiology of sleep from the level of its molecular and cellular neurophysiology through the macroscopic regional activity patterns that more directly inform the study of its neuropsychology and phenomenology. In this volume, Hobson et al. have provided a primer on these neurobiological topics with a focus on the REM-NREM cycle and, in less detail, on the sleep-wake cycle. Hobson et al. (sections 3.1 & 3.2) review literature postdating the extensive reviews provided by Hobson and Steriade (1986) and Steriade and McCarley (1990) and approximately predating the year 2000. Far more extensive reviews focusing on specific neurochemical systems and anatomical networks can be found in the contributions to two recent books edited by Lydic and Baghdoyan (1999) and Mallick and Inoue (1999) as well as in the third edition of Kryger et al. (2000). An overview of more recent (approximately year 2000) literature can be found in Jones (2000), Pace-Schott and Hobson (2002), and Saper (2000). The current section is intended to briefly review the most recent (2000–2001) literature on the neurobiology of sleep most relevant to dream science in order to maximize the reference value of this volume for the contemporary (mid-2002) student of this discipline.

New findings on the cellular neurophysiology of sleep

Although the prominence of cholinergic and aminergic neuronal populations in the control of the REM-NREM cycle is well accepted, the intricate modulation of the physiological components of these cardinal sleep stages by a wide …

The target chapters in this book address three issues in the science of sleep and dreaming: the relationship of dreaming to brain physiology and neurochemistry and the possible functions, or lack of functions, of REM sleep and of dreaming. The target chapters provide detailed summaries of previous work and a background to these current issues. This introduction aims to summarize the main claims of each of the target chapters and to cite recent papers of relevance to those chapters that appeared around the same time as or after the production of the BBS special issue. A further update, by Edward Pace-Schott, specifically on the neuroscience of sleep and dreaming, is provided at the end of the book.

The first three target chapters of this book are concerned with the relationship between dreaming and brain physiology and neurochemistry, with particular reference to the relationship of REM sleep to dreaming. Hobson, Pace-Schott, and Stickgold detail their AIM model of the mindbrain during dreaming and other states of consciousness. This model describes three dimensions of brain neuromodulation, these being level of brain activity (A), internal or external source of stimulation for cognition (I), and mode of organization of cognition (M), which they relate to aminergic/cholinergic balance. This chapter emphasizes the importance of REM sleep to dreaming, reviews the comparison of dreaming to waking cognition [of relevance here is Kahn et al. (2000) on how character recognition occurs during dreams], and, in common with Nielsen's target chapter, reviews the history of investigations into the quantitative and qualitative differences and similarities between dreams in REM and NREM sleep.

Abstract: We present evidence disputing the hypothesis that memories are processed or consolidated in REM sleep. A review of REM deprivation (REMD) studies in animals shows these reports to be about equally divided in showing that REMD does, or does not, disrupt learning/memory. The studies supporting a relationship between REM sleep and memory have been strongly criticized for the confounding effects of very stressful REM deprivation techniques. The three major classes of antidepressant drugs, monoamine oxidase inhibitors (MAOIs), tricyclic antidepressants (TCAs), and selective serotonin reuptake inhibitors (SSRIs), profoundly suppress REM sleep. The MAOIs virtually abolish REM sleep, and the TCAs and SSRIs have been shown to produce immediate (40–85%) and sustained (30–50%) reductions in REM sleep. Despite marked suppression of REM sleep, these classes of antidepressants on the whole do not disrupt learning/memory. There have been a few reports of patients who have survived bilateral lesions of the pons with few lingering complications. Although these lesions essentially abolished REM sleep, the patients reportedly led normal lives. Recent functional imaging studies in humans have revealed patterns of brain activity in REM sleep that are consistent with dream processes but not with memory consolidation. We propose that the primary function of REM sleep is to provide periodic endogenous stimulation to the brain which serves to maintain requisite levels of central nervous system (CNS) activity throughout sleep. REM is the mechanism used by the brain to promote recovery from sleep. We believe that the cumulative evidence indicates that REM sleep serves no role in the processing or consolidation of memory.

Keywords: antidepressant drugs, brain stem lesions; dreams; functional imaging; memory consolidation; REM deprivation; REM sleep; theta rhythm …

For centuries there have been theories about how and why sleep occurs. Since the discovery of REM sleep in 1953, science has also asked how and why the individual stages of sleep, such as REM sleep and slow wave sleep, occur and what relationship they have with dreaming. The relationship of dreaming to brain physiology and neurochemistry, and the possible functions, or lack of functions, of REM sleep and of dreaming have also been addressed. This book highlights the current debates, disagreements, and understandings among many of the world's leading researchers, from many different disciplines, on these questions, including both theoretical and experimental work. The book comprises a collection of target chapters, commentaries, and replies to commentaries that were first published as a special issue on sleep and dreaming of the journal Behavioral and Brain Sciences in December 2000.

These are currently areas of great ferment. Fifty years ago dreams seemed to occur almost exclusively in REM sleep, a few years later dreams were also shown to occur in non-REM sleep, and the debate continues today about whether these stages of sleep result in different types of dreams or whether dreaming can occur in all stages of sleep and how closely characteristics of dreaming, such as the illogicality of some dreams or the ease with which they are forgotten, are tied to the physiology and neurochemistry of the brain. Theories of the function of dreams have abounded, from the clearing out of memories to the linking and forming of memories to creative problem-solving. There have also been theories of the function of REM sleep, such as of brain maturation in the newborn and the consolidation of memories at all ages.

Abstract: Numerous studies have replicated the finding of mentation in both rapid eye movement (REM) and nonrapid eye movement (NREM) sleep. However, two different theoretical models have been proposed to account for this finding: (1) a one-generator model, in which mentation is generated by a single set of processes regardless of physiological differences between REM and NREM sleep; and (2) a two-generator model, in which qualitatively different generators produce cognitive activity in the two states. First, research is reviewed demonstrating conclusively that mentation can occur in NREM sleep; global estimates show an average mentation recall rate of about 50% from NREM sleep – a value that has increased substantially over the years. Second, nine different types of research on REM and NREM cognitive activity are examined for evidence supporting or refuting the two models. The evidence largely, but not completely, favors the two-generator model. Finally, in a preliminary attempt to reconcile the two models, an alternative model is proposed that assumes the existence of covert REM sleep processes during NREM sleep. Such covert activity may be responsible for much of the dreamlike cognitive activity occurring in NREM sleep.

Keywords: cognition in sleep; dreaming; NREM sleep; REM sleep; sleep mentation

Introduction

The discovery of REM and NREM mentation

Initial reports of an association between REM sleep and vivid dreaming (Aserinsky & Kleitman 1953; Dement 1955; Dement & Kleitman 1957a; 1957b) inspired studies designed to clarify relationships between sleep physiology and dream imagery. A perspective emerged – referred to by many as the “REM sleep = dreaming” perspective (see Berger 1994; Foulkes 1993b; Lavie 1994; Nielsen & Montplaisir 1994; Rechtschaffen 1994 for overview) – from …

Abstract: Several theories claim that dreaming is a random by-product of REM sleep physiology and that it does not serve any natural function. Phenomenal dream content, however, is not as disorganized as such views imply. The form and content of dreams is not random but organized and selective: during dreaming, the brain constructs a complex model of the world in which certain types of elements, when compared to waking life, are underrepresented whereas others are over represented. Furthermore, dream content is consistently and powerfully modulated by certain types of waking experiences. On the basis of this evidence, I put forward the hypothesis that the biological function of dreaming is to simulate threatening events, and to rehearse threat perception and threat avoidance. To evaluate this hypothesis, we need to consider the original evolutionary context of dreaming and the possible traces it has left in the dream content of the present human population. In the ancestral environment human life was short and full of threats. Any behavioral advantage in dealing with highly dangerous events would have increased the probability of reproductive success. A dream-production mechanism that tends to select threatening waking events and simulate them over and over again in various combinations would have been valuable for the development and maintenance of threat-avoidance skills. Empirical evidence from normative dream content, children's dreams, recurrent dreams, nightmares, post traumatic dreams, and the dreams of hunter-gatherers indicates that our dream-production mechanisms are in fact specialized in the simulation of threatening events, and thus provides support to the threat simulation hypothesis of the function of dreaming.

Keywords: dream content; dream function; evolution of consciousness; evolutionary psychology; fear; implicit learning; nightmares; rehearsal; REM; sleep; threat perception …