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 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.
 
KEY WORDS: Consciousness, Sleep, Dreaming, Neuroimaging, Neuromodulation, Phenomenology, Qualia, REM, NREM

I. INTRODUCTION

Dreaming is a universal human experience which 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, 1993; Fookson & Antrobus 1992), psychophysiology (e.g., Dement & Kleitman 1957), 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 among these fields.

We strongly believe that advances in all these fields make this a propitious time to review and further develop these bridges. It is our goal in this target article to do so. We will study dreams (defined in the American Heritage Dictionary (1992) as "a series of images, ideas, emotions, and sensations occurring involuntarily in the mind during certain stages of sleep") and REM sleep as well as the numerous forms of wake-state and sleep-state mentation. We will also review polysomnographically defined wake and sleep states. Our analyses will be based on comparisons and correlations among these various mental and physiological states.

A. An Integrative Strategy

Three major questions seem to us to be ripe for resolution through constructive debate:

B. A State Space Model of the Brain-Mind

In essence, our view is that the brain-mind is a unified system whose complex components dynamically interact so as to produce a continuously changing state. As such, any accurate characterization of the system must be multidimensional and dynamic and must be integrated across the neurobiological and psychological domains. Both neurobiological and psychological probes of the system must therefore be designed, applied and interpreted so as to recognize and clarify these features.

As a first step in that direction, we have created a three-dimensional state space model that allows us to represent the system according to variables with referents in both the neurobiological and psychological domains as is shown in Figure 1. They are activation (A), information flow (I), and mode of information processing (M). Each of these terms has meaning both at the cognitive and neurobiological levels.

Roughly speaking, these dimensions are meant to capture respectively: (1) the information processing capacity of the system (activation); (2) the degree to which the information processed comes from the outside world and is or is not reflected in behavior (information flow); and (3) the way in which the information in the system is processed (mode).

The resulting state space model, while still necessarily overly simplistic, is nonetheless a powerful tool for studies of consciousness. It captures many aspects of the neurobiological, cognitive and psychological dynamics of wake-sleep states, and is unique in several important respects that we will discuss in light of the controversial conceptual and empirical issues that have stymied the study of waking, sleeping and dreaming.

C. Caveat Lector

In setting the stage for a full explication of our integrative AIM model (part IV) we will review the evidence regarding the differentiation of brain-mind states at the levels of psychophysiology (Part II) and basic and clinical neuroscience (Part III). Although these reviews are extensive, they do not broach many of the fundamental questions of sleep research. For example, we do not consider the biological functions of REM sleep as we do elsewhere (Hobson 1988a) nor do we address the equally interesting question of how psychological and cognitive factors impinge upon sleep neurobiology, a subject which has been the focus of our most recent work (Stickgold et al. 1998a, 1999a,b; Xie et al. 1996). As has often been shown, cognitive activity affects sleep as well as vice versa (e.g., Smith and Lapp 1991) reflecting, certainly, a reciprocal effect of psychological factors and their neural substrates. Additionally, we sidestep entirely the intriguing but difficult issue of whether dreaming itself, as a conscious experience, has a psychological function over and above the postulated benefits of sleep to homeostasis and heteroplasticity (Hobson 1988a). Finally, it is important to note that we deal here exclusively with what Chalmers (1995) has termed the "easy problem" of consciousness, i.e. the mechanisms of the cognitive components of consciousness, rather than the "hard problem" of how consciousness itself could arise from a neural system (see, for example, Tononi & Edelman 1998; Woolf 1997) .

II. THE PHENOMENOLOGY AND PSYCHOPHYSIOLOGY OF WAKING, SLEEPING AND DREAMING

In this section we discuss the evidence which has been gathered over the past 40 years in an effort to define the conscious states of waking, sleeping and dreaming and to measure their formal features quantitatively. With respect to the first question raised by us in the introduction, we will defend the position that these three states can be defined, that their components can be analyzed and measured, and that they are significantly different from one another.

After presenting our justification for this claim, we will address the claim made by many psychologists that differences between REM and NREM mentation - and even differences between REM and waking mentation - are much smaller than we believe. In the course of this discussion, we will identify several areas of disagreement and then suggest some new approaches to their resolution.

Definitions of dreaming have ranged from the broadest "any mental activity occurring in sleep" to the narrower one which we prefer: "mental activity occurring in sleep characterized by vivid sensorimotor imagery that is experienced as waking reality despite such distinctive cognitive features as impossibility or improbability of time, place, person and actions; emotions, especially fear, elation and anger predominate over sadness, shame and guilt and sometimes reach sufficient strength to cause awakening; memory for even very vivid dreams is evanescent and tends to fade quickly upon awakening unless special steps are taken to retain it." We believe that this highly specified definition serves both folk psychology and cognitive neuroscience equally well. It captures what most people mean when they talk about dreams and it lends itself admirably to neurocognitive analysis as we now intend to show.

A. Early findings of distinct differences between REM and NREM mentation

Before proceeding, we provide definitions of "REM" and "NREM" sleep for those readers unfamiliar with these terms. These two clearly distinguishable types of sleep are defined, by convention, in terms of electrophysiological signs detected with a combination of electroencephalography (EEG), electroculography (EOG) and electromyography (EMG) whose measurement is collectively termed "polysomnography" (see Rechtschaffen and Kales 1968). First described by Aserinsky and Kleitmann in 1953, REM sleep (also known as "paradoxical," "active" or "desynchronized" sleep) is characterized by: 1) wake-like and "activated" (high frequency, low amplitude or "desynchronized") activity in the EEG; 2) singlets and clusters of rapid eye movements (REMs) in the EOG channel; and 3) very low levels of muscle tone (atonia) in the EMG channel. Non-REM (NREM) sleep includes all sleep apart from REM and is, by convention, divided into four stages corresponding to increasing depth of sleep as indicated by the progressive dominance of the EEG by high-voltage, low-frequency (also termed "synchronized") wave activity. Such low frequency waves dominate the deepest stages of NREM (stages 3 and 4) which are also termed "slow-wave" or "delta" sleep. We refer the reader to Hobson (1989) for a comprehensive primer on sleep physiology.

Aserinsky and Kleitman's report of the correlation of REM sleep with dreaming (Aserinsky & Kleitmann 1953) began an intense period of research on the relation of brain to mind that lasted well into the 1970s. In the early days of the human sleep-dream laboratory era, much attention was paid to the specificity, or lack thereof, of the REM-dream correlation using the newly available sleep laboratory paradigm. Normal subjects, usually students, were awakened from either the NREM or REM phase of sleep in the sleep laboratory and asked to report their recollection of any mental experience preceding the awakening.

During this period, the similarities and differences in mentation between the brain states of waking, NREM and REM sleep were lavishly documented (e.g., Goodenough et al. 1959; Pivik & Foulkes 1968; Foulkes 1962; Monroe et al. 1965; Foulkes & Fleisher 1975; Herman et al. 1978; Nielsen 1999; Rechtschaffen 1973; Rechtschaffen et al. 1963a; Vogel 1991). We have summarized these REM-NREM differences in Table 1. Some of the important conclusions from this cross-sectional normative paradigm are:

 

a) Following REM sleep awakenings, variously defined dream reports are obtained much more frequently (Aserinsky & Kleitman 1953, 1955; Dement 1955; Dement & Kleitman 1957; Wolpert & Trosman 1958; Kales et al. 1967) or at least substantially more frequently (Foulkes 1962; Goodenough et al. 1965b; Hobson et al. 1965; Molinari & Foulkes 1969; Rechtschaffen et al. 1963; Stoyva 1965) than after NREM awakenings. For reviews of this early work see Foulkes (1966, 1967), Herman et al. (1978), Nielsen (1999), Pivik (1991), Rechtschaffen (1973), and Snyder (1967). In an extensive review of 29 REM and 33 NREM recall rate studies, Nielsen (1999) found an average REM recall rate of 81.8 (+8.7) % compared to an average rate for NREM of 42.5 (+21.0)%.

b) The frequency of dream recall rapidly drops off as awakenings are delayed beyond the end of a REM period (Dement & Kleitman 1957; Goodenough et al. 1965a; Wolpert & Trosman 1958) a finding which has recently been both supported ( Stickgold et al. 1994a) and challenged (Rosenlicht et al. 1994). Subjects who are able to indicate that they are dreaming during sleep more often indicate dreaming during REM than during NREM (Antrobus et al. 1965).

c) There exists a positive relationship of both report word count and subjectively estimated dream duration with the length of preceding REM sleep (Dement & Kleitman 1957) and this relationship has been recently replicated for word count (Stickgold et al. 1994a). Moreover, stimulus-incorporation studies suggest that there exists a positive relationship between the length of time dream events would occupy in real time and the duration of the preceding REM sleep epoch (Dement & Wolpert 1958).

d) Judges are able to distinguish unaltered REM mentation reports from NREM reports (Monroe et al. 1965), a finding that has been recently replicated (e.g., Herman et al. 1978; Reinsel et al. 1992). Furthermore, some dreamers can subjectively determine whether they themselves had been awakened from REM or from NREM (Antrobus & Antrobus 1967).

e) Reports from REM sleep awakenings are typically longer (Antrobus 1983; Casagrande et al. 1990, 1996; Foulkes & Rechtschaffen 1964; Foulkes & Schmidt 1983; Stickgold et al. 1994a; Waterman et al. 1993), more perceptually vivid, more motorically animated, more emotionally charged, and less related to waking life than NREM reports (Antrobus et al. 1987; Cavallero et al. 1992; Foulkes 1962; Herman et al. 1978; Rechtschaffen et al. 1963a; Ogilvie et al. 1982; see Nielsen, 1999 and Table 1 for summaries). In addition, there is linguistic evidence for greater consolidation of dream elements in REM (Salzarulo & Cipolli 1979).

f) In contrast to REM reports, NREM reports contain thought-like mentation and representations of current concerns more often than do REM sleep reports (Foulkes 1962; Rechtschaffen et al. 1963a).

In REM sleep, the integrated conscious experience that is commonly referred to as dreaming is characterized by the following remarkably consistent set of features (see Hobson 1988b and 1994 for reviews):

We interpret the foregoing evidence as strongly supporting our conclusion that there are clear-cut and major differences among the states of waking, sleeping (NREM) and dreaming (REM) at the phenomenological level. We take the robust evidence for quantitative differences in amount of NREM and REM sleep mentation as convincing proof of the validity of an important role for not only activation (factor A) but for the two other factors, information source (I) and modulation (M) in our AIM model. In addition, we take the evidence that state transitions are gradual rather than discontinuous and the evidence that correlations between phenomenology and physiology are statistical rather than absolute as further support of this model.
 

B. Overview of the NREM-REM Sleep Mentation Controversy

While the discovery of REM sleep and its strong correlation with dreaming (Aserinsky & Kleitman 1953) initially led to the strong hypothesis that dreaming occurred only during REM sleep (Dement & Kleitman 1957), this hypothesis was clearly refuted by the discovery that reports of dreaming could be elicited from NREM sleep (Foulkes 1962) and that reports of dream-like mentation could also be obtained at sleep onset (Foulkes & Vogel 1965) and even from quiet waking (Foulkes & Fleischer 1975; Foulkes & Scott 1973). Given dreaming's lack of absolute state specificity, some investigators sought the psychophysiological correlates of specific dream features in the phasic events of REM and NREM sleep (Molinari & Foulkes 1969; see Kahn et al. 1997 and Pivik 1991 for reviews). Again, weak but consistently positive quantitative relationships were found (Kahn et al. 1997; Pivik 1991).

This lack of specificity led at least some investigators ultimately to conclude that investigations of REM sleep neurophysiology could provide no data helpful to understanding the genesis of dreaming (e.g., Bosinelli 1995; Foulkes 1990, 1991, 1993a, 1995, 1996a, 1997; Moffitt 1995). Such a view was encouraged by reports suggesting that in fact the differences between REM and NREM mentation were not nearly as great as had first been reported (e.g., Cavallero et al. 1992). In this section, we will present our reasons for rejecting these conclusions.

How could the firm conclusions of the pioneer era (1955-1975) have apparently dissolved in the subsequent era of growing controversy (1975-1999)? In this section, we will analyze some of the scientific problems that led to the decline of the sleep-laboratory paradigm as this psychophysiological approach lost much of its initially enthusiastic support. In the subsequent section we will turn our attention to the concomitant development of cellular and molecular neurobiology and show how the findings of basic research provided an alternative approach.

1. REM Sleep Dreaming is not Qualitatively Unique

While dream studies generally agree that REM reports are more frequent, longer, more bizarre, more visual, more animated and more emotional than NREM reports (Table 1), a pair of papers published in 1983 (Antrobus 1983; Foulkes & Schmidt 1983) led some researchers to the remarkable conclusion that the "characteristics [of dreaming] are pretty much the same throughout sleep" (Moffitt 1995) and that "dreaming in other sleep stages is not qualitatively different from REM dreaming" (Foulkes 1995). Because these papers are so central to the REM - NREM dreaming debate, we now offer a detailed review and critique of their findings and interpretations.

At the outset, it is important to point out that neither article actually concluded that REM and NREM dreams are indistinguishable, or even substantially the same, in either their quantitative or their qualitative features. In regard to qualitative features, Antrobus (1983) reported that when judges rated 154 REM and NREM reports for their relative "dreaminess" (using scales based on "visual imagery, bizarreness, hallucinatory quality and storylike quality"), they correctly identified 93% of the reports as either REM or NREM, indicating that REM dream reports were much more dreamlike than NREM reports. Similarly, Foulkes & Schmidt (1983, p. 276) concluded that "REM reports are likely to be significantly more dreamlike qualitatively (e.g., in character density, setting clarity) than typical NREM" reports, even when elicited after only five minutes of stage REM.

In regard to quantitative features, when Foulkes & Schmidt (1983) looked at 160 REM and NREM reports and characterized their lengths by the number of "temporal units" (narrative events), their data showed that temporal sequences (sequential events = temporal units - 1) were 14 times more common in REM reports than in NREM reports. In a similar way, Antrobus analyzed total recall frequency (TRF), which reflects the number of words in a report used to describe sleep mentation, and reported that word count significantly distinguished REM from NREM reports (F = 95.52). Using the same reports (J. Antrobus, personal communications), we have determined that the REM reports collected by Antrobus had a median length 6.4 times longer than their matched NREM reports, a number similar to the ratio of 7.0 obtained in a home study using reports from spontaneous awakenings (Stickgold et al. 1994a).

Since both Foulkes & Schmidt (1983) and Antrobus (1983) report such impressive differences between REM and NREM reports, one might wonder how and why these very authors have come to argue so strongly for a phenomenological sameness of these states. The critical question, raised by Foulkes and Schmidt and by Antrobus, pertains to the origin of the differences between REM and NREM reports, "whether there are...qualitative...differences as well as quantitative ones, and...whether such differences are merely attendant upon or are independent of the quantitative ones" (Foulkes & Schmidt 1983, p. 269). Or, as Antrobus wonders, whether "judges of Dreaming [dreaminess] implicitly rely on a dimension similar to the Total Recall Freq." (p. 562). It is this analysis that has led subsequent writers to claim that "when the quantitative characteristics of reports...from REM and nonREM...sleep are adjusted for length there are no differences in the characteristics of the reports" (Moffitt 1995; p. 19).

The normalization-for-length technique has been subsequently used to argue that bizarreness differences between REM and slow wave sleep (SWS) reports (Colace & Natale 1997), the number of dream-like features in a report (Fein et al. 1985; Rosenlicht & Feinberg 1997), memory sources of dreams (Cavallero et al. 1990) and even dream bizarreness itself (Bonato et al. 1991) are all directly and causally dependent on report length independently of sleep stage. Similar arguments have been advanced to explain correlations between dream bizarreness and creativity (Livingston & Levin 1991).

We will shortly reiterate our introductory arguments against this line of reasoning. Meanwhile, we emphasize some of these authors' own data that favor placing a strategic emphasis on the differences between REM and NREM mentation rather than using the similarities as a rationale for rejecting the cognitive neuroscience paradigm in favor of a purely cognitive description of mental states. (A similar critique of purely cognitive descriptions can be found in Nielsen, 1999.)

For example, Antrobus has recently shown that the REM/NREM distinction exerts a far greater effect on bizarreness than diurnal activation (Antrobus et al. 1995). He attributed the observed increase in bizarreness in REM reports to the increased activation seen in that state (Antrobus et al. 1995). It is also noteworthy that purely visual (versus verbal) imagery gave robust REM/NREM differences suggesting a differential sensory activation between the two states (Antrobus et al. 1995). And even when REM and NREM dreams were adjusted for length (a procedure we will shortly argue to be invalid), both Antrobus (1983) and Foulkes & Schmidt (1983) still found significant differences (e.g., in character density and setting clarity) between the two states. Notably, the persistence of a REM/NREM effect on bizarreness, visual imagery and several other dream features in spite of normalization for report length has recently been confirmed (Casagrande et al. 1996; Faucher et al. 1999; Nielsen 1999; Raymond et al. 1999; Waterman et al. 1993). For example, when analysis of covariance (with report length as the covariate) is used to partial out the effect of report length on dream features, REM reports were still judged significantly more visual and bizarre than sleep onset or stage 2 reports (Casagrande et al. 1996) and more visual than NREM reports (Waterman et al. 1993).

Even when dream features appear to be specifically linked to distinctive REM physiology, interpretations can still be cast toward either camp. Hong et al. (1997) reported an impressive correlation between visual imagery and REM density (r = 0.8), which we would argue as evidence for a dependence of dream imagery on a qualitative feature of REM sleep. But Antrobus et al (1995) consider this to be another example of the simple dependence of dream content on levels of brain activation, arguing that rapid eye movements are not under strict brainstem cholinergic control, but come increasingly under the control of the frontal eye fields as general cortical activation increases.

Whatever one's assessment of the similarity versus difference argument, it is clear that none of the analyses in these two papers can distinguish between two competing hypotheses: 1) that dream features are dependent on report length; and its simpler converse 2) that report length is dependent on dream features. We now consider the arguments in favor of the second hypothesis which we have adopted in our own work.

2. The Relationship Between Dream Features and Dream Report Length

That report length depends on dream features was first implied by Hunt (1982) in his analysis of dreaming as fundamentally visuospatial versus verbal-propositional and was then explicitly proposed by Hunt et al. (1993). We agree with their logical assumption that reports with more dream features will require more words to describe them. For example, a report with such dream features as self-representation, visual hallucination, emotion, narrative plot and bizarreness will almost certainly be longer than a report with none of these features. Similarly, it is highly unlikely that a report with a word count of only seven words, the median length of the Antrobus (1983) NREM reports (J. Antrobus, personal communication), could possibly have more than one of the above features.

Inexplicably, Antrobus (1983) and Foulkes & Schmidt (1983) both seem to regard word count and content as independent of each other. In doing so, each has emphasized a very different explanation. Although conceding that alternative explanations were "in no way excluded by these findings," Antrobus (1983) concluded that the NREM reports were shorter due to a defect in "the ability of the subject to recall and describe the [dream] events" (p. 567). On this view, the shorter reports failed to include dream features which were nonetheless present in the NREM dream itself. To us this seems, at best, a risky assumption. In contrast, Foulkes & Schmidt (1983) concluded that the shortened reports and the rarity of dream features reported resulted from differences in dream production. On this view, the differences reflected "the relative paucity and superficiality of mnemonic units active during NREM sleep" (p. 279) compared to REM sleep. The conclusion of Foulkes & Schmidt (1983) is strikingly similar to our position, which is that the relative brevity of NREM reports reflects a decrease in the types (superficiality) and number (paucity) of dream features present in the conscious experience reported in them. If Foulkes really agrees with us on this point, he cannot then also countenance controlling for word count in evaluating reports.

Analyzing the same data set used by Antrobus (1983) we have shown that REM/NREM differences can not be explained simply in terms of report length (Porte & Hobson 1986). Thus we agree with Antrobus when he pointed out that there is still a part of the REM/NREM variance that Dreaming (i.e., judges' idiosyncratic scales for "dreaminess") picks up better than a Total Recall Frequency factor. Similarly, Foulkes & Schmidt (1983) reported that some residual REM/NREM differences in temporal unit composition (e.g., in character density) persist even after report length is controlled. Residual stage differences following normalization for report length in these as well as additional studies have recently been reviewed by Nielsen (1999).

In the face of such unambiguous statements, it is critical to try to understand why these results have been so frequently and so passionately misinterpreted. In part, the erroneous interpretations were encouraged by the original authors. For example, Antrobus (1983, p. 567) concluded that "although there are slight differences ... it is quite clear that the global judgment of Dreaming adds little, if anything, to Total Recall [Frequency] with respect to the association with the sleep stages REM and NREM." Similarly, Foulkes & Schmidt (1983; p. 279) concluded that "most typically observed inter-stage differences in dream reports stem from different lengths rather than the different stages of the reports" (emphasis added). Because they have conflated causality with correlation, both Antrobus and Foulkes & Schmidt unjustifiably assume that most of the differences seen can be explained as correlates of report length. We disagree on the basis of the following studies.

Recent evidence provides strong support for Hunt's proposition that report length reflects the number and intensity of dreamlike features prior to awakening. Hunt et al. (1993) have argued "...it is not the length of the dream that somehow makes bizarreness more likely, but...it is more parsimonious to conclude that episodes of bizarreness within the dream are one major determinant of overall dream length...making length a necessary consequence of bizarreness and not the other way around" (p. 180). In addition, Hunt et al. (1993) note that Hauri et al.'s (1967) factor analysis of dreams found that bizarreness and report length significantly load on the same factor (and therefore strongly co-vary) "...which would make their enforced statistical separation highly questionable" (Hunt et al. 1993, p. 181). In other words, if quantity follows quality and is, in fact, caused by it, then longer reports are needed to describe dreamier dreams. On this view, word count is perhaps even a direct measure of dreaminess and might well be taken as such.

To support their position, Hunt et al. (1993) first demonstrated that awake subjects used more words to describe a visually bizarre picture than a mundane picture. They then showed that the bizarreness scores correlated positively with the number of words devoted to describing the bizarre episodes. Finally, they showed that normalizing dream features for report length actually eliminated the correlations of bizarreness with non-verbal imagination test scores. Hunt and co-workers therefore concluded that bizarreness directly determines a major component of report length and that controlling for total word count introduces an artifactual dilution of bizarreness scores.

In summary, a critical review of the papers of Antrobus (1983) and Foulkes & Schmidt (1983) reveals that these papers report significant quantitative differences in the features of REM and NREM dreams. Both papers also find features such as dreaminess or character density to differ significantly between REM and NREM dreams even when report length is unjustifiably normalized. Neither study reports data that argue against the contention that the strong correlation between report length and dream features occurs because reports with more dream features require more words to describe them (Hunt et al. 1993; Nielsen 1999). We urge the collection of additional data to further clarify the nature of these REM/NREM differences. Such data should include ample numbers of reports, collected longitudinally in naturalistic settings, which are obtained from home awakenings physiologically monitored with unintrusive devices such as the Nightcap (e.g., Rowley et al. 1998).

C. Methodological Considerations in the Study of Dreaming

The study of mental states is replete with methodological shortcomings and conceptual confusions. We believe that some of these areas of confusion can be clarified in a manner which could increase consensus. In what follows, we address five methodological issues to point out the nature of the problems, offer clarifications and suggest possible resolutions.

1. The Reduction of Psychological States to Narrative Reports

The most profound problem in studying conscious states is the necessity of reliance on verbal reports. This method is problematic because these accounts are just reports, not the subject's experience of the states themselves. This reduction of conscious experience to prose has at least four important ramifications:

1) A multimodal conscious experience including pseudo-sensory perceptual, emotional and motoric dimensions is reduced to only one mode, that of narration. (To emphasize this point, we merely point out that if a picture is worth a thousand words, we certainly are not getting the whole picture with a seven-word report!)

2) The narratives describing sleep state mentation are all generated during the waking state and are thus likely to mix, if not contaminate, the dreaming phenomenology with the phenomenology of waking (for a discussion of this point relative to dream meaning, see Hunt 1989, p. 9).

3) Analysis of narrative dream reports is extremely limited in its power to recreate or model the true underlying mechanism of dream production at any fundamental, primordial level of explanation (be it cognitive-mnemonic, linguistic or neuropsychological) because narratives about experience display a high degree of what Pylyshyn (1989) terms "cognitive penetrability."

Pylyshyn's point can be applied to dreaming as follows. The behavior of the dream production system is highly malleable using the same cognitive processes invoked to explain its behavior such as the dreamer's goals and beliefs (see Pylyshyn 1989). For example, in the case of the dreamer's goals, the frequency of overall dream recall as well as lucidity can be greatly increased by auto-suggestion techniques which employ many of the same cognitive abilities (e.g., imagination and visualization) that most theorists believe contribute to dream production itself (see Section III.C.). In the case of beliefs, the meaning of a dream experience while it is occurring is highly dependent on the dreamer's personal (and changeable) philosophy of what dreaming is (e.g., a message from a deity, a psychopathomimetic experience, "travel outside the body," etc.). According to Pylyshn (1989) such highly penetrable experiences, rather than illustrating primordial cognitive mechanisms, instead reflect "the nature of the representations and...cognitive processes operating over these representations" (p. 81) which, in the case of dream reports, is language itself. Given that Pylyshn (1989) asserts that cognitive penetrability can affect even highly objective and replicable psychological data (such as the visualized-image-size/image-scanning-time relationships described by Kosslyn), penetrability is all the more likely to influence the highly elaborated and individualistic phenomenon of dream reporting. The rendering of dream reports in conventional (wake state) grammar and syntax may, therefore, tend to obscure important differences between the actual experiences of waking and dreaming.

These considerations raise the concern that using the sentence or the word as a unit for quantifying mental activity may say more about language than about the multimodal nature of conscious experience. This is important because so many researchers consider the quantification of report length as the single most salient feature of a dream. In this context, it is also worth noting that verbal retrospective reports are often considered inadequate to describe mental states which are closer to dreaming than to waking mentation. These states include religious conversion, near-death experience, functional psychosis, delirium, drug-induced conditions and other altered states of consciousness.

This aspect of the REM physiology-dream mentation controversy may be particularly relevant to the current debate about self-representation and bizarreness in dreams of children aged 3 to 8 (see Foulkes 1990, 1993a, 1996, 1997 and Resnick et al. 1994). Based upon an extensive longitudinal study (Foulkes 1982a) and a later cross-sectional study (Foulkes et al. 1990), Foulkes asserted that "dreaming is absent until ages 3 to 5 and does not assume the form of adult dreaming until ages 6 to 7" (Foulkes 1997, p. 4). Foulkes hypothesizes that, lacking or being deficient in their ability to consciously mentally represent their perceptuo-behavioral experience, young children (like animals) may not experience dreaming in spite of having an abundance of REM (Foulkes 1990, 1993b). He argues further that dreaming is "..a high-level symbolic skill, a form of intelligent behavior with cognitive prerequisites and showing systematic development over time" (Foulkes 1993b, p. 120), and that dreaming has as its prerequisite conscious representational competence (Foulkes 1990; Foulkes et al. 1990). As evidence to support this he cites studies in which he finds very low recall of dreaming and little bizarreness prior to age 5 (Foulkes 1982a; Foulkes et al. 1979), low rates of reporting at ages 5-8 (Foulkes 1982a; Foulkes et al. 1990), acquisition of kinetic versus static imagery only after age 6 (Foulkes et al. 1990), and acquisition of self-representation as an active dream participant as well as narrative continuity only after age 7 (Foulkes et al. 1990, 1991). Further, from his data showing correlation of report rate with measures of visuospatial versus verbal skills (Foulkes et al. 1990), Foulkes (1993a) suggests that "...young children may fail to report dreams because they are not having them, rather than because they have forgotten them or are unable to verbalize their contents" (p. 201). For a recent review see Foulkes (1999).

Subsequent studies have shown that dream bizarreness does indeed increase over ages 3 to 8 (Colace et al. 1993, 1996, 1997; Resnick et al. 1994). However, other of Foulkes' findings have not been supported. For example, dream reporting rates in 4 to 5 year olds has been reported to be almost identical to that in 8 to 10 year olds (Resnick et al. 1994). In addition, active self representation in dreams of 4 to 5 year olds has been reported to occur in over 80% of their dream reports (Colace et al. 1995; Resnick et al. 1994). Finally, substantial occurrence rates for bizarre elements have been reported in the dreams of both 4 to 5 year olds (0.45 per 100 words) and 8 to 10 year olds (0.71 per 100 words) (Resnick et al. 1994).

Moreover, although rates of adult dream recall have been related to performance on tests of visuospatial skill (Butler & Watson 1985), rates of dream recall have also been correlated with individual differences in visual memory (Schredl et al. 1995). Therefore, any ontogenetic changes in visual memory would confound the effects of developmental changes in higher order visuospatial skills on dream reporting rates in children.

Overarching these conflicting data, however, is the theoretical point bearing on the current discussion: i.e., that dream reports are given in waking and thus, of necessity, must be constrained by an organism's waking cognitive and linguistic abilities. At one extreme, it must be conceded that even if a cat had the most vivid of "dreams," it would not be able to report it. Similarly, if a toddler is variously unable (or unwilling) to conceive and verbalize a complex perceptual-emotional-motor REM experience, it does not mean it was not originally experienced in some form which, later in life, might be reported as a dream. In other words, we challenge here the assumption by Foulkes (e.g., 1990) and others (e.g., Bosinelli 1995) that "dreaming" is an experience which can only occur if it can be later be reported by an organism possessing linguistic abilities. We recognize that verification of oneiric activity in organisms which are unable to report (or even, possibly, reflect upon) their experiences is currently impossible, although we do not rule out the possibility that new methods may someday provide hints as to the conscious experiences of non-verbal beings (e.g., see Marten and Psarakos 1995).

Nevertheless, as with many other psychological constructs such as emotional expression (e.g., Darwin 1873) or behavioral inhibition (e.g., Goldman-Rakic 1987), such inferences drawn between human developmental as well as mammalian phylogenetic levels has a long scientific tradition. It is, therefore, not inherently invalid to cautiously speculate from adult human oneiric experience to observed REM behavior in infants and animals, especially given the abundant behavioral correlates (e.g., ethologically meaningful oneiric behavior; for a full discussion see Jouvet, 1999). Similarly, we specifically suggest that the human neonate, spending as it does more than 50% of its time in REM sleep (Hobson 1989), is having indescribable but nevertheless real oneiric experiences. An infant's waking experience remains essentially indescribable and speculative to us older persons but we do not doubt that infants enjoy some sort of waking conscious experience. For us, it is not at all difficult to imagine that an infant might be experiencing hallucinosis, emotions, and fictive kinesthetic sensations during REM sleep.

Given these caveats, we suggest that more effort be put into the development and use of other methodologies and scales such as the photo-response visual brightness and clarity scale (Antrobus et al. 1987, 1995; Rechtschaffen & Buchignani 1992), temporal unit analysis (Cavallero et al. 1990; Foulkes & Schmidt 1983), computerized content analyses (Gottschalk 1999), the analysis of dream drawings (Hobson 1988b), or the use of affirmative probes (e.g., Herman 1992; Merritt et al. 1994; Pace-Schott et al. 1997; Stickgold et al. 1997a; see Herman 1992 and Hobson & Stickgold 1994a for further discussion). In other words, we need recourse to more diverse and creative means to elicit more detailed descriptions of salient aspects of conscious experience.

2. The Sleep Laboratory Environment

The sleep laboratory itself constitutes a second major methodological problem. Anyone who has ever slept in a sleep laboratory (as all of us have!) knows that it is an inhospitable and unnatural setting which makes sleep more difficult and less deep than is possible in more naturalistic settings. To appreciate this point, the reader need only imagine going to an unfamiliar place in an inner city neighborhood of dubious safety, encountering a technician who is a stranger and often of the opposite sex, having ten electrodes affixed to the scalp with cement that smells like airplane dope and then being bid "goodnight" and "pleasant dreams." Hence the famous first night effect (objectively poor sleep owing to discomfort and anxiety) often extends to a second night, and may contribute to a constriction of dream experience (as in dreams of the sleep lab setting) over even longer times. The laboratory environment may even alter the content of dreams for spontaneous awakenings in the laboratory at the end of a night's sleep as evidenced by the high frequency of laboratory references in morning spontaneous awakening REM and NREM laboratory dream reports (Cicogna et al. 1998).

Studies such as those of Dement et al. (1965), Domhoff & Kamiya (1964), Okuma et al. (1975) and Whitman et al. (1962) have shown substantial incorporation of the experimental situation into laboratory dream reports particularly on the first night in the laboratory but persisting, at a lower level, into subsequent laboratory nights (Dement et al. 1965; Domhoff & Kamiya 1964). Similarly, content differences have been noted between laboratory and home dreaming (Domhoff & Kamiya 1964; Hall & Van de Castle 1966). Although these early studies were confounded by spontaneous (home) versus instrumental (laboratory) awakening conditions (as has been noted by Foulkes 1979), later studies controlling for reporting conditions (Lloyd & Cartwright 1991; Weisz & Foulkes 1970) still found some content differences between the home and laboratory dreams of adults. Waterman et al. (1993) emphasize that home-laboratory differences can arise from both environmental factors and factors related to investigator expectancies and, therefore, both should be controlled. In our view, adaptation to the sleep lab may take four days or longer (see Domhoff & Kamiya 1964) exceeding the length of most laboratory studies.

As in the case of NREM compared to REM dreaming, we are not arguing for a gross, qualitative distinction between home and laboratory dreams. Laboratory dreams are, undoubtedly, largely representative of many of the formal and content features of dreaming in naturalistic settings. Nevertheless, we suggest that quantitative constraints on the dreaming experience may be imposed by the laboratory setting such that the full potential expression of certain dream features is limited. Of additional concern is the finding by Antrobus et al. (1991) that REM-NREM differences in both word count and global judgement of dreamlike quality diminish over 14 nights in the sleep laboratory, an effect they attribute largely to motivational factors in dream reporting. Minimizing any such "laboratory-fatigue" confound constitutes further argument for longitudinal awakenings to be performed in the more comfortable environs of the home.

To overcome these problems, several options are possible. First, laboratory studies can simply be extended in time, perhaps recording each subject for a full week. This has obvious disadvantages including inconvenience, high cost and the above noted motivational effects. A second option is to continue to run relatively short (1 - 4 night) paradigms, and accept the suppressive effects on sleep architecture and dream content. While perhaps no longer normatively valid, the data obtained would still be at least reliable. A third option, and the one that we have chosen, is to move recording into the home for prolonged recording sessions using the Nightcap (Ajilore et al. 1995; Mamelak & Hobson 1989b; Pace-Schott et al. 1994; Rowley et al. 1998; Stickgold et al. 1994a, 1998b).

3. The Question of "Similarity" and "Difference"

We have long thought that the argument over whether mentation in two states like REM and NREM sleep is more similar or different was specious. Thinking the dilemma to be false, we have ignored or minimized it in our previous writings. However, we now feel obliged to clarify for the reader how the debate over REM and NREM mentation has become inextricably entangled with the larger and more general question of the mind-brain problem. In doing so, we hope to elevate the debate from the parochial to the general level and to make our own position on mind-brain issues crystal clear.

In some ways, understanding the conflicting opinions that swirl around the sleep and dream mental content debate is relatively straightforward. One group of psychologists, exemplified by David Foulkes and the late Alan Moffitt, hypothesizes that the brain and the mind are so loosely linked that the study of the mind need not be constrained - or even informed - by the study of the brain (e.g., Bosinelli 1995; Foulkes 1991, 1993a, 1996a, 1997; Moffitt 1995). This group interprets the empirical data as indicating that mental content does not differ qualitatively across brain states. There is only one dream mentation production system which is more or less active during waking and sleep. In such theories, termed "One-Generator" models of sleep mentation by Nielsen (1999), it is only the fluctuating level of cognitive activation that determines differences between REM and NREM sleep in report length as well as in the broad range of dream features that co-vary with report length. By taking this position, these psychologists minimize the importance of physiology, which they assert to be irrelevant to the understanding of dreaming. How cognitive activation could be independent of brain activation is a question not addressed by these scientists.

Another group, consisting largely of psychophysiologists, holds that the mind and the brain form an integrated system, so tightly linked within and across states that detailed qualitative and quantitative distinctions at either level of analysis imply the existence of isomorphic distinctions at the other. This is the position that we take. For us, the cognition production system is the brain. And, of course, it is always the same brain. But we know that the brain's mode of information processing changes radically across states. So, therefore, must its mental products. Nielsen (1999) terms this point of view a "Two-Generator" model of sleep mentation. For us, the state-specific changes in brain function virtually guarantee concomitant changes in mental function, even if our psychological methodology may still be inadequate to identify these changes (just as for many years the physiological changes also eluded us!).

With respect, we suggest that the failure to demonstrate psychological differences concomitant with physiological ones must be laid at the door of inadequate psychological methodology. If psychology has so far failed to document the robust phenomenological differences between waking and dreaming that most people experience every day of their lives, then more vigorous and more creative psychological research is needed. Otherwise we are faced with the absurd and unacceptable conclusion that brain and mind have nothing to do with each other.

That even a single, "One-Generator" system (i.e., a "dream mentation production system") may show dramatically different features in different states is in no way a self-contradiction. To our way of thinking, states of the brain are analogous to other dynamic states of matter. Consider, for example, the way that liquid water changes state with changes in temperature: above 100° C it is steam; below 0° C it is ice. These states are analogous to the states of waking, NREM sleep and REM sleep in the brain (as well as to less common mental states such as coma, hypnosis and mania). No one would say that in the frozen state (ice) or in the vapor state (steam) that the material is not still water. Nor could any sentient person ignore the obvious differences in the properties and behavior of water across states. We believe that it is equally inappropriate to argue that since there is a single dream production system (i.e., the brain-mind), that the properties and behavior of its products, e.g., dreams, must be identical or even similar across different states. Such an important error in scientific thinking would lead to minimizing or missing entirely the change in matter (in this case the brain) that underlies the change in its state-dependent properties (in this case consciousness).

The question of whether REM and NREM mentation are the same or different has often devolved into a search for characteristics of mentation that are absolutely unique to REM sleep. We consider this quest to be a fool's errand and indeed no absolute qualitative distinction between the two states has yet been documented. Since the late 1950s, many sleep laboratory studies have shown substantial recall of mentation from NREM, thereby obviating an exclusive association of sleep mentation with REM (Cicogna et al., 1998; Foulkes 1962, 1966; Foulkes & Rechtschaffen 1964; Goodenough et al. 1959, 1965a; Kamiya 1961; Pivik & Foulkes 1968; Rechtschaffen et al. 1963; Salzarulo & Cipolli 1979; Stoyva 1965; Molinari & Foulkes 1969; Zimmerman 1970; see Foulkes 1967, Herman et al. 1978 and Nielsen, 1999 for reviews). For example, among nine studies, the percentage of NREM awakenings yielding at least minimal recall varied from 23 to 74% (Foulkes 1967) and, as noted, Nielsen (1999) has found an average NREM recall rate of 42.5% over 33 published studies. Recall rates similar to those of NREM in general have even been obtained from stages III and IV of NREM (e.g., Bosinelli 1995; Cavallero et al. 1992; Goodenough et al. 1965a; Herman et al. 1978; Nielsen, 1999; Pivik & Foulkes 1968; Salzarulo & Cipolli 1979; Tracy & Tracy 1974). In a review of eight studies of stages III and IV mentation, Nielsen (1999) found an average recall rate of 52.5 (+18.6) %, but also notes that a substantial percentage of subjects never recall stage III and IV mentation or require several nights of awakenings before reporting such mentation.

The findings of several studies have countered the hypothesis that NREM mentation is simply recall from previous REM (Foulkes 1962, 1967; Foulkes & Rechtschaffen 1964; Goodenough et al. 1965a; Rechtschaffen et al. 1963), although report length does drop precipitously following the end of REM periods (Stickgold et al. 1994a).

The fact that differences are not absolute does not mean however that no differences exist. Indeed, all the evidence shows that such differences do exist and we have already advanced good reasons to believe that these may have been seriously underestimated. For example, similarities in dream features such as bizarreness may be inflated when report length is controlled in REM and NREM reports (Hunt et al. 1993) and REM-NREM bizarreness differences may persist even when report length is partialled out (Casagrande et al. 1996; Nielsen 1999; Waterman et al. 1993). In addition, recent work comparing sleep onset REM and NREM dreams using an experimental protocol which controlled for previous sleep and waking time has shown that sleep onset REM periods are specifically related to physiological signs of REM whereas NREM dreams were related to intrusions of waking into NREM (Takeuchi et al. 1999b). These authors conclude that the mechanisms underlying REM and NREM dreaming must, therefore, differ (Takeuchi et al. 1999b). Therefore, we conclude that while some NREM dreams approach REM dreams in length, vividness, dreaminess and bizarreness (Cicogna et al., 1998; Foulkes & Schmidt 1983; Herman et al. 1978; Nielsen, 1999) and while "dream-like" versus "thought-like" mentation may predominate in some NREM reports (Foulkes 1962; Nielsen 1999; Rechtschaffen et al. 1963a; Zimmerman 1970), NREM reports are far more likely than REM reports to be short, dull and undreamlike (Nielsen 1999; Rechtschaffen et al. 1963).

Much of the above-noted problems inherent in assessing the similarity versus difference of two phenomena can be addressed with improved methodologies. For example, when two such states (such as REM and NREM) are being compared in terms of specific parameters (such as bizarreness) to a third state (such as waking), the question of the similarity versus difference between the two states then becomes much more tractable.

4. The Source and Fate of Dream Memory

A tendency to emphasize psychological similarity has also characterized recent studies on the memory sources of REM and NREM dreams. Using a modification of Tulving & Thompson's (1973) classification of memory sources and an experimental free association technique, Cavallero and his colleagues initially found a distinct difference in memory sources between early-night REM and NREM mentation (Bosinelli 1991; Cavallero & Cicogna 1993; Cicogna et al. 1986). Early-night NREM sources consisted primarily of discrete biographical episodes while REM sources were a mixture of episodic, abstract self-referential and semantic sources (Bosinelli 1991; Cavallero & Cicogna 1993; Cicogna et al. 1986). This observation fits with the commonly accepted distinction between NREM dreaming as a simpler and REM dreaming as a more complex state of consciousness.

However, when REM and NREM reports were collected later in the night and matched for "temporal unit composition" (a procedure akin to diluting bizarreness by controlling for word count), these same researchers emphasized the similarity of memory sources between REM and NREM (Bosinelli 1991; Cavallero & Cicogna 1993; Cavallero et al. 1988, 1990, 1992; Cicogna et al. 1991; Fagioli et al. 1989). Likewise, Cicogna et al. (1991) reported few REM/Stage 2 differences in number of temporal units, implausibility, self presence, settings or characters. Nonetheless, as in the case of dream content (Antrobus 1983; Foulkes & Schmidt 1983), some residual state-related memory source differences continued to be reported (Cavallero & Cicogna 1993; Cavallero et al. 1990, 1992; Cicogna et al. 1991) and these need to be explained.

The research on memory sources for mentation among the different behavioral states overlooks the far more robust difference in the overall functioning of memory processes that distinguishes sleep from waking. This is the notorious difficulty of recalling dreams or any other mental content following either instrumental laboratory or spontaneous awakening. Many dreamers are aware that recall actively eludes them as they awaken. And even when dream recall is confident and detailed, it is common for subjects to assert that they are sure that there was much more antecedent dreaming that could not be recalled. One reason for the neglect of this robust phenomenon is that it is difficult to study something, in this case memory, that isn't there! But the very absence of recall is a datum which any dream theory must explain, especially in the face of the robust brain activation in REM sleep!

Freud's famous explanation was that dream forgetting was an active function of repression. We have instead attributed this prominent failure of recall to a state dependent amnesia caused by aminergic demodulation of the sleeping brain (Hobson 1988b). The waking level of aminergic modulation falls to 50% in NREM sleep and to nearly zero in REM (Hobson & Steriade 1986; Steriade & McCarley 1990). It would appear that the intense activation of REM must overcome this demodulation and persist into subsequent waking in order for very vivid dreams to be remembered. In our view, the low level of production and recall of NREM mentation is due to the additive effects of inactivation and demodulation.

A strong implication of this model is that memory may be as deficient during dreaming as it is upon subsequent awakening. This hypothesis is consonant with subjective experience. For example, when one introspectively compares recall of a night's dreaming with that of a corresponding waking epoch, one of the most obvious differences lies in the far greater amount of detail which can be recalled in waking. Likewise, it is commonplace for long dreams to have complete scene shifts of which the dreamer takes no significant cognitive account. If such orientational translocations occurred in waking, memory would immediately note the discontinuity and seek an explanation for it. This intuitively convincing difference between memory for dreaming and memory of waking mentation is confirmed by several empirical studies. While the frequent inability to recall dreamed experience in subsequent waking has been a robust finding in dream research (Goodenough 1991), there is also strong evidence of deficient memory for prior waking experience in subsequent sleep.

For example, little continuity has been shown between pre-sleep stimuli and the content of REM dreaming when this phenomenon has been probed using the following paradigms:

1) Specific experimental pre-sleep stimuli in the form of films have little effect on dream content (Cartwright et al. 1969; DeKoninck & Koulack 1975; Foulkes et al. 1967; Foulkes & Rechtschaffen 1964; Goodenough et al. 1975; Karacan et al. 1966; Witkin 1969; Witkin & Lewis 1967).

2) Specific experimental pre-sleep stimuli such as static visual images or altered social milieu are rarely incorporated into dreams (Carpenter 1987; Orr et al. 1968; Shevrin & Fisher 1967).

3) Specific pre-sleep waking behavioral or thought experiences are not easily detectable in subsequent dreams (Bakeland et al. 1968; Bakeland 1971; Breger et al. 1971; Cartwright 1974; Hauri 1970).

4) Presleep mentation is infrequently picked up by the dream process (Rados & Cartwright 1982; Roussy et al. 1996, 1997).

5) Naturalistic daytime events rarely enter dream content, casting grave doubt on the classical psychoanalytic concept of day residue as dream instigator (Epstein 1985; Harlow & Roll 1992).

6. Pre-sleep modification of biological drives or perceptual experience has very weak effects on dreaming (Baldridge et al. 1965; Bokert 1968; Dement & Wolpert 1958; Roffwarg et al. 1978). (For reviews see Arkin & Antrobus 1978 and Cavallero & Cicogna 1993).

It must, therefore, be concluded that since dreaming is so little shaped by pre-sleep experience, memory systems active during REM sleep have extremely poor access to recent waking memories. Even if dreaming is concerned far more with emotionally salient content than with current events, it is remarkable that the dream construction process fails to incorporate recent episodic memories, including emotionally salient ones, to any significant extent. Two experimental exceptions to this generality, however, should be noted. The first involves the practice of dream incubation whereby focused pre-sleep attention on a specific concern has been shown to increase its rate of occurrence in subsequent dreaming (Saredi et al. 1997). Dream incubation techniques, however, introduce substantial confounds in the form of artificially imposed practice effects as well as the focus on emotionally salient issues. The second involves the finding by Rosenblatt et al. (1992) that significantly more of cartoon segments viewed prior to sleep were recalled following REM versus Stage 2 NREM awakenings, a difference which disappears if a 30 second pre-reporting waking delay is interposed after awakening. Following the arousal-retrieval model of Goodenough (1991), Rosenblatt et al. attribute this REM-NREM difference to greater mnemonic capacity immediately following post-REM versus post-NREM awakenings resulting from greater immediately pre-awakening cortical arousal in REM versus NREM. Utilizing the semantic priming task, we have recently reported a similarly positive mnemonic effect of pre-awakening REM versus NREM for associative memory processes (Stickgold et al. 1999c). Certain forms of memory, such as generating associations to weakly related word primes, may, in fact, be preferentially enhanced by both the activation and the neuromodulatory differences (see section IV) between REM and NREM (Stickgold et al., 1999c). In contrast, greater sleep inertia (Dinges 1990) following NREM awakenings (a phenomenon undoubtedly reflecting low pre-awakening brain activation) may less selectively impair a wide spectrum of mnemonic processes.

Even within sleep, memory appears impaired. If episodic experiences within sleep were to persist in the sleeper's memory, one would expect greater content and thematic continuity between contiguous REM periods than more distant REM periods. But despite the fact that content and thematic continuity of successive dreams is greater within the same night than across nights, continuity does not differ between contiguous and noncontiguous REM periods of the same night (Cipolli et al. 1987; Fagioli et al. 1989).

We have recently completed three preliminary studies which seek to quantify aspects of memory within sleep and to compare sleep memory to waking memory. In the first study, 27 subjects became aware of and could later recall three aspects of their memory functioning (semantic, recent and remote episodic) more often during two waking experiences than during dreaming. Since both types of waking experience sampled were much shorter than the duration of a night's dreaming, results further support the concept of a mnemonic deficiency in dreaming compared to waking (Pace-Schott et al. 1997b).

A second study examined perceived duration of dreaming. The 22.5 minute median perceived duration of dreams by 54 subjects was associated with an unexpectedly large variation. Even ignoring the highest and lowest 10% still left a 24-fold variation. Such wide variance in a basic memory function further suggests a profound alteration of memory processes in dreaming as compared to waking (Stickgold et al. 1997a).

In the third study, 11 subjects recorded the processes by which a total of 103 dreams were recalled. Fifty-two reports (50%) were recalled in "chunks" (i.e., entire dream segments were recalled as units). Another 38 reports (37%) were recalled all at once upon waking and 13 reports (13%) were recalled gradually. Nine of the 11 subjects reported at least one dream recalled in chunks, and there were often significant delays between the recall of different "chunks." These results point strongly to the presence of stored dream memories which cannot be readily accessed on awakening and further suggests both qualitative and quantitative alterations in basic memory processes during and after dreaming (Stickgold et al. 1997a; Stickgold 1998).

All of the above findings can be regarded as being caused by the failure of recent episodic memory (as defined by Tulving 1994) in sleep. And as we have noted, recent episodic memory is weak across wake-sleep and sleep-wake transitions as well as within sleep itself (Pace-Schott et al. 1997a). We believe that a deficiency of memory in dreaming may go a long way toward explaining such distinctive and robust dream phenomena as orientational instability, loss of self-reflective awareness, and failure of directed thought and attention.

5. Type I vs. Type II Statistical Analyses

In analyzing studies of dream mentation, it is important to understand the nature of the statistical tests employed. In general, such tests calculate the probability that a specific null hypothesis - normally that there is no difference between two population samples - is or is not true. The most common statistical tests, i.e., Student's t-test and ANOVA, measure Type I error which determines the probability that the obtained results could be explained by the null hypothesis. When the probability is sufficiently low, normally less than 0.05, the null hypothesis is rejected and one concludes that the populations are different. Such analyses, however, provide no information on whether or not the null hypothesis is true. Thus, while a low p-value provides strong evidence that the null hypothesis is false, a high p-value does not necessarily indicate that it is true.

This is relevant to the conclusion of both of the papers we critiqued above. Antrobus (1983) concluded that "the global judgment of Dreaming adds little, if anything, to Total Recall Content with respect to the association with the sleep stages REM and NREM" (p. 567), although his statistics did confirm a significant contribution (F(1,71)=15.9, p<0.01). Nevertheless, this conclusion formed the basis of the wider interpretation that the differences between REM and NREM reports are merely a consequence of enhanced recall in REM.

In the second paper critiqued, Foulkes & Schmidt (1983) concluded that global discontinuity "is stage-invariant [and] never significantly discriminated reports from different stages of sleep, even in length-uncontrolled comparisons" (p. 277). While this was true, it was also true that sleep onset reports contained 2.3 times more global discontinuity than NREM reports, a ratio that increased to more than 3 to 1 when normalized for report length (measured in "temporal units"), a fact that could lead to a conclusion quite different from the one drawn by the authors.

It thus appears premature to conclude, based on these early studies, that robust differences between REM and NREM sleep mentation do not exist. Until studies are carried out that measure Type II error and determine the likelihood that the null hypothesis is correct, it is only safe to say that these studies have failed to demonstrate either the presence or absence of differences between REM and NREM mentation. Under the circumstances, more recent studies reporting the presence of significant differences would appear more easily interpreted.

6. The Need for New Approaches

The conclusion that we draw from all these studies is that there are significant differences between the formal aspects of the states of consciousness associated with waking, NREM and REM sleep. These differences, which are quantitative not qualitative, have not yet been adequately characterized for a variety of methodological reasons. Instead of continuing to argue over this issue, we urge our colleagues to join us in a more creative attempt to capture and measure the dimensions of conscious experience.

Basing the attempt to characterize dreaming solely on the basis of verbal reports of the poorly recalled subjective experience of subjects sleeping in unfamiliar, non-natural settings has led, not surprisingly, to a sterile and non-productive controversy about whether the conscious correlates of waking, NREM sleep and REM sleep are more similar or different and to a very unfortunate split in what was once a unified field.

This mind-brain split is akin to the gulf that opened between psychiatry and neurology after Sigmund Freud abandoned the goals of his brain-based Project for a Scientific Psychology and declared brain science off limits to his psychology. To reunify two approaches that belong together, we call for a new neuropsychology of conscious states that integrates from the level of cellular-molecular events to the formal features of the mental states of which they form the substrate.

III. THE COGNITIVE NEUROSCIENCE OF WAKING, SLEEPING AND DREAMING

We now turn our attention to the shifts in activation level, input-output gating processes and the neuromodulatory balance of the brain that underlie the ultradian REM/NREM cycle in humans and in animals. We first enumerate the profound physiological differences that distinctively differentiate waking, NREM and REM sleep and show that these differences are as robust as those shown above in the phenomenology of waking, sleeping and dreaming. Then, we point out relationships between the physiological and phenomenological changes seen as the brain-mind shifts from one state to another, as a prelude to integrative modeling. Our overarching hypothesis is that for each phenomenological difference seen between conscious states it is possible to identify a specific physiological counterpart. The end result is a first approximation of a cognitive neuroscience of brain-mind state.

A. Recent Findings in Human Neurobiology

1. Neuroimaging Studies

The experimental study of human REM sleep dreaming has until recently been limited on the physiological side by the poor resolving power of the EEG. Even expensive and cumbersome evoked potential and computer averaging approaches have not helped us to analyze and compare REM sleep physiology with that of waking in an effective way. This limitation has probably helped reinforce the erroneous idea that the brain activation of REM sleep and waking are identical or at least, very similar. However, recent technological advances in the field of human brain imaging have made it possible to document a highly selective regional activation pattern of the brain in REM sleep (Braun et al. 1997, 1998; Maquet et al. 1996; Nofzinger et al. 1997). At the same time, experiments of nature - in the form of strokes - have allowed a correlation of the locale of brain lesions with deficits or accentuations of dream experience in patients (Doricchi & Violani 1992; Solms 1997).

Before discussing these intriguing new results, it is important to stress the methodological limitations of both the brain lesion and imaging techniques. We know from our long and relevant experience in basic sleep research that neither method can capture many significant mechanistic and functional details that emerge from cellular and molecular level neurophysiology (see Steriade and Hobson 1976 and Hobson et al. 1986 for a full discussion of these issues). For example, it is now clear that the lesion method, applied to the pontine brain stem, gave misleading results regarding both the general role of that region in state control and failed even to hint at the specific functions of its subcomponent nuclei. This is because the lesion method cannot discriminate between the effects of destruction and disconnection and cannot target specific neuronal groups in heterogeneous regions like the brain stem.

It is important to note that the preliminary regional functional neuroimaging studies which we review below suffer from such unavoidable limitations of new technologies as the following (see Rauch & Renshaw 1995 for a more complete discussion). First, one must consider whether or not more efficient functioning of an area might result in less versus more observed metabolism or whether glucose or oxygen uptake by inhibitory interneurons may produce local maxima in areas that are, in fact, less active due to inhibition. Second, there are statistical problems inherent in the small sample sizes used in some of these sleep studies (e.g., Braun et al. 1998; Nofzinger et al. 1997) as well as the repeated comparisons employed by the statistical parametric mapping technique (Friston et al. 1991) which is used by all these investigators. Third, global activation measures like electroencephalographic voltage averaging or cerebral blood flow cannot be expected to reveal mechanistic and functional details because they cannot identify small but influential neuronal populations like the locus coeruleus, the raphe nuclei and the pedunculopontine tegmental nucleus. Fourth, there is the potential of altered sleep physiology due to the sleep deprivation (Maquet et al. 1996) or REM deprivation (Braun et al. 1997, 1998) procedures used to maximize sleep stability and stimulate REM in these studies. And fifth, the functional activity of a brain area may vary with changes in its inputs as most dramatically illustrated by neuroplasticity involving recruitment of dedicated brain areas to subserve new modalities such as the visual cortex in braille learning (e.g., Pascual-Leone 1999) or the reorganization of visual association cortex following V1 damage (e.g., Baeseler et al. 1999). Additionally, it is possible that normal functional disconnections, as as occurs between V1 and visual association cortices in REM (Braun et al., 1998), result in the same neural structures performing differing, state-specific functional tasks.

In spite of these caveats, the widespread use of this technology and the broad agreement of the data with clinical neuropsychological findings argues strongly for the basic validity of neuroimaging as a tool in cognitive neuroscience (Cabeza & Nyberg 1997). Specifically in response to the fifth caveat above, strong suggestion that the functions of specific brain areas are similar between REM and wake is provided by the observable enactment of experienced dream movement in the REM sleep behavior disorder (Schenck et al. 1993). Moreover, wake-like function of regional brain areas is preserved in many abnormal states such as focal motor activity during seizures (Adams et al. 1997) or the recruitment of visual association cortex during visual hallucinations (Ffytche et al. 1998; Silbersweig et al. 1995). In future sleep research, many of these limitations may be overcome by the finer temporal and spatial resolution offered by functional MRI (fMRI) imaging (e.g., Ellis et al. 1999; Huang-Hellinger et al. 1995; Ives et al. 1997; Sutton et al. 1996, 1997, 1998).

Our review of this new literature is undertaken with these shortcomings in mind. Three factors weighed heavily in our evaluation of these data: 1) their novelty and uniqueness in beginning to describe the role of forebrain subsystems; 2) the surprising concordance in the neuroimaging results which emerged from studies carried out simultaneously by three independent groups; and 3) the complementarity between the lesion and imaging studies which confer the value of a double dissociation on the validity of the inferences drawn.

2. PET Studies Indicating Regional Activation Differences Between REM Sleep and Waking

Two very recent and entirely independent PET studies confirm the importance of the pontine brain stem in REM sleep brain activation (Braun et al. 1997; Maquet et al. 1996). This is an important advance because it validates, for the first time, the experimental animal data on the critical and specific role of the pontine brain stem in REM sleep generation. At the same time these new studies also provide important new data for our understanding of dream synthesis by the forebrain. Instead of the global, regionally nonspecific picture of forebrain activation that has been suggested by EEG studies, all of these new imaging studies indicate a preferential activation of limbic and paralimbic regions of the forebrain in REM compared to waking (Braun et al. 1997, 1998; Maquet et al. 1996; Nofzinger et al. 1997). One implication of these discoveries is that dream emotion may be a primary shaper of dream plots rather than playing a secondary role in dream plot instigation.

a. The PET Imaging Findings of the Maquet Group

Maquet et al. (1996) used an H2150 positron source to study REM sleep activation in their subjects who were then awakened for the solicitation of dream reports. In addition to the pontine tegmentum, significant activation was seen in both amygdalae and the anterior cingulate cortex (Table 2). Significantly, despite the general deactivation in much of the parietal cortex, Maquet et al. (1996) reported activation of the right parietal operculum - a brain region thought to be important for spatial imagery construction, an important aspect of dream cognition. The authors interpreted their data in terms of the selective processing, in REM, of emotionally influenced memories (see also Braun et al. 1997; Maquet & Franck 1997).

b. The PET Imaging Findings of the Braun Group

In another H2150 PET study, Braun et al. (1997) largely replicated the Maquet group's findings of a consistent REM-related brainstem, limbic and paralimbic activation. In REM compared individually to delta NREM and to pre- and post-sleep waking (see Table 2), these authors showed relative activation of the pons, midbrain, anterior hypothalamus, hippocampus, caudate, and medial prefrontal, caudal orbital, anterior cingulate, parahippocampal and inferior temporal cortices (Braun et al. 1997). Based on their observations, the Braun group then offered the following speculations which are relevant to the neurology of dreaming:

1) Ascending reticular activation during REM as compared to waking may favor a more ventral cholinergic route leading from the brainstem to the basal forebrain over a more dorsal route via the thalamus.

2) Activation of the cerebellar vermis in REM may reflect input to this structure from the brainstem vestibular nuclei. We note that these nuclei also constitute an important potential source of neuronal activation causing the unique vestibular features of fictive movement in dreams (Hobson et al. 1997; Leslie & Ogilvie 1996; Sauvageau et al. 1998).

3) Noting both a particularly strong REM sleep-related activation of the basal ganglia and the known connectivity of these subcortical structures, Braun et al. suggest that the basal ganglia may play an important role in an ascending thalamocortical activation network. They suggest that this network extends successively from the brainstem to the intralaminar thalamic nuclei, then to the basal ganglia, and back to the ventral anterior and ventromedial thalamic nuclei, and thence to the cortex.

This network contains multiple regulatory back projections including interconnections between the pedunculopontine tegmentum and the striatum further suggesting a possible role for the basal ganglia in the rostral transmission of PGO waves and the modulation of REM sleep phenomena. The extensive interconnections of the basal ganglia and the pedunculopontine area have recently been reviewed by Rye (1997) and Inglis and Winn (1995). The role of the basal ganglia in the initiation of motor activity may, in turn, be related to the ubiquity of motion in dreams (Hobson 1988b; Porte & Hobson 1996).

4) The REM-associated increase in activation of unimodal associative visual (Brodmann areas 19 and 37) and auditory (Brodmann area 22) cortices contrasted with the maintained (NREM and REM) sleep-related deactivation of heteromodal association areas in the frontal and parietal cortex. Combined with findings of striate cortex deactivation in REM, this group (Braun et al. 1998) has subsequently theorized that, during REM, internal information is being processed between extrastriate and limbic cortices while they are functionally isolated from the external world both in terms of input (from the striate cortex) and output (via the frontal cortex).

5) The prominent decrease in the executive portions of the frontal cortex (dorsolateral and orbital prefrontal cortices) contrasts with the REM-associated increase in activation of the limbic associated medial prefrontal area. This medial area region has the most abundant limbic connections in the prefrontal cortex, has been associated with arousal and attention, and disruption of this area has been shown to cause confabulatory syndromes formally similar to dreaming. (Note also the dream-wake confusional syndrome associated with anterior limbic cortical lesions reported by Solms 1997.)

c. The PET Imaging Findings of the Nofzinger Group

Also confirming widespread limbic activation in REM sleep, Nofzinger et al. (1997) described increased glucose utilization in the lateral hypothalamic area and the amygdaloid complex using an 18F-fluoro-deoxyglucose (FDG) PET technique (Table 2). The largest area of activation was, in their own words, "...an extensive confluent area along the midline that includes the lateral hypothalamic area, septal area, ventral striatum-substantia innominata, infralimbic cortex, prelimbic and orbitofrontal and the anterior cingulate cortex...Much of this is bilateral." (p. 198). The authors suggest that an important function of REM sleep is the integration of neocortical function with basal forebrain and hypothalamic motivational and reward mechanisms.

3. Selective Deactivation of the Dorsolateral Prefrontal Cortex in REM Sleep

Relevant to the cognitive deficits in self-reflective awareness, orientation and memory during dreaming was the 15O2 PET finding of significant deactivation, in REM, of a vast area of dorsolateral prefrontal cortex (Braun et al. 1997; Maquet et al. 1996). A similar decrease in cerebral blood flow to frontal areas during REM had been previously noted by Madsen et al. (1991b) using SPECT. Dorsolateral prefrontal deactivation during REM, however, was not replicated by an FDG study (Nofzinger et al. 1997) and this discrepancy, therefore, remains to be clarified by other FDG as well as 15O2 studies. (A potential cause of this discrepancy arising from differences between FDG and 15O2 methods is discussed further on p. 98.)

Nevertheless, it seems likely that considerable portions of executive and association cortex active in waking may be far less active in REM leading Braun et al. (1997) to speculate that "...REM sleep may constitute a state of generalized brain activity with the specific exclusion of executive systems which normally participate in the highest order analysis and integration of neural information" (p. 1190).

Taken together, these results strongly suggest that the forebrain activation and synthesis processes underlying dreaming are very different from those of waking. Not only is REM sleep chemically biased but the preferential cholinergic neuromodulation is associated with selective activation of the subcortical and cortical limbic structures (which mediate emotion) and with relative inactivation of the frontal cortex (which mediates directed thought). These findings greatly enrich and inform the integrated picture of REM sleep dreaming as emotion-driven cognition with deficient memory, orientation, volition and analytic thinking.

The Maquet (Maquet et al. 1996; Maquet & Franck 1997), Nofzinger (Nofzinger et al. 1997) and Braun (Braun et al. 1997) groups all stress that their findings suggest assigning REM sleep a role in the processing of emotion (along with its cognitive and autonomic correlates) in memory systems via a limbic-cortical interplay. Additionally, PET researchers suggest the possible origin of dream emotionality in REM-associated limbic activation (Braun et al. 1997; Maquet & Franck 1997) and dream-associated executive deficiencies in REM-associated frontal deactivation (Braun et al. 1997; Maquet & Franck 1997). Although tantalizing correlations such as: 1) limbic activation and dream emotionality, 2) dream emotionality and affect congruent dream narratives, and 3) frontal deactivation and dream bizarreness, are now becoming apparent in the sleep and dream literature, the precise causal sequence among these phenomena remains to be established by future research.

Two additional findings support this proposed cortico-limbic interaction. First, the anterior cingulate cortex has consistently shown increased activation in REM in other PET studies (e.g., Buchsbaum et al. 1989; Hong et al. 1995; Bootzin et al. 1998). Second, recent studies of human limbic structures with depth electrodes during REM sleep have shown distinctive rhythmic EEG patterns possibly related to the REM-associated hippocampal theta rhythms seen in animals (Mann et al. 1997; Staba et al. 1998). Human frontal midline theta has also been detected using scalp electrodes (Inanaga 1998).

4. Global and Regional Decreases in Activation Level in NREM Sleep

Neuroimaging studies also strongly support a distinction between REM and NREM sleep as states whose differing neuroanatomical activation patterns predict their observed phenomenological differences (Table 2). PET studies of NREM sleep generally show a decrease in global cerebral energy metabolism (i.e., O2 or glucose utilization) relative to waking and REM (Buchsbaum et al. 1989; Heiss et al. 1985; Madsen & Vorstup 1991; Madsen et al. 1991a,b; Maquet 1995; Maquet et al. 1990, 1992, 1997). The magnitude of this decline relative to waking has varied from 11% glucose utilization in stage 2 (Maquet et al. 1992) to 40% glucose utilization in stages 3 and 4 (Maquet et al. 1990). A similar pattern has usually been reported for global cerebral blood flow as measured by 15O2 PET, SPECT, near infrared spectroscopy or a modification of the Kety-Schmidt O2 uptake technique (Braun et al. 1997; Hoshi et al. 1994; Madsen et al. 1991a,b; Maquet et al. 1997; Meyer et al. 1987; Sakai et al. 1980), although some studies have failed to show this global hemodynamic change (Andersson et al. 1995, 1998; Hofle et al. 1997). In addition, cerebral energy metabolism decreases with progressively greater depth of NREM sleep (Maquet 1995) a result recently replicated with fMRI (Sutton et al. 1997). By contrast, in REM, global cerebral energy metabolism tends to be equal to (Asenbaum et al. 1995; Braun et al. 1997; Madsen et al. 1991a; Maquet et al. 1990) or greater than (Buchsbaum, et al. 1989; Heiss et al. 1985) that of waking. Cerebral blood flow velocity measured in the middle cerebral artery similarly shows a slowing during NREM followed by values similar to waking during REM (Droste et al. 1993; Haiak et al. 1994; Klingelhofer et al. 1995; Kuboyama et al. 1997).

More striking than global patterns are the now well-replicated regional variations in cerebral energy metabolism over the wake-NREM-REM sleep cycle (Table 2). Earlier studies showing specific declines in thalamic glucose utilization in NREM relative to waking (Buchsbaum et al. 1989; Maquet et al. 1990, 1992) have been confirmed by recent oxygen utilization studies (Andersson et al., 1998; Braun et al. 1997; Hofle et al. 1997; Maquet et al. 1997). In addition to prominent thalamic deactivation, all three recent studies have found regional deactivation during NREM in the pontine brain stem, orbitofrontal cortex and anterior cingulate cortex (Braun et al. 1997; Hofle et al. 1997; Maquet et al. 1997). NREM deactivation of lateral prefrontal cortex was also observed in some studies (Andersson et al., 1998; Braun et al. 1997). Thalamic activation was found to decline significantly concomitant with increased delta EEG activity and there was an additional decline associated with increased spindle-frequency activity when the decrements associated with delta were subtracted (Hofle et al. 1997).

Hofle et al. (1997) and Maquet et al. (1997) both interpret this pattern of decline as reflecting the progressive deactivation of the reticular activating system (RAS) which accompanies deepening NREM sleep. This deactivation leads to dysfacilitation of thalamocortical relay neurons which allows the emergence of underlying thalamocortical oscillatory rhythms (Steriade & McCarley 1990; Steriade et al. 1993a-d, 1994). GABAergic neurons of the thalamic reticular nucleus then further hyperpolarize and dysfacilitate thalamic relay neurons as NREM deepens (Steriade et al. 1994). In this hyperpolarized condition, thalamic neurons become constrained to burst firing patterns first in spindle (12-14 Hz) and later in delta (1-4 Hz) frequencies as NREM deepens from Stage 2 to delta sleep (Steriade et al. 1993c,d). The cortex may further constrain these spindle and delta-wave-generating thalamocortical bursts within a newly described slow (<1 Hz) oscillation seen in cats (Steriade et al. 1993a-d) and humans (Achermann & Borbely 1997). In conclusion, the metabolic decline seen during NREM is centered on the central core structures (brain stem, thalamus) which are known to play a role in generation of the slow oscillations of NREM sleep (Maquet et al. 1997).

The regional pattern of deactivation in NREM, therefore, sharply contrasts with the regional activation of these same regions (i.e., thalamus, pontine brain stem, anterior cingulate cortex) in REM (Braun et al. 1997; Maquet et al. 1996; Nofzinger et al. 1997). Details of these stage-related differences are shown in Table 2. Note that a recent cat study has shown a similar pattern of brain glucose metabolism in REM (Lydic et al. 1991b).

5. Interpreting the PET Imaging Results with Respect to the Psychophysiology of Dreaming

According to PET researchers, regional activation during REM may reflect a specific activation of subcortical and cortical arousal and limbic structures for the adaptive processing of emotional and motivational learning (Maquet et al. 1996; Nofzinger et al. 1997). Such processing may, in turn, account for the emotionality and psychological salience of REM dreaming (Braun et al. 1997). Some support for this comes from a PET (glucose) study showing correlation between content-analyzed dream anxiety and medial frontal activation (Gottschalk et al. 1991).

In summary, the markedly differing physiology of wake, NREM and REM cerebral activation should be reflected in the respective phenomenology of mentation reported from these three conscious states. More particularly, the specific phenomenology of REM mentation may reflect the neurobiologically specific brain activation pattern. Nofzinger et al. (1997) conclude that "...the current findings of increased limbic and paralimbic activation during REM sleep...as well as global, regionally non-selective cortical deactivation and decreased metabolism during NREM sleep, are generally supportive of the traditional notion that more story-like affect-laden dreams are more attributable to the REM sleep, than NREM sleep behavioral state" (p. 199).

6. Brain Lesions Resulting in Loss or Alteration of Dreaming

a. Solms' New Nosology for Lesion-Related Disorders of Dreaming

A set of findings and conclusions which have proved remarkably complementary to the neuroimaging results have been reached following a neuropsychological survey of 332 clinical cases of cerebral lesions as well as a review of 73 extant publications on the dreaming-related sequelae of cerebral injury (Solms 1997). Using these welcome and long overdue neuropsychological data, Solms proposes a new nosology for the brain-lesion related disorders of dreaming.

In one syndrome, "global anoneria," total cessation of dreaming in patients (whose normal waking vision is preserved) results from either posterior cortical or deep bilateral frontal lesions. The posterior global anoneria syndrome results from lesions of the inferior parietal lobes in either hemisphere, with lesions to Brodmann's areas 39 and 40 being the most restricted damage sufficient to produce the syndrome. The anterior variant of global anoneria results from deep medial frontal damage resulting in the disconnection of the mediobasal frontal cortex from the brain stem and diencephalic limbic regions. In this syndrome, bilateral damage to white matter in the vicinity of the frontal horns of the lateral ventricles was the most restricted site causing the syndrome.

In a second syndrome, "visual anoneria," bilateral medial occipito-temporal lesions produce full or partial loss of dream visual imagery (again with normal waking vision). Among his own patients, a decrease in the "vivacity" of dreaming was reported by two patients with damage to the seat of normal vision in the medial-occipital-temporal cortex (especially areas V3, V3a and V4 but not V1, V5 or V6). Notably, a correlate of visual anoneria was visual irreminiscence, the inability to produce mental imagery in waking. In addition, partial variants of visual anoneria exist which involve selective loss of particular visual elements (e.g., "kinematic anoneria" or "facial anoneria").

In addition to these two disorders of attenuated dreaming, Solms reported another interrelated pair of symptom complexes which combined increased frequency and intensity of dreaming. He suggested that increased vivacity and frequency of dreaming was associated with anterior limbic lesions while recurring nightmares are associated with temporal seizures.

b. Double Dissociations Suggested by PET and Lesion Findings

We believe that these findings map particularly well onto the neuroimaging findings on REM. For example, extrastriate visual cortex is activated during REM (Braun et al. 1997, 1998) and lesions to this region produce the distinctive dream deficits of full or partial visual anoneria (Solms 1997). In contrast, the striate visual cortex is deactivated during REM (Braun et al. 1998) while lesions to this region do not affect dreaming (Solms 1997). Similarly, the seat of spatial cognition in the inferior parietal cortex (BA 40) is activated in the right (but not the left) hemisphere during REM (Maquet et al. 1996) while damage to this region, especially on the right, is sufficient to produce global anoneria (Solms 1997). Moreover, much of the lateral prefrontal area is both deactivated during REM (Braun et al. 1997; Maquet et al. 1996) while lesions to this region do not affect dreaming (Dorricchi and Violani 1992; Solms 1997).

Two exceptions to this general correspondence involve lesions of the brainstem (for which Solms reports no attenuation of dreaming) and lesions of the rostral limbic system (for which Solms reports an accentuation of dreaming). In the case of pontine lesions, we suggest that any lesion capable of destroying the pontine REM sleep generator mechanism would have to be so extensive as to eliminate consciousness altogether. We base this caveat upon the difficulty of suppressing REM by experimental lesions of the pons in animals. In the case of the rostral limbic system, we caution that lesions there could as well be irritative as destructive and that lesions in different areas of this functionally highly heterogeneous region (Devinsky et al. 1995) could produce dramatically different effects.

B. Reciprocal Interaction: A Neurobiological Update

The discovery of the ubiquity of REM sleep in mammals provided the brain side of the brain-mind state question with an animal model (Dallaire et al. 1974; Dement 1958; Jouvet & Michel 1959; Jouvet 1962, 1999; Snyder 1966). While animal studies showed that potent and widespread activation of the brain did occur in REM sleep, it soon became clear that Moruzzi and Magoun's concept of a brain stem reticular activating system (Moruzzi & Magoun 1949) required extension and modification to account for the differences between the behavioral and subjective concomitants of waking and those of REM sleep (see Hobson & Brazier 1981).

1. Implications for Dream Theory

We take the theoretical position that it is the cellular and molecular level brain events to be discussed that bias the brain to produce the conscious state differences that contrast waking, NREM and REM sleep. As we will point out in detail in Part IV when we develop the AIM model, the shift from aminergic dominance in waking to cholinergic dominance in REM lowers the probability that consciousness will be exteroreceptive, logical and mnemonic while correspondingly raising the probability that consciousness will be interoceptive, illogical and amnesic.

2. Behavioral State-Dependent Variations in Neuromodulation

A conceptual breakthrough was made possible by the discovery of the chemically specific neuromodulatory subsystems of the brain stem (e.g., Dahlstrom & Fuxe 1964; for reviews see Foote et al. 1983; Gottesmann, 1999; Hobson & Steriade 1986; Hobson et al. 1998; Jacobs & Azmita 1992; Lydic & Baghdoyan 1999; Mallick & Inoue, 1999; Rye 1997; Steriade & McCarley 1990) and of their differential activity in waking (noradrenergic and serotonergic systems on, cholinergic system damped) and REM sleep (noradrenergic and serotonergic systems off, cholinergic system undamped) (Aston-Jones & Bloom 1981; Cespuglio et al. 1981; Chu & Bloom 1973, 1974; Hobson et al. 1975; Jacobs 1986; Lydic et al. 1983, 1987; McCarley & Hobson 1975; McGinty & Harper 1976; Rasmussen et al. 1986; Reiner 1986; Steriade & McCarley 1990; Trulson & Jacobs 1979).

a. The Original Reciprocal Interaction Model: An Aminergic-Cholinergic Interplay

The model of reciprocal interaction (McCarley & Hobson 1975) provided a theoretical framework for experimental interventions at the cellular and molecular level that has vindicated the notion that waking and dreaming are at opposite ends of an aminergic-cholinergic neuromodulatory continuum, with NREM sleep holding an intermediate position (Figure 3). The reciprocal interaction hypothesis (McCarley & Hobson 1975) provided a description of the aminergic-cholinergic interplay at the synaptic level and a mathematical analysis of the dynamics of the neurobiological control system (Figure 2, 3A). In this section we review subsequent work that has led to the alteration (Figure 3B) and elaboration (Figure 4) of the model.

Although there is abundant evidence for a pontine peribrachial cholinergic mechanism of REM generation centered in the pedunculopontine (PPT) and laterodorsal tegmental (LDT) nuclei (for recent reviews see Datta 1995, 1997b, 1999; Hobson 1992b; Hobson et al. 1993; Lydic and Baghdoyan 1999; Rye 1997), not all pontine PPT and LDT neurons are cholinergic (Kamodi et al. 1992; Kang & Kitai 1990; Leonard & Llinas 1990, 1994; Sakai & Koyama 1996; Steriade et al. 1988) and cortical acetylcholine release may be as high during wakefulness as during sleep (e.g., Jasper & Tessier 1971; Jimenez-Capdeville & Dykes 1996; Marrosu et al. 1995).

Recently, reciprocal interaction (McCarley & Hobson 1975) and reciprocal inhibition (Sakai 1988) models for control of the REM sleep cycle by brain stem cholinergic and aminergic neurons have been questioned (Leonard & Llinas 1994). Specifically, the self-stimulatory role of acetylcholine on pontine PGO-bursting neurons has not been confirmed in in vitro slice preparations (Leonard & Llinas 1994). For example, ACh has been shown to hyperpolarize cell membranes in slice preparations of the rodent parabrachial nucleus (Egan & North 1986a), LDT (Luebke et al. 1993; Leonard & Llinas 1994), and PPT (Leonard & Llinas 1994). Similarly, LDT and PPT neurons with burst discharge properties most like those hypothesized to occur in PGO-burst neurons ("type I" neurons) may not be cholinergic (Leonard & Llinas 1990). Much evidence remains, however, that the reciprocal interaction model accurately describes essential elements of REM sleep cycle control even though some of its detailed synaptic assumptions need correction (Figure 3B).

b. New Findings Supporting the Cholinergic Enhancement of REM Sleep

Numerous findings confirm the hypothesis that cholinergic mechanisms are essential to the generation of REM sleep and its physiological signs (for recent reviews see Capece et al. 1999; Datta 1995, 1997b,1999; Gottesmann 1999; Hobson 1992b; Hobson et al. 1986, 1993; Hobson & Steriade 1986; Lydic & Baghdoyan 1999; Jones 1991, 1998; Mallick & Inoue 1999; McCarley et al. 1995, 1997; Rye 1997; Sakai 1988; Steriade & McCarley 1990). A selection of the many recent examples is as follows:

1) Microinjection of cholinergic agonist or cholinesterase inhibitor into many areas of the paramedian pontine reticular formation induces REM sleep (Baghdoyan et al. 1987, 1989; Hobson et al. 1993; Vanni-Mercier et al. 1989; Velazquez-Moctezuma et al. 1989, 1991; Yamamoto et al. 1990a,b). In addition to these short term REM induction sites, carbachol injection into a pontine site in the caudal peribrachial area has been shown to induce long-term (over 7 days) REM enhancement (Calvo et al. 1992; Datta et al. 1992, 1993).

2) Cholinergic (type II and III) PPT and LDT neurons have firing properties which make them well suited for the tonic maintenance of REM (Leonard & Llinas 1990).

3) PGO input to the LGB is cholinergic (Steriade et al. 1988) and can be antidromically traced to pontine PGO-burst neurons (Sakai & Jouvet 1980) and retrograde tracers injected into the thalamus label 50% or more of cholinergic PPT/LDT neurons (Oakman et al. 1999; Rye 1997). Moreover, stimulation of mesopontine neurons induces depolarization of cortically projecting thalamic neurons (Curro-Dossi et al. 1991).

4) PGO waves can be blocked by cholinergic antagonists (Hu et al. 1988) and neurotoxic lesions of pontomesencephalic cholinergic neurons reduces the rate of PGO spiking (Webster & Jones 1988).

5) PPT and LDT neurons show specifically c-fos and fos-like immunoreactivity following carbachol-induced REM sleep (Shiromani et al. 1995, 1996)

6) Low amplitude electrical stimulation of the LDT enhances subsequent REM sleep (Thakkar et al. 1996).

7) Electrical stimulation of the cholinergic LDT evokes excitatory post synaptic potentials (EPSPs) in pontine reticular formation neurons which can be blocked by scopolamine (Imon et al. 1996).

8) The excitatory amino acid, glutamate, when microinjected into the PPT dose-dependently increases REM sleep (Datta 1997a; Datta & Siwek 1997).

9) Microdialysis studies showed enhanced release of endogenous acetylcholine in the medial pontine reticular formation during natural (Kodama et al. 1990) and carbachol-induced (Lydic et al. 1991a) REM sleep.

10) Thalamic ACh concentration of mesopontine origin is higher in wake and REM than in NREM (Williams et al. 1994), a REM-specific increase of ACh in the lateral geniculate body has been observed (Kodama & Honda 1996), and both muscarinic and nicotinic receptors participate in the depolarization of thalamic nuclei by the cholinergic brainstem (Curro-Dossi et al. 1991).

11) Although in vivo cholinergic REM enhancement has been difficult to demonstrate in rats (Deurveiller et al. 1997), such enhancement has recently been reported (Datta et al. 1998; Marks & Birabil 1998) and a specific carbachol-sensitive site in the dorsal locus subcoeruleus of rats has recently been described (Datta et al. 1998). Moreover, rats which are genetically supersensitive to ACh show enhanced REM sleep (Benca et al. 1996)

12) The new presynaptic anticholinergic agents have been shown to block REM (Salin-Pascual et al. 1995; Capece et al. 1997).

13) Muscarinic activation by carbachol has been shown to increase G-protein binding in brainstem nuclei associated with REM sleep (Capece et al. 1998).

14) Cholinergic PPT neurons have now been quantitatively mapped in the human pontine brainstem (Manaye et al. 1999).

It may not be an exaggeration to state that the evidence for cholinergic REM sleep generation is now so overwhelming and so widely accepted that this tenet of the reciprocal interaction model is an established principle.

c. New Findings Supporting the Serotonergic and Noradrenergic Suppression of REM Sleep

But what about the essence of the theory: the idea that cholinergic REM sleep generation can only occur when the noradrenergic and serotonergic mediators of waking release their inhibitory constraint? The evidence for inhibitory serotonergic and noradrenergic influences on cholinergic neurons and REM sleep is now also quite strong. For example:

1) Serotonergic neurons have been shown to project to the LDT and PPT (Honda & Semba 1994; Steininger et al. 1997) and serotonin has been shown to hyperpolarize rat cholinergic LDT cells in vitro (Luebke et al. 1992a; Leonard & Llinas 1994) and to reduce REM sleep percent in vivo (Horner et al. 1997).

2) Serotonin has been shown to counteract the REM-like carbachol-induced atonia of hypoglossal motoneurons (Kubin et al. 1994, 1996; Okabe & Kubin 1997).

3) In the cat, extracellular levels of serotonin are higher in waking than in NREM and higher in NREM than REM in the hypothalamus (Auerbach et al. 1989; Imeri et al. 1994), dorsal raphe (Portas et al. 1998) and frontal cortex (Portas et al. 1998) of rats as well as the dorsal raphe (Portas & McCarley 1994) and medial pontine reticular formation (Iwakiri et al. 1993) of cats. And, this same pattern of extracellular serotonin concentration change over the sleep-wake cycle has recently been demonstrated in the human amygdala, hippocampus, orbitofrontal cortex and cingulate cortex (Wilson et al. 1997).

4) Microinjection of the serotonin agonist 8-OH-DPAT into the peribrachial region impeded REM initiation in cats (Sanford et al. 1994) and systemic injection of 8-OH-DPAT into serotonin-depleted rats also suppressed REM (Monti et al. 1994). However, localization of the serotonergic REM suppressive effect to the PPT/LDT has recently been challenged in favor of an amygdalar-pontine interaction (Sanford et al. 1996, 1998b; Morrison et al. 1999).

5) Microinjection with simultaneous unit recording has shown that microinjection of 8-OH-DPAT suppresses the firing of REM-on but not REM-and-Wake-on cells of the cholinergic LDT and PPT (Thakkar et al. 1997, 1998).

6) In-vivo microdialysis of serotonin agonists into the dorsal raphe nucleus (DRN) decreased DRN levels of serotonin (presumably via serotonin autoreceptors on DRN cells) which in turn increased REM sleep percent (Portas et al. 1996; Thakkar et al., 1998).

7) Electrical stimulation of the pons in the vicinity of the (noradrenergic) locus coeruleus reduced REM sleep in rats (Singh & Mallick 1996) and locus coeruleus neurons have been shown to become quiescent during REM in the monkey (Rajkowski et al. 1997).

8) The alpha-2 noradrenergic agonist clonidine suppresses REM in human subjects (Gentili et al. 1996; Nicholson & Pascoe 1991) and the cat (Tononi et al. 1991) while the noradrenergic antagonist idazoxan increases REM when injected into the pontine reticular formation of cats (Bier & McCarley 1994).

9) There is near universal suppression of REM sleep in humans by acute dosage of serotonin and norepinephrine reuptake-inhibiting antidepressants (Gaillard et al. 1994; Nicholson et al. 1989; Vogel 1975; Vogel et al. 1990).

10) Mesopontine injection of a serotonin agonist depressed ACh release in the lateral geniculate body (Kodama & Honda 1996).

It can therefore also be stated that aminergic suppression of REM sleep is now an established principle (for recent reviews see Monti & Monti 1999 and Luppi et al. 1999a,b).

d. Modification of the Original Reciprocal Interaction Hypothesis to Accommodate New Findings

Modifications of simple reciprocal inhibition or interaction models, which are consonant with recent