We discuss the relationship between sleep, dreams, and memory, proposing that the content of dreams reflects aspects of memory consolidation taking place during the different stages of sleep. Although we acknowledge the likely involvement of various neuromodulators in these phenomena, we focus on the hormone cortisol, which is known to exert influence on many of the brain systems involved in memory. The concentration of cortisol escalates over the course of the night's sleep, in ways that we propose can help explain the changing nature of dreams across the sleep cycle.
There is currently no convincing explanation for why we dream or what we dream about. In this article we propose an approach to dreaming that focuses on the relationship between sleep and memory. We suggest that dreams reflect a biological process of long-term memory consolidation, serving to strengthen the neural traces of recent events, to integrate these new traces with older memories and previously stored knowledge, and to maintain the stability of existing memory representations in the face of subsequent experience (Winson 1985, 2002, 2004; Kali and Dayan 2004).
It is generally assumed that long-term memory consolidation involves interactions among multiple brain systems, modulated by various neurotransmitters and neurohormones. We propose that the characteristics of dreams are best understood in the context of this neuromodulatory impact on the brain systems involved in memory consolidation. Although a number of neurotransmitters and neurohormones are likely involved, we focus our attention in particular on the stress hormone cortisol, which has widespread effects on memory during waking life through its impact on many of the critical brain structures implicated in memory function.
Our hypothesis, briefly stated, is that variations in cortisol (and other neurotransmitters) determine the functional status of hippocampal ↔ neocortical circuits, thereby influencing the memory consolidation processes that transpire during sleep. The status of these circuits largely determines the phenomenology of dreams, providing an explanation for why we dream and of what. As a corollary, dreams can be thought of as windows onto the inner workings of our memory systems, at least those of which we can become conscious.
In addition to exploring these ideas in more detail, we provide some background concerning (1) the states of sleep and the role of various neurotransmitters in switching from one sleep state to another, (2) how the characteristics of dreams vary as a function of sleep state, (3) the memory content typically associated with dreaming in different dream states, and (4) the role of sleep in the consolidation of memory.
Background to the hypothesis
Stages of sleep
There are two major types of sleep. The first, rapid eye movement or REM sleep, occurs in ∼90-min cycles and alternates with four additional stages known collectively as NREM sleep—the second type of sleep. Slow wave sleep (SWS) is the deepest of the NREM phases and is the phase from which people have the most difficulty being awakened. REM sleep is characterized by low-amplitude, fast electroencephalographic (EEG) oscillations, rapid eye movements (Aserinsky and Kleitman 1953), and decreased muscle tone, whereas SWS is characterized by large-amplitude, low-frequency EEG oscillations (Maquet 2001). More than 80% of SWS is concentrated in the first half of the typical 8-h night, whereas the second half of the night contains roughly twice as much REM sleep as does the first half. This domination of early sleep by SWS, and of late sleep by REM, likely has important functional consequences but also makes it difficult at this time to know which distinction is critical: NREM sleep versus REM sleep or early sleep versus late sleep. We will use the terms NREM/early sleep and REM/late sleep, where necessary, to reflect this current ambiguity.
Neurotransmitters, particularly the monoamines (largely serotonin [5-HT] and norepinephrine [NE]) and acetylcholine, play a critical role in switching the brain from one sleep stage to another. REM sleep occurs when activity in the aminergic system has decreased enough to allow the reticular system to escape its inhibitory influence (Hobson et al. 1975, 1998). The release from aminergic inhibition stimulates cholinergic reticular neurons in the brainstem and switches the sleeping brain into the highly active REM state, in which acetylcholine levels are as high as in the waking state. 5-HT and NE, on the other hand, are virtually absent during REM. SWS, conversely, is associated with an absence of acetylcholine and nearly normal levels of 5-HT and NE (Hobson and Pace-Schott 2002).
The distribution of dreams
In the study of dreams, a major distinction has been drawn between REM and NREM sleep. Until recently, virtually all dream research focused on REM sleep, and indeed, dreams are prevalent during REM. In a recent review of 29 REM and 33 NREM recall studies, Nielsen (2000) reported an average REM dream recall rate of 81.8%. Importantly, however, he also reported an average NREM recall rate of ∼50%. Some NREM dreams are similar in content to REM dreams; the majority of these come from those few NREM periods occurring early in the morning, during the peak phase of the diurnal rhythm, when cortisol levels are at their zenith (Kondo et al. 1989). Foulkes (1985) has argued for the existence of NREM dreaming and against a simple “REM sleep = dreaming” view. By simply changing the question asked of awakened subjects from “Did you dream?” to “Did you experience any mental content?,” Foulkes was able to show a far higher percentage of dream reports from NREM stages than original studies had suggested. These dream reports after NREM awakenings led Foulkes and others to conclude that the stream of consciousness never ceases during sleep and that the brain engages in cognitive activity of some sort during all sleep stages (Antrobus 1990).
Dreams and episodic memory content
Typical REM and NREM dreams are quite distinct, particularly with respect to episodic memory content. Episodic memory refers to knowledge about the past that incorporates information about where and when particular events occurred. It is typically contrasted with semantic memory, which consists of knowledge (e.g., facts, word meanings) that has been uncoupled from place and time, existing on its own (Tulving 1983). When examining REM sleep dreams for memory content, one finds that episodic memories are rare (see Baylor and Cavallero 2001) and typically emerge as disconnected fragments that are often difficult to relate to waking life events (see Schwartz 2003). These fragmented REM dreams often have bizarre content (Stickgold et al. 2001; Hobson 2002). For example, the normal rules of space and time can be ignored or disobeyed, so that in REM dreams it is possible to walk through walls, fly, interact with an entirely unknown person as if she was your mother, or stroll through Paris past the Empire State Building. NREM dreams, however, are quite different (Cavallero et al. 1992). Here, episodic memories do appear in dream content (see Foulkes 1962; Cicogna et al. 1986, 1991; Cavallero et al. 1992; Baylor and Cavallero 2001). Recent episodes are predominant, but remote memories occasionally appear as well. This pattern of results suggests to us that the memory systems needed to generate complete episodic retrieval are functional in NREM sleep but not in REM sleep. Although we do not fully understand how nightly neurochemical fluctuations account for this difference, some clues are available.
Sleep and memory consolidation
One important clue is that different types of memory (e.g., procedural, episodic) appear to be best consolidated during specific stages of sleep. REM sleep may be preferentially important for the consolidation of procedural memories and some types of emotional information (see Karni et al. 1994; Plihal and Born 1999a; Kuriyama et al. 2004; Smith et al. 2004), whereas NREM, especially SWS, appears to be critical for explicit, episodic memory consolidation (Plihal and Born 1997, 1999a,b; Rubin et al. 1999; also see Peigneux et al. 2001). This role for SWS appears to apply both to verbal tasks (e.g., list learning, paired-associated learning tasks; Plihal and Born 1997) and spatial tasks (e.g., spatial rotation; Plihal and Born 1999a). For example, Plihal and Born (1997) tested both episodic and procedural memory after retention intervals defined over early sleep (dominated by SWS) and late sleep (dominated by REM). Subjects were trained to criterion in the recall of a paired-associate word list (episodic) and a mirror-tracing task (procedural) and were retested after 3-h retention intervals, during either early or late nocturnal sleep. Recall of paired associates improved significantly more after a 3-h sleep period rich in SWS than after a 3-h sleep period rich in REM or after a 3-h period of wake. Mirror tracing, on the other hand, improved significantly more after a 3-h sleep period rich in REM than after 3 h spent either in SWS or awake. The fact that memories for personal episodes only undergo effective consolidation early in the night, when NREM (SWS) is particularly prominent, provides another indication that episodic memory systems are functional during NREM sleep.
Summary of background
This brief review highlights several points:
Sleep stages vary across the night: Early sleep is rich in NREM, but late sleep is rich in REM. These stage changes relate to, and are caused by, neurochemical fluctuations during sleep.
Dream content varies as a function of sleep stage or time of night: There is considerable episodic content in dreams during NREM/early sleep, but little episodic content in dreams during REM/late sleep.
Sleep affects memory consolidation, but in a complex way: Procedural memory benefits from both REM/late sleep and NREM/early sleep, but episodic memory only benefits from NREM/early sleep.
These points raise two critical questions:
What can account for the differences in dream content and effectiveness of memory consolidation as an apparent function of NREM/early sleep versus REM/late sleep?
What underlying concomitants of this difference actually produce the variations in dream content and memory consolidation?
Are neurotransmitters the key, as some have suggested (see Hobson 1988)? Is it strictly the REM/NREM distinction, or alternatively, could it be fundamental differences in early versus late sleep? It is important to note that Plihal and Born's studies (1997, 1999a) used late versus early sleep as the manipulation, not REM versus NREM per se. Moreover, late night NREM dreams are more “dream-like” and are thus often indistinguishable from REM dreams (Kondo et al. 1989), so perhaps something about late night sleep accounts for differences in dream content and memory consolidation. These are just some of the issues that arise within the framework we propose.
Comments