Memory is not regarded as a unitary cognitive function but as the interaction of several systems. In humans, we can now go beyond the classic declarative versus non-declarative memory dichotomy and differentiate between these memory systems more accurately. Thus, according to Tulving (1995), human memory encompasses a short-term memory system (or working memory) and four systems of long-term memory: procedural memory, the perceptual representation system, semantic memory and episodic memory. Procedural memory can be defined as a system dedicated to the encoding, storage and retrieval of the procedures subtending perceptual-motor, perceptual-verbal and cognitive skills (Cohen and Squire, 1980). The perceptual representation system is involved in non-conscious expressions of memory, particularly priming effects (Tulving and Schacter, 1990). Procedural memory and priming effects are commonly designated as non-declarative (or implicit) memory, while the concept of declarative memory refers to semantic and episodic memory. Semantic memory encompasses knowledge about the world regardless of the spatio-temporal context of acquisition (I know that Rome is the capital of Italy, but I cannot say where and when I learned this fact). Semantic memory is characterized by a noetic awareness of the existence of the world, objects and events that also reflects a feeling of familiarity. Lastly, episodic memory refers to a system that stores events located in time and space (I remember our visit to the royal palace in Prague last Saturday). Episodic memory is characterized by autonoetic consciousness, which gives a subject the conscious sensation of travelling back in time to relive the original event and thus provides a means of linking events in the past, present and future (Tulving, 2001, 2002). Autonoetic consciousness enables us to recollect vivid spatio-temporal and phenomenological details of the event.
In Tulving's model, information is encoded into systems serially, that is, the registration of information in one system is contingent on the successful processing in another system. For example, this model predicts that encoding in semantic memory can be efficient even if encoding processes in episodic memory are deficient, but not the reverse situation. Storage is parallel in the different systems and information from each system can be retrieved independently of information in other systems. Tulving's SPI model is the one that prevails in the neuropsychology of human memory, bearing in mind that memory is a dynamic process based on the interaction between the different systems.
Before getting to the heart of the matter, we first need to discuss a methodological issue raised by the studies relating sleep to memory. Numerous studies in this field have used sleep deprivation paradigms, where deprivation may either be total, selective of a given sleep stage or partial (of the first or second half of the night). Researchers first performed selective deprivation, in particular of REM sleep. The results obtained using this methodology must be viewed with some caution. Indeed, the numerous arousals needed to bring about selective deprivation may split sleep up and induce modifications of sleep patterns, emotional and attentional disorders, stress, a reduction in motivation and disturbances in biological rhythms (Cipolli, 1995; Horne and McGrath, 1984). These non-specific disturbances could affect behavioural performance and mask the real effects of sleep deprivation (Born and Gais, 2000). Stress response is often put forward to explain memory impairment after sleep deprivation. Indeed, corticotrophin-releasing hormone is a major component of the stress response and it has been shown that changes in the concentration of corticosteroids can affect consolidation (Plihal and Born, 1999b). The partial sleep deprivation paradigm could reduce these non-specific effects, as sleep is uninterrupted during the first or second half of the night. In this sense, this method is probably less disturbing than selective deprivation. However, this technique also has its drawbacks, as it means that part of the night is missed, resulting in a compensatory need for the lacking sleep stage. Hence, the results from sleep deprivation studies should be taken cautiously and confirmed by findings obtained using different paradigms.
Sleep and perceptual representation system
The assessment of the perceptual representation system relies on the demonstration of the existence of perceptual priming effects. Priming refers to facilitative changes in the ability to identify, generate or process an item due to a prior encounter with this item or a similar stimulus (Tulving and Schacter, 1990). Priming does not require conscious or explicit recollection of the prior encounter with the item and, in this respect, is regarded, as a form of implicit (or non-declarative) memory (Graf and Schacter, 1985). Priming and procedural memory are therefore both expressions of implicit memory, but they differ in the nature of the stored representations and their neural substrates. In tasks assessing perceptual priming, stored information corresponds to items (i.e. drawings, words) presented only once, whereas procedural memory involves the storage of procedures acquired over several training sessions. In addition, priming and procedural memory refer to different memory systems, as attested by neuropsychological dissociations, particularly in subcortical dementias, and are subserved by different brain areas, as evidenced by neuroimaging studies (subcortical areas such as the striatum for procedural memory (see for example Hikosaka et al., 1998) versus neocortical areas for priming (see for example Buckner et al., 1995). In the light of these differences, these systems could well be differentially affected by sleep.
Studies assessing the effects of sleep on priming are relatively scarce. Plihal and Born (1999a) used a wordstem completion task to assess the effects of a partial sleep deprivation on implicit memory. The use of this completion task is always controversial, as it does not specifically assess the perceptual representation system. In an initial, study phase, subjects were shown a word list and instructed to rate the nouns according to their melodious sounds. This instruction was considered to induce an incidental encoding of the items. After a distraction task, subjects were invited to complete a list of wordstems with the first noun that came into their head. Priming was attested by an increased percentage for the completion of previously-seen words, compared with novel ones. After a 3-h interval, during the first or second half of the night and filled with either sleep or wakefulness, the authors administered the completion task again, using wordstems derived from the remaining words in the initial list and the same number of items derived from a novel list. Priming effects were greater after late sleep than after early sleep. In other words, subjects who had slept during the second half of the night gave significantly more items belonging to the initial list than those who had slept during the first half. Hence, REM sleep appears to enhance the consolidation of implicit information.
Using the same partial sleep deprivation paradigm, Wagner et al. (2003) investigated the impact of nocturnal sleep on implicit memories for unknown faces. During the study phase, subjects had to indicate the gender of the individuals as quickly as possible, by pressing keys. During the test phase, they were instructed to indicate the gaze direction of the faces. Priming would normally correspond to shorter reaction times for the previously-seen faces than for new ones. Surprisingly, in subjects who had slept during the second half of the night, the authors observed longer reaction times for previously-encountered faces, which they termed an inverse priming effect. According to Wagner and his colleagues, this inverse priming effect reflected a facilitated identification of previously-encountered faces after REM sleep, thereby producing interference with the response generation during the test phase which required subjects not to identify faces but to determine the direction of their gaze. This explanation was confirmed by a complementary experiment in which subjects were required, in the study phase, to indicate gender and then, in the test phase, to decide whether a face was familiar or not. In this second study, no interference was found and priming effects were stronger (i.e. shorter mean reaction time for previously-encountered faces) when the retention interval was dominated by REM sleep (late night sleep).
These studies assessing the effects of sleep stages on priming effects have provided concordant results in favour of a beneficial role for REM sleep on the consolidation of implicit information. These results nevertheless have to be confirmed, taking care to design tasks that only involve implicit processes.
Sleep and semantic memory
Relationships between sleep and the consolidation of semantic information have seldom been investigated. Nonetheless, one series of studies has shown that semantic processing may occur during certain sleep stages. During wakefulness and different sleep stages, Brualla et al. (1998) recorded electrophysiological responses (event-related potentials) to the presentation of words, some semantically associated, others not. During the waking state, the presentation of words elicited a N400 response (an electrophysiological marker of semantic discordance) which was greater in magnitude for words that were semantically unrelated to the preceding word than for items that were semantically associated. This decrease in the N400 response for semantically associated words reflected semantic priming. These priming effects were observed when items were presented during stage 2 sleep or REM sleep, but not during SWS. In a similar vein, Perrin et al. (1999) recorded auditory evoked potentials to the subject's own name and to other first names during wakefulness, stage 2 sleep and REM sleep. These authors underlined that a differential response to the subject's own name, comparable with that observed during wakefulness, was elicited during stage 2 and REM sleep. These results suggest that the brain retains the ability to identify a pertinent stimulus among others during these sleep stages.
Stickgold et al. (1999) also explored semantic priming effects using a lexical decision task. This task is classically used to assess implicitly semantic memory but, in this study, the authors sought to investigate the impact of the subjects’ cognitive state when awakening (after a stage 2 NREM sleep or a REM sleep episode) on the strength of associative links between pairs of items. To this end, the task was administered to subjects four times: once prior to bedtime, twice immediately after awakening from stage 2 NREM sleep and REM sleep respectively, and 5 min after waking up in the morning. This task featured lists of prime-target pairs comprising unrelated, weakly related or strongly associated words, as well as word/non-word pairs. For each list, subjects were required to decide, as quickly as possible, if the second word of the pair (i.e. the target) was a word or a non-word. Priming was attested by shorter reaction times for items that were preceded by a semantically linked prime, than for weakly related ones. Subjects waking up from NREM sleep (stage 2) displayed priming effects whereas subjects waking up from REM sleep presented different responses i.e. shorter reaction times for weakly associated items. These results suggest that cognitive processes occurring during the waking state, NREM and REM sleep are qualitatively different and that the automatic spread of activation believed to underlie semantic priming is strongly hindered during REM sleep. This hindering of normal cognitive processing helps to explain the bizarre and hyperassociative nature of REM sleep dreaming.
The following studies had a different purpose and mainly assessed postlearning sleep modifications. De Koninck et al. (1989) monitored native English-speaking students during a 6-week French immersion course. Their knowledge of this language was limited to secondary-school level. While the proportion of REM sleep increased in these subjects during the course, the other sleep stages were not modified. This increase in REM sleep correlated with improvements in performance. Thus, subjects who did not really progress during the course (improvement <4%) did not have any significant modification in REM sleep. These results must, however, be viewed with caution. Indeed, this task consisting in acquiring new information in semantic memory (reason why we class it as a semantic task), is not a pure-process task since it also involves, at least, an episodic component. Likewise, Mandai et al. (1989) studied modifications in REM sleep after a Morse code learning session. Subjects underwent a 90-min training session that consisted in identifying and reproducing sets of Morse code signals. This training session was administered before sleep and subjects were retested on the same task after awakening. Learning Morse code led to an increase in the amount of REM sleep and of the number of REM sleep episodes. Moreover, performance correlated with the density of REMs during REM sleep. Once again, these results suggesting a beneficial effect of REM sleep must not be taken at face value, as this task also involves a major procedural component. In this sense, learning Morse code could also be regarded as a cognitive skill which also depends, as previously shown, on REM sleep.
The results of the studies presented in this section indicate (1) that cognitive processes occurring during the waking state and the diverse sleep stages are qualitatively different and (2) that the amount of REM sleep increases after the acquisition of new semantic knowledge. The importance of these results remains, nonetheless, limited by the fact that the tasks used in the literature to assess semantic memory are not pure and involve procedural and/or episodic memory. Hence, it is hard to say whether the consolidation in semantic memory truly benefits from REM sleep or depends instead on the other processes involved.
Sleep and episodic memory
Literature dealing with episodic memory consolidation during sleep is particularly abundant but reveals several discrepancies. Yaroush et al. (1971) studied the retention of a word list across retention intervals located either during the day (waking state) or during the first or the second half of the night. The authors found a beneficial effect of sleep in the first half of the night (i.e. SWS) on recall performance. By the same token, Barrett and Ekstrand (1972) explored the consolidation of a word list in three groups of subjects. To eliminate circadian effects, the retention interval was placed between 2:50 hours and 6:50 hours for all subjects. This interval corresponded to a wakeful period for the first group and, for the second and third groups, to early sleep (rich in SWS) and to late sleep (rich in REM sleep) respectively. Recall was better after sleep than after wakefulness and better when the retention interval was filled with SWS rather than with REM sleep. More recently, Plihal and Born have confirmed these results. Using a partial sleep deprivation paradigm, they showed that SWS enhances declarative memory, as assessed via two distinct tasks: a verbal paired associate task (Plihal and Born, 1997; see Fig. 2b) and a mental spatial rotation task (Plihal and Born, 1999a).
Gais et al. (2002) have also supported the involvement of NREM sleep in the consolidation of episodic or declarative memories, measuring learning-dependent sleep modifications after paired-associate learning. The authors administered a cued recall task immediately after learning and after a whole night's sleep. Spindle density was higher in subjects who performed the learning task than in control subjects. This effect was maximal during the first 90 min of sleep. In addition, spindles density correlated with performance on immediate and delayed cued recall. Spindle activity during non-REM sleep therefore appears to be particularly sensitive to the learning consolidation and thus successful recall of episodic information.
However, other studies have brought conflicting results. Thus, the recall of words, grammatically correct but meaningless sentences, and prose passages is significantly impaired after selective REM sleep deprivation (Empson and Clarke, 1970). Likewise, the recall of short stories is sensitive to REM sleep deprivation (Tilley and Empson, 1978). A beneficial effect of REM sleep has also been found for the recall of words belonging to different semantic categories (Tilley, 1981) as well as for the retention of emotional texts (Wagner et al., 2001). Only one study (Chernik, 1972) has failed to find any significant impairment of word-pairs retention after REM sleep deprivation. Lastly, Ficca et al. (2000) have shown that the recall of pairs of unrelated words is impaired after fragmented sleep leading to a disruption of the sleep cycle, but not if awakenings during the night preserved the sleep cycle. This emphasizes the importance of sleep organization, i.e. the regular occurrence of NREM-REM sleep cycles, rather than of specific sleep states per se.
Studies concerning episodic memory consolidation present a degree of heterogeneity in their results, probably because of the nature of the stimuli used (e.g. neutral/emotional) and the cognitive processes involved. Moreover, many of the tasks used to assess episodic memory do not truly fit the current definition of this memory system. As previously mentioned, episodic memory refers to a system which stores events located in time and space, and is characterized by autonoetic consciousness. Autonoetic consciousness corresponds to a feeling of re-experiencing or reliving the past and mentally travelling back in subjective time. It differs from noetic consciousness, which characterizes semantic memory and corresponds to the subject's ability to be aware of information about the world in the absence of any recollection (Tulving, 1985, 2001, 2002; Wheeler et al., 1997). Autonoetic consciousness is usually assessed during recognition tasks with the Remember/Know (R/K) paradigm (Gardiner et al., 1998). ‘Remember’ responses are based on the subject's ability to re-experience the source of acquisition of the event (spatio-temporal and phenomenological details) and reflect autonoetic consciousness. By contrast, ‘Know’ responses, reflecting noetic consciousness, are based on a feeling of familiarity in the absence of conscious recollection. The tasks used to assess episodic memory in sleep studies are generally restricted to learning lists of words. The different components of episodic memory (factual, spatial and temporal) are rarely dissociated, and the state of consciousness is given little consideration. Some recent studies of episodic memory have used original tasks which fit more comfortably within current theoretical frameworks. Accordingly, we will now focus on this handful of studies that have assessed episodic memory via purer tasks than the aforementioned.
Peigneux et al. (2004) recently performed a neuroimaging study using a virtual route-learning task. These authors discovered that hippocampal areas that were activated while exploring the 3D environment were re-activated during subsequent SWS (Fig. 5a). In addition, the hippocampal activity expressed during SWS was positively correlated with the improvement in route retrieval on the following day (Fig. 5b). These results support the view that re-expression of hippocampal activity during post-training SWS reflects the off-line processing of recent spatial episodic traces, which may lead to the plastic changes underlying the overnight improvement in performance.
Figure 5. Hippocampal reactivation during slow-wave sleep and consolidation of spatial episodic memories. (a) Regression between regional cerebral blood flow increases during SWS and overnight improvement in performance (distance left to the target in presleep minus postsleep session) superimposed on sagittal (top) and transverse (bottom) cross-sections of the average T1-weighted MR image. Activations are located in the right parahippocampal gyrus (top cross-section) and right hippocampus (visible on both cross-sections). Adapted with permission from Peigneux et al. (2004).
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Recently, in a partial sleep deprivation paradigm, we investigated the consolidation of episodic memories using an original task that takes into account the three components (factual, spatial, and temporal) of episodic memory, as well as the state of consciousness of the subject performing the task (Rauchs et al., 2004). This task, called the ‘What–Where–When’ test (Guillery et al., 2000) consists in memorizing two lists of words (factual information or ‘What’), their location (at the top or the bottom of a page; spatial information or ‘Where’) and the list to which they belong (temporal information or ‘When’). Immediately after subjects have learned this information, free recall is tested. The second part of the task took place after a 4-h retention interval and comprised another free recall, followed by a forced choice recognition task for the word and each feature (spatial and temporal). For each response during this recognition task, subjects also had to indicate their subjective experience by means of the R/K paradigm (Gardiner et al., 1998). Thus, subjects give either an R response, if they are able to bring to mind some recollection of what occurred when the item was encoded (i.e. thoughts, feelings or perceptions) or a K response, if retrieval is achieved without this access. Our main results indicated that spatial aspects of episodic memory (including the number of spatial features remembered and R responses associated with a correct recognition of the location of the items) benefit from late REM sleep, whereas SWS appears to be more beneficial to the temporal dimension of episodic memory (see Fig. 6). Hence, we suggest that the consolidation of a genuine episodic memory, i.e. including all its dimensions, requires both SWS and REM sleep, these stages probably dealing with distinct aspects of the memory.
Figure 6. Mean performance (±SD) on delayed free recall for spatial information (top) and mean forgetting rate (±SD) of temporal information (bottom) after early and late sleep (grey bars) and corresponding wake control groups (white bars) for an episodic memory task: the ‘What, Where, When’ test. While consolidation of spatial information benefits from REM sleep, consolidation of temporal features appears to rely instead on SWS. *P < 0.05; **P < 0.01. Adapted from Rauchs et al. (2004).
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Fosse et al. (2003) have examined the relationships between dreaming and episodic memory, focusing on the degree of similarity between the events that have occurred during the recent waking life and the dreams. Subjects kept a diary in which they reported their activities and dream reports. Recent episodic memories, assessed using very strict criteria, were replayed in less than 2% of the dreams. So, while elements of memories of recent waking life are reactivated during sleep, they do not take the form of intact episodic memories. For these authors, reactivation of episodic memories appears to be actively blocked during sleep. This finding, which suggests that sleep does not act on the memory traces to be consolidated, must be viewed with caution, as this study does not specifically assess retention. Nonetheless, the fact that only a few elements of an episodic memory are reactivated during sleep provides new insights into the process of consolidating episodic memories. Indeed, in a discussion of the study performed by Fosse et al. (2003), Schwartz (2003) provides a possible explanation for episodic memory consolidation during sleep. During the waking state, information flows to the hippocampus, which links together the various elements of an episodic memory that will be stored in different neocortical areas. According to some authors (Buzsaki, 1996; Hasselmo, 1999), the memory trace is transferred during SWS to the neocortex through neuronal bursts initiated in the hippocampus. By contrast, during REM sleep, the hippocampal outflow to the neocortex is blocked, and information flows mainly in the opposite direction. During this sleep stage, the information arriving in the hippocampus, at least for recent memories, probably flows from independent cortical modules. Because of this, there is no reason to expect a report of complete and integrated episodic memories during REM sleep. The results would be different for older, consolidated memories, i.e. stored within inter-connected cortical modules. Moreover, recall processes depend on the integrity of the prefrontal cortex, which is deactivated during sleep. Thus, one can assume that episodic elements will be reactivated during sleep in a fragmented fashion, rather than in the form of an integrated life episode (Schwartz, 2003).
This model of memory consolidation proposed by Buzsaki (1996) and Hasselmo (1999) has recently been tested in humans (Gais and Born, 2004). In this study, the authors showed that an injection of the cholinesterase inhibitor physostigmine during SWS prevents the consolidation of declarative memories but has no effect on the consolidation of a motor skill. Thus, while the acquisition of declarative (or episodic) memories requires high levels of acetylcholine during the waking state (Hasselmo, 1999), the consolidation needs a low cholinergic tone, which results in the cholinergic suppression of excitatory feedback synapses in the hippocampal CA3 field and on efferent projections spreading activation from CA3 to CA1, the entorhinal cortex and neocortex. Thus, the reduction of acetylcholine levels may provide an ideal window for transferring memory traces that have been recently encoded and indexed in the hippocampus to the neocortex.
Results concerning episodic memory consolidation have provided heterogeneous results, most of them arguing in favour of the role of SWS, others in favour of REM sleep. This heterogeneity can be explained, at least in part, by the material used and the processes involved while performing the task. Further investigations would appear to be necessary, in order to find out whether these partially discrepant results can be explained by the fact that episodic memory consolidation depends, like the consolidation of implicit information, on the alternation of both SWS and REM sleep episodes. Virtual reality techniques seem to be particularly useful in assessing contextual memory (spatial and temporal context) more accurately.