SLEEP AND MEMORY II:
INVESTIGATIONS ON HUMANS
Vadim S. Rotenberg vadir@post.tau.ac.il
NEUROSCIENCE and BIOBEHAVIORAL REVIEWS, 16(4) 503-505, 1992.
The positive effect of delta-sleep on retention depends on REM sleep, which facilitates this positive effect, but at the same time has its own inhibitory effect on retention. The nature of this double influence of REM sleep on retention is discussed in the context of the restoration of search activity being the main REM sleep function. Such restoration can explain the indirect positive effect of REM sleep on retention, especially on retention of the unusual and emotionally meaningful information that can cause distress. Psychic activity in REM sleep (dreams) has a direct negative effect on retention, which may be due to the interference between dream images and learned material.
Key Words: Memory, REM sleep,Delta-sleep, Search activity,Dreams
In investigations performed on animals, the greatest attention has been paid to the dynamic of sleep structure in relation to the learning process. The results of the similar investigations performed on humans contain some contradictions.
For example, the process of adaptation to the experience of inverted space (elicited by special eye-glasses) was accompanied by an increase of REM sleep and decrease of REM sleep latent period (LPREM) (17,20). These results were not confirmed, however, by Alien, Oswald, Lewis, and Tagney (1): REM sleep remained constant during this training despite progress in the process of learning. Verbal tasks did not produce alteration in sleep structure (16). In another study, however, success during intense learning of a foreign language correlated with a definite increase in REM sleep percentage (7) and subjects who displayed this increase were free from emotional stress during learning. A load on the visual system during the day was accompanied by a slow-wave sleep increase (13).
These contradictions may present evidence of the dependence of sleep alterations on the subject's attitudes to the learning process: If the subject demonstrates renunciation of search in the unusual and complicated situation (inverted visual perception, intensive learning of foreign language), REM sleep requirement may increase and the result of the learning process may depend on the degree of satisfaction of this requirement. This remains only a hypothesis.
The most common experiment performed on human subjects is based on another method: Subjects were motivated to learn a verbal text before the night's sleep or after awakening during the night, and afterward the retention of this material was correlated with the percentage of different sleep stages, to determine the influence of these sleep stages on the process of retention.
One of the best investigations within this model was performed by Latash and Manov (14) with results that are of interest to this discussion. For the learning task, subjects in this study received two lists of verbal material: nonsensical trigrams, and words that contained three letters (consonant, vowel, consonant). The whole investigation was divided into three subsequent experiments. The goal of the first experiment was to show whether the night's sleep has a positive influence on the retention of material learned immediately before sleep as compared with the same period of wakefulness. The positive influence of sleep on retention was confirmed. Especially prominent was the beneficial influence on the retention of nonsensical material in comparison to the words. The authors concluded that the nonsensical material, which does not provoke any associations, requires some additional processes of assimilation that takes place during sleep. This conclusion is in agreement with the results of Benson and Feinberg (3).
In the second stage of this investigation, Latash and Manov used only nonsensical trigrams. The experiment was divided into two parts. At first, subjects learned trigrams before sleep, and the level of retention was tested during experimental awakenings after the end of the second sleep cycle. In the second part of the experiment, the learning process took place during the experimental awakening after the second sleep cycle, and the level of the retention was tested after the natural morning awakening. During the first two cycles, delta-sleep dominates; during the last two cycles REM sleep dominates. That is why it was possible to investigate the influence of delta and REM sleep on retention separately. The authors found a prominent positive effect of delta-sleep on retention.
As of now, the concrete brain mechanisms that facilitate retention during delta-sleep have not been discovered. It is only possible to suggest that during delta-sleep the informational overload is overcome through the reorganization of information according to its importance for the subsequent wakefulness. An indirect argument for this suggestion may be derived from the data about the alterations of behavior after delta-sleep deprivation: sleepiness, decreased attention, and decreased ability to assimilate new information. It is possible that the galvanic skin reaction increase in delta-sleep reflects the process of reorganization of information according to the degree of the importance of the latter.
REM sleep also has an effect on retention, but this effect was more ambiguous: on one hand, retention was higher after the second half of the night (when REM sleep predominates) than during the same time period spent in wakefulness (9). On the other hand, there are no correlations between the degree of retention and the percentage of REM sleep. At the same time, in these two last cycles delta-sleep also does not correlate with retention (14). The authors found that the correlation between delta-sleep and the amount of retention after the second part of the night became reliable statistically only when they took into consideration the ratio between delta-sleep time and time occupied by rapid eye movements in REM sleep. The higher the ratio-eye movements time to delta-sleep time (ratio I)- the higher is the retention. The total amount of rapid eye movements does correlate with REM sleep time, but retention does not correlate with the ratio of REM sleep time to delta sleep time (ratio II). The authors came to the conclusion that the absence of the latter correlation, in spite of the presence of the correlation between retention and ratio I, is a sign of a negative effect of the tonic components of REM sleep on retention. It seems that REM sleep has a double effect on retention: facilitation and inhibition.
This interesting and unpredictable conclusion was confirmed in the next experiment. Subjects were awakened in the first or second cycle in delta-sleep or after the first or second episode of REM sleep. Every subject received all four conditions, but every night every subject had only one awakening, during which he was tested for the amount of retention of the material the subject learned before going to sleep. The authors found that the loss of information during sleep is not determined by the period from learning to testing. Retention after the second REM sleep episode is lower than immediately before the second REM sleep episode. (In the previous sleep period such a great loss does not take place, despite the fact that the length of this period is longer.)
The addition of a short period of time that is spent in a second REM sleep episode has a more inhibitory influence on retention than one would predict, which suggests that REM sleep per se has an inhibitory influence on retention. At the same time, the retention after REM sleep displayed a positive correlation with the previous delta-sleep, but this correlation was absent if the subject was awakened before REM sleep but after delta-sleep. Only after the second REM sleep episode was it possible to find a positive correlation between delta-sleep and retention. This means that the positive effect of delta-sleep on retention depends on REM sleep, which facilitates this positive effect, but at the same time has his own inhibitory effect on retention.
How is it possible to explain these results? What is the nature of the double influence of REM sleep on retention? I suggest that the explanation of the REM sleep effect on memory as a psychic function must be based on the psychological function of dreams. It is necessary to recall that in humans, as in animals, the effects of REM sleep deprivation on memory depend on the peculiarity of the previous or subsequent learning. For instance, REM sleep deprivation before learning does not interfere with the retention of trigrams (6) and does not
destroy verbal memory (15). Moreover, the retention of paired word associations is worse after sleep that contains a high percentage of REM sleep (2). At the same time, the retention of more complicated and unusual material, such as tasks requiring divergent thinking, requires REM sleep participation (8,15). REM sleep is especially important for the retention of the emotionally significant and relevant information. An excellent experiment (11) elicited an effect opposite to the Zeigarnik effect in subjects who were deprived of REM sleep after the process of the solution of a list of difficult and frustrating anagrams.
When REM sleep is preserved, subjects do not lose information that is emotionally meaningful and provokes a feeling of incompetence (5). Both the activation of the divergent way of thinking and an emotionally stressful situation before sleep increase REM sleep percentage in the second half of the night. Night sleep that was characterized by a high ratio REM sleep/ delta sleep, blocked the negative solution of a conflict situation in TAT but did not help to resolve crosswords (4). After sleep with a high REM sleep percentage, relevant information was assimilated easily (18).
Thus, REM sleep is necessary for the assimilation of information that touches the subject deeply, or for the assimilation of unusual information, that is, for unprepared learning. These are the findings we have seen in animals. And the explanation may also be the same: if the situation connected with the learning process causes the renunciation of search, then REM sleep is required for the compensation of this state. If there are no signs of giving up, depression or neurotic anxiety, then the requirement of REM sleep is also not very high, for instance, in short sleepers who are active and energetic and have a restricted REM sleep (12). Usually they have no complaints regarding their memory.
Now let us turn to the question of why REM sleep plays an important role in the retention of nonsensical trigrams in the above-mentioned experiment performed by Latash and Ma-nov (14). Our previous analysis led us to the conclusion that for such mnemonistic activity, REM sleep must be unimportant. It is necessary to recall that the positive role of REM sleep in the retention of trigrams is realized not directly, but only through the increase of delta-sleep efficiency. It is also necessary to take into consideration that subjects involved in the psychological experiment also have problems in their own lives that have nothing to do with the experiment, and these problems may sometimes cause anxiety, especially in the evening. This emotional tension, which often appears in the evening in the so-called sensitive subjects of long-sleepers, requires REM sleep for its compensation; and if this compensation did not take place it might have a negative effect on retention, including the retention of the irrelevant information. This emotional tension could destroy the memory process in delta-sleep, and the positive REM sleep influence on memory might be discovered only through the ratio of rapid eye movements to delta sleep. Before Latash and Manov no one used this ratio for investigations of memory functions. In this context it is necessary to stress, that in retarded children a positive correlation was established between retention and phasic components of REM sleep (10).
Along with the indirect positive effect on retention, the psychic activity in REM sleep also has a direct negative effect on retention, which may be due to the interference between dream images and learned material. The vivid and emotional images can compete with the experience of the previous wakefulness. The interference between different dreams was established by special investigations (19).
Because short-lasting awakenings around REM sleep are common, dreams can interfere with one another and also with any information perceived during wakefulness. We suggest that this is the nature of the double effect of REM sleep on memory: As a restorer of search activity REM sleep increased the effectiveness of mnestic processes, but as a container of concrete information it can interfere with memory process. The role of these different functions in different conditions may also be different. If the learning process per se causes the renunciation of search, the requirement in REM sleep is especially high. If not, REM sleep deprivation may even facilitate retention.
Of course, dream content per se may also by chance enhance memory function, especially if dreams contain (or at least reflect) information from the previous wakefulness that has to be retained. If the relevant information is supplied during REM sleep as a natural component of dreams or in the experimental conditions, this information has more of a chance for retention due to the general positive influence of the REM sleep on memory. However, it is necessary to stress once more that according to the present point of view, REM sleep, irrespective of the concrete content of dreams, may have a positive influence on memory due to the restoration of search activity.
ACKNOWLEDGEMENTS
My best thanks to Prof. R. Greenberg and Dr. J. Fisch for help in manuscript preparation.
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