consolidation of implicit memory traces during rem sleep
TRANSCRIPT
Tel-Aviv UniversitySchool of Social Studies
Department of Psychology
Consolidation of Implicit Memory Traces
During Rapid Eye Movement (REM) Sleep
Thesis submitted in partial fulfillment of theM. A. degree in cognitive psychology
Tel-Aviv University, Israel
By
Michal Eisenstein
Directed by
Dr. Yonatan Goshen-GottsteinDr. Yaron Dagan
November 1999
Table of Contents
1
Abstract 3
Introduction 4
Animal Studies 6
Human Studies 13
The present study 19
Methodology 22
Subjects 22
Tools 22
Design
25
Procedure 26
Results
28
Sleep data 28
Priming data 29
Discussion 33
References 36
2
Abstract
It is well established that registration of information is followed by a
brief period of time, the phase of consolidation, allowing short-term
memories to be converted into more enduring long-term ones. Sleep,
or more specifically, REM sleep, seems to play a role in this process.
Previous studies in humans have shown that sleep is involved in the
consolidation process of procedural memory tasks, but not always in
that of explicit memory tasks. We would like to show that
consolidation of implicit memory traces also occurs during REM sleep.
15 normal undergraduate students participated in a sleep study in
which they went through a REM deprivation night and a control night,
counterbalanced in order. Before going to sleep, subjects studied a list
of words by judging their pleasantness (deep processing). The
following morning they were instructed to fill in fragments of these
studied words and of new, unstudied words with the first word that
comes to mind (implicit memory task). Subjects also performed a
control task. As expected, performance following REM deprivation was
poorer than that following the control night. The control task assured
that this was not due to cognitive fatigue following REM deprivation.
The implications of these findings are discussed, together with further
research possibilities.
3
Introduction
Time is an enemy of memory, although forgetting does have some
adaptive features. We often forget our memories, some rapidly, while
others more slowly. Indeed, psychologists and neurobiologists have
discovered that some memories appear to be more resistant to
forgetting than others, and even become more resistant to forgetting
as time passes. The term consolidation may help clarify this seemingly
puzzling state of affairs.
The concept of consolidation has had a long controversial history in
the psychology and neurobiology of memory (Schacter, 1996,). Many
of the current researchers of this field distinguish between two quite
different types of memory consolidation.
One type of consolidation operates over time periods of months,
years, and even decades. That is, some memories become more
resistant to disruption by brain injury as the years pass (Schacter,
1996). This is not the type of consolidation that this study addresses.
The second type of consolidation, which is relevant for this paper,
operates over time periods of minutes or hours. It is well known that
registration of information is followed by a brief period of time – the
phase of consolidation, which refers to neural processing that occurs
after information is initially registered and contributes to its permanent
storage (Nadel & Moscovitch, 1997; for a review, see McGaugh, 1966).
This is when immediate or short-term memories are converted into
4
more enduring long-term memories. During this period, application of
various treatments can impair or improve subsequent retention
performance, hence indicating that the new memory is at that time in
a labile, unsettled form (Hennevin, Hars, Maho & Block, 1995).
Neurobiologists have studied this type of consolidation process
extensively in rats, mice, and other even simpler organisms, and have
arrived at the conclusion that the long-term memory involves a
process known as protein synthesis and appears to be accompanied by
the growth of new synapses. This can be seen as a switch from a
process-based memory to a structural- based memory. Still, no one
knows exactly what changes in the brain correspond to long-term
memory consolidation, nor how and when it takes place (Schacter,
1996).
Recent research points to a possible player in the consolidation
process: Sleep. Over a decade ago, the neuroscientist Jonathan Winson
(for review, see Winson, 1993) hypothesized that memory becomes
consolidated during sleep, particularly during Rapid Eye Movement
(REM) sleep - the “dreaming” stage. REM sleep is a paradoxical state,
originally termed paradoxical sleep (PS) by Jouvet (1967). The paradox
consists of the simultaneous presence of total muscular atonia in
contrast with heightened activity displayed by a variety of other
biological channels, such as the electroencephalogram (EEG),
electrocardiogram (ECG) and breathing. Winson’s idea was that during
sleep, the brain is not preoccupied by external stimulation and is thus
free to work through the experiences of the day, discarding the trivial
5
and saving the significant. Indeed, the presence of dreaming in REM
sleep suggests that some type of internal information processing is
taking place. Sleep researchers have often observed that dreams
contain remnants of recent experiences. It seems likely that as we
sleep, our brains are working hard to save the experiences that will
remain with us. The goal of this study was to shed more light upon the
role played by REM sleep on memory consolidation.
That consolidation of memory occurs during REM sleep can, in
principle, be obtained from both neuro-chemical evidence and from
behavioral evidence. The following review of the literature includes
both animal studies and human studies, the latter introduced
separately, and later on in the text.
Animal studies
Neuro-chemical evidence
There is more than one reason to believe that post-training REM sleep
is a time for enhanced cellular and synaptic changes, one of which
appears to be enhanced activity of the transmitter Acetylcholine (ACh).
ACh has long been linked with both learning/memory processes
(Corkin, 1981; Coyle, Price & DeLong, 1983; Deutsch, 1983), and REM
sleep activity (Baghdoyan, Rodrigo-Angulo, Assens, McCarley &
Hobson, 1987; Gillin & Sitaram, 1984; Jouvet, 1975; McGinty &
Drucker-Colin, 1982; Sitaram, Weingartner, & Gillin, 1978).
Furthermore, levels of ACh and AChE (acetylcholine esterase) activity
have been observed to gradually increase over normal levels at the
6
same time that REM sleep increases were observed in the shuttle
avoidance task (in which rats learn to avoid an aversive electric shock
preceded by a tone; Smith, Tenn & Annett, 1991). Interference with
normal ACh metabolism by both the protein synthesis inhibitor
anisomycin and the ACh antagonist scopolamine during the period in
which increases in REM sleep were observed resulted in poorer task
memory as well as lower levels of ACh and AChE. These drugs were
ineffective when applied either before or after this specific time period
of REM sleep increases (Smith et al., 1991).
The hypothesis that neuro-chemical processes occurring during REM
sleep actively contribute to the effectiveness of processing memories
necessitates that first, brain mechanisms that allow information
processing would be active during REM sleep. And second, that the
effects of events that occur during REM sleep could be transferred to
the awake state (Hennevin et al., 1995). It is widely accepted that at
the cellular level, REM sleep shares many functional characteristics
with wakefulness (Llinas & Paré, 1991; Steriade, 1989): both are brain
activated states, implying a tonic readiness of cerebral networks
securing synaptic transmission and prompt cellular responses to
afferent information. In both states, thalamo-cortical neurons display
enhanced excitability and a tonic mode of discharges permitting
increased transfer function of incoming messages, as opposed to the
oscillatory mode of functioning that characterizes slow-wave sleep
(SWS - for review, see Steriade, 1991). Despite this, the ability of the
brain to process information during REM sleep remains controversial.
7
Behavioral evidence
At the behavioral level, two lines of evidence suggest that
consolidation of memory traces, at least regarding certain types of
learning, occurs during REM sleep.
REM sleep increases following training
The first line of evidence comes from findings showing that REM sleep
increases following successful task acquisition (Block, Hennevin &
Leconte, 1979; Hennevin & Leconte, 1971; McGrath & Cohen, 1978;
Smith, 1985; Smith, Kitahama, Valatx & Jouvet, 1974; Smith & Lapp,
1986; Smith & Wong, 1991; Smith, Young & Young, 1980). Thus,
REM sleep increased in mice and rats following a variety of learning
procedures, such as “active avoidance conditioning”. In this
paradigm, rats learn to avoid an aversive electric shock by jumping
to the other side of the cage after a sound that precedes an electric
shock. While rats were learning this task, a significant increase was
found in the quantity of their REM sleep recorded after each daily
period of training. When learning was completed and the animals
performed the task almost perfectly, the quantity of their REM sleep
returned to normal, pre-learning levels. The control animals that did
not exhibit learning did not show such an increase in REM sleep
(Bloch et al., 1979). This suggests that REM sleep is linked in
important ways to successful learning. Similar results can be found
for other types of learning, such as lever pressing and maze
learning (Bloch et al., 1979).
8
In addition, when sleep was delayed for three hours after each
learning session, the acquisition of learning was impaired and there
was no increase in REM sleep. Bloch et al. (1979) thus summarized
their studies: “It would appear that one of the essential elements of
memory fixation is the presence of REM sleep in sufficient quantity,
occurring quickly after learning”.
Nevertheless, several studies recorded 24-hours per day during
baseline and for the duration of the training situation. In these studies,
the levels of REM sleep were observed to persist for times well beyond
the first three post-training hours (Fishbein & Gutwein, 1977; Smith,
Conway & Rose, 1993; Smith et al., 1974; Smith, Lowe & Smith, 1977;
Smith & Wong, 1991; Smith et al., 1980). Thus, all these studies
showed that the REM sleep increases following the end of training
persisted longer than three hours and often had a latency to onset
after the end of training of more than three hours (for a detailed
review, see Smith, 1996).
In a few studies, continuous sleep recording was carried out for
periods of several days after the end of acquisition (Smith & Lapp,
1986; Smith et al., 1980). Altogether, it seems clear that post-training
REM sleep increases are quite prolonged, and may persist for as much
as six days after training. As for the latency to onset and duration, they
appear to be a function of the strain and type of animal, the task, and
even the number of training trials per session (Smith, 1996).
9
Post-training REM sleep deprivation studies
The second line of behavioral evidence demonstrating that
consolidation of memory traces occurs during REM sleep, a line that
will be pursued in the present study, is found in the impaired memory
that is observed when REM sleep is selectively prevented (Block et al.,
1979; Fishbein & Gutwein, 1977; Hennevin & Leconte, 1971; McGrath
& Cohen, 1978; Pearlman, 1979; Smith, 1985; Smith & Butler, 1982;
Smith & Kelly, 1988; Smith & Lapp, 1986; Smith & MacNeill, 1993). In
studies of this type, rats are trained in a specific task and are deprived
of REM sleep immediately afterwards (it should be noted that some
studies, pre-training REM sleep deprivation was performed. These were
not included in the present review, as they do not test the
consolidation hypothesis). The most widely used technique for
depriving animals of REM sleep is the “inverted plant pot” (also “water
tank” and “pedestal”) technique. A small plant pot is placed upside
down in a basin of water leaving only a very slim surface above water.
The animal is placed on the surface for that period of time during
which REM sleep is to be prevented. Animals can stay above water
during waking and non-REM (NREM) sleep, yet as soon as they enter
the REM stage, they lose postural tone (due to the muscular paralysis
characteristic of REM sleep), and partially or fully slip from the pedestal
into the water and awaken. The procedure is thought to fairly
selectively deprive animals of REM sleep. Controls are placed on larger
diameter pedestals or allowed normal sleep in their cages.
10
A large number of studies were performed with no knowledge of the
latency to onset or the duration of the REM sleep increases following
the end of the training session. It was usually assumed that REM sleep
increases would manifest in the first few hours of sleep following
training (for review, see Block et al., 1979; McGrath & Cohen, 1978;
Pearlman, 1979; Smith, 1985).
In one such study, rats were trained and returned to their cages after
spending two to three hours on plant pots. When they were tested 24
hours later, they showed deficient retention in comparison with control
rats who were returned to their cages immediately after training, or
who, after spending two hours undisturbed in their cages, were put on
the plant pots for the same period of time (Pearlman & Greenberg,
1973).
In other studies, however, REM sleep deprivation (REMD) was carried
out on animals in which the post-training REM sleep changes had been
examined. As a consequence, it was possible to correlate the onset of
the REM sleep increases observed with the time after training that the
REMD was most effective in impairing memory. Thus, on the basis of
these studies using the same
experimental situation, the concept of the REM sleep window
(REMW) was introduced (Smith, 1985).
The REMW has been defined as a time after acquisition when there
are increases in REM sleep over normal levels. What's more, if REMD is
applied at these times of expected above normal REM sleep, there is
memory impairment (Smith, 1985). Regarding the characteristics of
11
the REMW, the general pattern seems to be that, for a given task, the
more trials given in a single session, the shorter the latency to onset of
the first REMW (Smith, 1996). When a smaller number of trials per
session is given over a period of days, it is possible to see increases in
REM sleep in the 24-h period just prior to an increase in actual correct
performance at the behavioral level (Smith et al., 1974; Smith et al.,
1980). These results suggest that the REM sleep changes can actually
predict the imminent onset of the most prominent behavioral
improvements. It also implies that a certain amount of learning must
occur before the REM sleep mechanism is triggered (Smith, 1996).
In one study (Smith & Butler, 1982), during five days of shuttle
avoidance training, rats were allowed REM sleep only during the two
previously established REMW’s (9-12 h and 17-20 h after the end of the
last training trial; Smith & Butler, 1982; Smith et al., 1980), while REMD
continued outside of these times. Despite the obvious signs of stress as
a result of the extended REMD, these animals learned as well as rested
controls.
In other studies, however, it was found that the relationship between
memory consolidation and REM sleep might be much more complex. It
seems that learning some tasks is negatively affected by REMD, while
learning other tasks is not, or even in a few cases, facilitation of
performance was reported. Greenberg and Pearlman (1974) have
attempted to reconcile the lack of consistent results by proposing a
distinction between REM-dependent and REM-independent learning,
according to the relative difficulty of the task to be learned. Based on
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Seligman’s (1970) distinction between prepared and unprepared
learning, they suggested that tasks involving little change in the
animal’s behavioral repertoire are REM-independent and hence
resistant to REMD, whereas tasks that require assimilation of unusual
information and adaptative change in behavior are REM-dependent
and thus impaired by REMD. Experimental data provide relatively
consistent support for this proposition (see Pearlman, 1979).
It should be mentioned that REMD has consequences other than
impaired retention. With use of the inverted plant pot technique, stress
and frustration are inevitable due to the confinement conditions, falling
into the water and sleep interruption. In addition, REMD produces a
state of heightened cerebral excitability (for a critical review, see
Horne & McGrath, 1984).
Before moving on to studies conducted in human subjects, it should
be stressed that in animals, the memory tasks investigated in order to
assess the role of REM sleep in memory consolidation are procedural in
nature. In human subjects, however, additional memory systems can
be examined. This would allow us to examine whether REM sleep plays
a role in the consolidation of these memory systems as well.
Human studies
In studies with human subjects, the role of REM sleep in consolidation
is equivocal. Most of the studies designed to test whether memory
consolidation was linked to REM sleep in humans usually yielded
conflicting results (Horne & McGrath, 1984; McGrath & Cohen, 1978).
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REM sleep increases following training
On the whole, human studies have not shown that heightened
learning experiences or enriched conditions in waking produce
increases in the amount of REM sleep (Allen, Oswald, Lewis & Tagney,
1972; Bowe-Anders, Herman & Roffwarg, 1974, Horne, 1976; Horne &
Walmsley, 1976; Zimmerman, Stoyva & Reite, 1978), although there
have been some exceptions, as can be seen below.
One study observed the sleep of students at times when they were
not taking any courses and again just after they had completed their
exams. Compared to their own baseline levels and to control subjects
not taking exams, the test subjects exhibited increases in the number
of actual eye movements and eye-movement density from 3-5 days
after the end of their exams (Smith, 1993; Smith & Lapp, 1991).
Additional findings indicate that REM sleep does play a role in special
learning tasks. When language learning of aphasics was observed, an
increase in REM sleep was found in those patients who succeeded in
re-learning a large portion of the words they had forgotten, while the
REM sleep of patients who failed to re-learn their lost vocabulary
remained unchanged (Greenberg & Dewan, 1969). What's more, it has
been found that intensive learning of a new language by young people
is associated with an increase in REM sleep (De Koninck, Proulx, healy,
Arsenault & Prevost, 1975).
Furthermore, evidence regarding the relationship between REM sleep
and intellectual aptitude has been obtained from experiments on
mentally retarded children. In these children, the duration of REM sleep
14
is usually shorter than that in normal, age-matched children, and
characterized by fewer eye movements (see Castaldo, 1969; Grubar,
1983). A positive correlation has also been established between
retention and phasic components of REM sleep in retarded children
(Fukuma, Umezava, Kobayashi & Motoike, 1974).
Post-training REM sleep deprivation studies
An examination of earlier human studies in which training was
followed by REMD and then subjects were tested for retention at some
later time shows varied results. When the material to be learned
consisted of such tasks as word lists or paired associates, no
deprivation effects were reported (Castaldo, Krynicki & Goldstein,
1974; Chernik, 1972; Ekstrand, 1972; Ekstrand, Sullivan, Parker &
West, 1971; Empson & Clarke, 1970; Lewin & Glaubman, 1975;
McGrath & Cohen, 1978; Smith, 1993). However, when the material to
be learned consisted of more complex manipulation of words or
symbols, deprivation was reported to impair memory processes
(Cartwright, Lloyd, butters, Weiner, McCarthy & Hancock, 1975;
Empson & Clarke, 1970; Grieser, greenberg & Harrison, 1972; McGrath
& Cohen, 1978; Smith, 1993; Tilley & Empson, 1978).
It has recently been reported that memory for a complex logic task
was impaired following either total sleep deprivation (TSD) or selective
REMD, while memory for a paired associate task was not impaired
under either of the above conditions (Sandys-Wunsch & Smith, 1991;
Smith, 1993; Smith & Whittaker, 1987). These data suggest that the
15
type of task might be differentially sensitive to REMD (Smith, 1996). In
other words, the effects of REMD following the learning phase seem to
depend on task requirements (McGrath & Cohen, 1978).
Memory systems and REM sleep
Several theorists have proposed the existence of at least two
different kinds of memory systems (Moscovitch, 1992; Schacter &
Tulving, 1994; Squire, 1986; Squire, 1987; Tulving, 1985). The
assessment of declarative or explicit memory requires direct recall
from prior episodes, while assessment of procedural or implicit
memory is attained by behavioral measures that do not require direct
recall from previous events. These two types of memory are presumed
to be processed by different functional or even anatomical systems
(Moscovitch, 1992; Schacter, 1987; Squire, 1986; Squire, 1987;
Tulving, Schacter & Starck, 1982; Weiskrantz, 1987).
Converging evidence suggests that, in contrast to explicit memory
tasks, implicit memory tasks do not require conscious or intentional
recollection. Thus, numerous dissociations have been found between
explicit and implicit tests of memory. The most striking of these, is that
displayed by amnesic patients. These patients, who by definition show
impaired performance on explicit memory tests, nevertheless display
completely normal repetition priming effects on implicit tests of
memory (Moscovitch, Vriezen & Goshen-Gottstein, 1993). Thus, it is
possible that in humans, REM sleep is essential for only certain types of
16
learning and memory tasks, while not necessary for others, depending
on the different memory systems that mediate these tasks.
Recently, the possibility that only some types of learning in humans
are connected to REM sleep was supported by a carefully conducted
laboratory study (Karni, Tanne, Rubinstein, Askenasy & Sagi, 1994).
Participants were trained to rapidly recognize oriented symbols hidden
in images flashed at a very high speed at the periphery of their visual
field. This type of task – perceptual search – is unique in that it shows a
marked improvement approximately eight to ten hours following a
training period. Participants, who were trained in the perceptual task
and then retired to sleep, showed the anticipated improvement the
next day. This improvement was also found in those participants who
were awakened repeatedly from sleep stages other than REM.
However, participants who underwent REMD failed to show the
expected improvement. The researchers proposed that the
consolidation of the learning process of this perceptual task occurred
mainly during REM sleep. Thus, it is possible that REM sleep is
especially important for tasks such as Karni et al.’s perceptual-search
task. That is, tasks considered to be procedural memory tasks.
Procedural-memory tasks (Cohen & Eichenbaum, 1993) are tasks that
measure a general ability to acquire a new skill. In the case of Karni et
al.’s perceptual-search task, the skill was that of a perceptual ability to
recognize certain stimuli embedded among other, masking stimuli, in
the visual field.
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To summarize, let us Return to the distinction between explicit and
implicit memory systems: on explicit tests of memory, memory is
tested by referring subjects to a prior learning episode and asking
them to recall or recognize previously learned materials. On implicit-
memory tasks, in contrast, participants are not referred to a prior
learning episode. Instead, memory is indexed by facilitated
performance on tasks that make no reference to the study episode.
Karni et al.’s perceptual search task is an implicit task in that subjects
were asked to recognize the embedded stimuli, and this was done
without reference to the prior learning episodes where this task had
originally been acquired.
While the perceptual-search task is a procedural task, and this may
be the important characteristic that defines its need for REM sleep to
allow consolidation, the search task is also an implicit-memory task,
and it is this aspect of the task that may be dependent on REM sleep
for consolidation1.
As for the times after acquisition when REM sleep is most important
for efficient memory processing, using a complex logic task TSD
resulted in memory loss when it occurred the same night or two nights
after acquisition (Smith, 1993; Smith & Whittaker, 1987). This result
was confirmed in a second study using ethanol to suppress REM sleep
in college students (Sandys-Wunsch & Smith, 1991). These results
suggest both a first day effect and a 2-day delayed vulnerability to
1 One unpublished study reports impaired memory following TSD or REMD for procedural/implicit tasks as opposed to declarative/procedural tasks. Subjects were sleep deprived for one night and then tested a week later. However, since the study was reported as an abstract only (Conway & Smith, 1994), it is impossible to understand exactly what was done and how to refer to this report.
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REM sleep loss. However, there would not appear to be a 3-4-h REMW
in humans as has been found in rats. Moreover, the available data
suggest that on vulnerable nights, all of the REM periods of the night
are necessary and interference with even some of them substantially
impairs memory (Sandys-Wunsch & Smith, 1991; Smith, 1993).
The present study
The purpose of this work was to determine whether REM sleep is
necessary for all types of implicit memory tasks, or only for implicit
memory tasks that test procedural memory. To this end, we examined
the role of REM sleep in an implicit memory task that does not test a
general skill (i.e., procedural knowledge), but rather, an implicit
memory task that tests specific information that was previously
learned, namely, the repetition-priming effect.
The repetition-priming effect is the facilitated ability of subjects to
identify physically degraded stimuli when these correspond to
previously studied words than when not. For example, in the study
phase subjects may be asked to process words by judging their
pleasantness (e.g., ASSASSIN), while they are not told to memorize
them and they remain unaware of the fact that they will subsequently
be tested on these words. In the test phase, subjects may be asked to
fill in fragments of these words (e.g., A_ _A_ _IN) together with
fragments of new, unstudied words, with the first word that comes to
mind. A repetition-priming effect is found when subjects complete
fragments that correspond to studied words (using the appropriate
19
studied word) with a higher probability than fragments that correspond
to unstudied words. Note that subjects have not acquired a general
ability to solve word fragments, which would have been displayed in an
overall elevated ability to complete any word fragments, but instead,
have acquired item-specific information that allows them to complete
some word fragments better than others. The same type of effect can
be found when using perceptually degraded words instead of
fragments (for a comprehensive review, see Roediger and McDermott,
1993).
Research hypotheses
The present study aimed to determine whether REM sleep is
necessary for the consolidation of implicit memory traces. Hence, a
post-training REMD procedure was performed, using an implicit word
fragment-completion task and a control task designed to assess
subjects’ general level of cognitive fatigue.
We anticipated that performance on the implicit memory task would
be impaired after a night of REM deprivation, as compared with NREM
deprivation. However, impaired implicit-memory performance may also
be attributed to general cognitive fatigue due to the REMD procedure
rather than to lack of memory consolidation per se. Therefore, a
control task was necessary to ensure that this is not the case, on
condition that performance on the control task would not differ
following REM deprivation and NREM deprivation conditions. The
20
control task was always performed after the implicit memory task,
when subjects would presumably by most fatigued.
Hence, it was hypothesized that: First, subjects’ sleep would not differ
between the two experimental nights, except for differences due to the
experimental manipulation (REMD vs. control). Second, a greater
priming effect would be exhibited on the implicit memory task
following the control night than the REMD night. And third, subjects’
performance on the control task would not differ between the control
night and the REMD night.
Should these hypotheses be verified, we may conclude that REM
sleep is critical not only for general skill learning, but also for item-
specific implicit memory. If, however, REM sleep does not affect
consolidation on the fragment-completion task (i. e. performance on
the implicit memory task would not differ between the two nights, or
would be better following the REMD night, or performance on the
control task would be worse following the REMD night, suggesting that
subjects experienced increased cognitive fatigue as a result), then
tests that are both implicit and procedural may prove to be the only
tests that require REM sleep for the process of consolidation.
Methodology
Subjects
Subjects were 15 first-year undergraduate students (7 men and 8
women) between the ages of 21-25 (mean=22 yrs; SD=1.06) who
21
received credit for their participation in the experiment and were all
good sleepers, as assessed by the Mini Sleep Questionnaire (Zomer,
Peled & Lavie, 1985; see below). All participants spoke fluent Hebrew
and had normal or corrected-to-normal vision.
Tools
Mini Sleep Questionnaire (MSQ): Includes 10 short questions
regarding sleep quality, which are answered by choosing a number
from within a range of 1 to 5, thus classifying subjects into 3 groups:
‘good sleep’ (score between 10-24); ‘suspicion of a mild sleep disorder’
(score between 25-30); and ‘suspicion of a severe sleep disorder’
(score >30; Zomer et al., 1985).
Nicolet UltraSom system: A comprehensive computerized
polysomnographic (PSG) device by which subjects’ sleep was recorded,
using five channels: EEG, EOG and submental EMG. Data from all
channels were viewed on-screen at real time, recorded, and analyzed
by a skilled technician according to standard criteria (Rechtschaffen &
Kales, 1968).
Implicit memory task: A word-fragment completion task.
Materials: materials for the implicit memory task were 90 words in
Hebrew of 5-8 letters in length together with their corresponding
fragments (see appendix 1). The fragments were constructed such that
it would be possible to fill them correctly with more than one word, but
not with more than one target. In a previous experiment (Goshen-
Gottstein & Peres, in preparation), participants filled in these fragments
22
with the first word that came to mind, thus establishing baseline levels
of fragment completion. Only fragments that were filled with their
targets by 20%-30% of the subjects were included. The 90 original
target words were then randomly divided into two lists of equal length.
Study Phase: During the study phase, half of the participants received
the first list of targets, and the other half the second list of targets. On
these targets participants performed pleasantness judgments that are
known to yield good memory performance (Craik & Lockhart, 1972).
Each target, printed in Hebrew, size 48 David font, appeared centered
on a 15” computer screen after a 500ms fixation (+). Each target
remained on screen for five full seconds, after which it disappeared,
and only after the subject has responded the next trial began. A scale
of 1-4 (1=very unpleasant; 4=very pleasant) was continually present
on the screen. The targets were shown in random order. Participants
were not told that they would be tested on these targets the following
morning.
Test Phase: During the test phase, all participants received all 90
fragments, counterbalanced such that each participant received an
equal number of fragments corresponding to studied and unstudied
words, and across participants, each fragment corresponded equally
often to studied and unstudied words. Fragments were also printed in
Hebrew (using one underline to represent one missing letter and
separated by one space between adjacent letters), size 48 David font.
The fragments were centered on the same computer screen in the
same surroundings as of the study phase, and presented in random
23
order. Each fragment remained on screen until a key was pressed, but
no longer than thirty seconds. Consequently, the next trial began.
An implicit test was administered, thus differing from the traditional
explicit test with respect to retrieval instructions only. That is,
participants were asked to fill in the fragments (on paper) with the first
word that comes to mind.
Control task: A word-fragment completion task.
Materials: Materials for the control task were 139 fragments of
unstudied country names in Hebrew, of 3-10 letters in length (see
appendix 2). The fragments were constructed such that it would not be
possible to fill them in with more than one country name. Country
names consisting of more than one word were excluded.
During the control task, all participants received 40 of these country
fragments randomly chosen from the pool of 139. These country
fragments were also printed in Hebrew (using one underline to
represent one missing letter and separated by one space between
adjacent letters), size 48 David font. They were centered on the same
computer screen in the same surroundings as of the study and test
phases, and presented in random order. Each fragment remained on
screen until a key was pressed, but no longer than thirty seconds.
Consequently, the next trial began. Participants were instructed to fill
in the country fragments with the appropriate country name.
Design
24
Sleep condition (REM deprivation; NREM deprivation) was
manipulated within subjects. Each participant spent three nights in the
sleep lab, going through both sleep conditions after one night of
adaptation in order to avoid first-night effects. Thus, each subject
served as his/her own control. The first subject went through the first
night on Dec 28th, 1998, the last on May 22nd, 1999. The first
experimental night was performed on Jan 30th, 1999, the last on Sep
7th, 1999. The mean interval between the adaptation night and the first
experimental night was 48 days (range=33-87 days; SD=14.76). The
mean interval between the first experimental night and the second
experimental night was 93 days (range=50-134 days; SD=24.41).
Sleep condition was counterbalanced between subjects. Half were
first REM deprived and then NREM deprived, while the other half were
first NREM deprived and then REM deprived (see below).
In the REM deprivation (REMD) condition, participants were awakened
each time they entered the REM stage and were kept awake for at
least 5 min to assure that they will not go immediately back to REM
sleep. During this time, subjects were requested to report any mental
content passing through their mind just before being awakened.
In the NREM deprivation (NREMD) condition, subjects were awakened
an equal number of times as in the REM deprivation condition yet only
during NREM sleep. They were kept awake for the same period of time,
and also asked to report mental content. In the case of the NREM
condition being performed initially, the subject was awakened for the
25
same number of times as a matched subject who went through REM
deprivation first.
Memory task: All of the participants performed the implicit memory
task. The same subject cannot perform both explicit and implicit tasks
since performance of the implicit task after the explicit task would yield
contamination of the implicit memory processes by explicit/intentional
processes. Thus, a memory test condition would have to be performed
between subjects yet due to time and budget limitations this was not
possible.
Control task: All of the participants performed the control task
immediately after the implicit memory task.
Procedure
Subjects were tested individually and screened by the MSQ. The 15
best sleepers (7 best men and 8 best women) were chosen (mean
score=18;
SD=4.07) and were assigned three nights in the sleep lab (The
Institute for Fatigue and Sleep Medicine, “Sheba” Medical Center, Tel-
Hashomer, Israel).
None of the participants were informed that they were participating
in a memory experiment. Instead, they were told that they would be
taking part in an experiment on dreaming. Thus, they would be
presented with a list of words and asked to rate the extent to which the
words have subjectively pleasant or unpleasant meanings, and
26
consequently, they would be awakened several times during the night
and asked to report dreams or other mental content.
During the first adaptation night, subjects slept uninterrupted,
connected to electrodes, although their sleep was not recorded.
During the second and third nights, participants performed the study
phase upon arrival at the lab. During the study phase, each subject
received the same list of targets on both experimental nights.
Consequently, subjects were connected to the PSG electrodes and
went to sleep. During the night, the sleep condition manipulation was
carried out, and in the morning subjects performed the implicit
memory task, followed by the control task.
For all three nights, subjects chose their own sleep onset and offset
times.
Two subjects dropped out of the experiment due to technical failures.
For one subject, the PSG device failed to record his first experimental
night. For the second subject, the memory test program threw her out
during the implicit test following her third night.
Results
Sleep data
Following both experimental nights, each subject’s PSG recordings were scored for
sleep stages. That is, stages 1-4 and REM sleep. Additional variables were analyzed such
as bed-time, wake-up time, sleep latency (time from lights out to falling asleep in
27
minutes; scored automatically), number of awakenings>1min (the number of times the
subjects was awake for more than one minute after sleep onset), number of
awakenings<1min (the number of times the subjects was awake for less than one minute
after sleep onset), TST (total sleep time), sleep efficiency (TST/time in bed in
percentage), % stage-2 sleep, % SWS (stages 3-4), % REM sleep, and REM latency (in
minutes). Subsequently, paired 2-tailed t-tests were performed to check for significant
differences between the two experimental nights. Means and results are displayed in table
1 (see table 1).
SleepCondition
Bed-time(decimal)
Wake-upTime(decimal)
Sleep Latency(minutes)
Number of Awakenings>1 min
Number of Awakenings <1 min
Total SleepTime(minutes)
REMDeprivation
24.29SD=0.45
6.25SD=0.54
21.15SD=25.10
6.62SD=2.29
1.54SD=1.66
249.85SD=70.68
NREMDeprivation
24.19SD=0.74
6.32SD=0.42
14.96SD=10.77
5.92SD=2.56
3.31SD=4.92
298.65SD=66.60
tp
0.44p<.66
0.49p<.63
1.38p<.19
1.06p<.31
1.44p<.17
2.43*p<.03
SleepCondition
SleepEfficiency(%)
% Stage 2 % SlowWave Sleep
% REMSleep
REMLatency(minutes)
REMDeprivation
70.15SD=13.99
42.80SD=9.49
31.01SD=10.29
2.65SD=2.17
82.79SD=34.68
NREMDeprivation
79.82SD=8.32
40.03SD=10.45
23.73SD=2.56
19.50SD=7.21
80.83SD=32.52
tp
3.34**p<.006
1.03p<.32
2.41*p<.03
9.51**p<.000001
0.22p<.83
Table 1: Means and Results for sleep data. N=13. Significance: *p<.05; **p<.01.
As can be seen from the very significant difference of REM sleep
percentage between the two sleep conditions, it is clear that the
manipulation (REMD) was successful in depriving only one group of
REM sleep while awakening subjects for about the same number of
times during the two experimental nights. This can be seen by the
similar number of awakenings longer than one minute during both
experimental nights.
28
In addition, unforeseen significant differences were found for TST,
sleep efficiency and SWS percentage. These will be addressed in the
discussion section.
Priming data
The control task was the first to be examined. The score on this task
consisted of the number of country fragments that the subject filled in
with the appropriate country names. Percent of correct scores and
standard deviations gathered for the REMD and NREMD conditions on
the control task were 69.23%, SD=5.12; 65.78%, SD=4.63,
respectively. No significant difference was found between the two
sleep conditions using a paired t-test (t(12)=1.626; p<.13). Thus, it
seems safe to conclude that subjects were not more cognitively
fatigued following the REMD night than the NREMD night.
In order to examine the differences in performance on the implicit
test between the two experimental nights, the dependent variable was
calculated by summing separately the number of studied and
unstudied fragments that the subjects correctly completed on the
fragment completion task. That is, a fragment was considered to have
been correctly completed only when the subject filled it in with the
appropriate target. Thus, correct studied and unstudied words were
summed to give two correct scores for each subject, for each of the
experimental nights (a total of four scores for each subject).
Consequently, the unstudied score was subtracted from the studied
score to give the “amount” of priming (“priming” score) present for
29
each test/sleep condition. A positive product resulting from this
subtraction would indicate the existence of priming. Indeed, from
looking at the priming scores of each subject separately, it was found
that this pattern was displayed by all of the subjects on both sleep
conditions, meaning that learning took place following all of the study
phases. Moreover, when looking at each subject’s priming scores
following the two sleep conditions, 11 out of the 13 subjects displayed
a greater priming score following the NREMD night than following the
REMD night. A sign test was carried out on these scores and turned out
to be significant (Z=2.22; p<.027). This means that for these 11
subjects, priming was decreased following the REMD procedure.
Percent of correct scores and standard deviations for each of the
nights is displayed in table 2 (See table 2).
30
SleepCondition
Studied Unstudied Priming
REM Deprivation
47.18%SD=5.72
29.91%SD=5.22
17.27%SD=5.07
NREMDeprivation
51.62%SD=5.95
25.64%SD=4.86
25.98%SD=3.71
Table 2: Percent of correct scores on both tests for each of the experimental nights; N=13.
The unstudied score gives the “guessing” baseline relative to which
the studied score is evaluated. If, for example, no difference is found
between the studied and unstudied scores – we may conclude that no
learning has occurred. If, on the other hand, learning did take place, a
studied score that is greater that the unstudied score should manifest
this, and the difference between the two represents the “amount” of
priming that occurred during the night. In our case, we wished to
examine the difference between the priming scores of the two
experimental nights and expected to find a greater priming score for
the night of NREM deprivation. A paired t-test was performed and
indeed, this is what was found (t(12)=2.638; p<.02).
31
Discussion
This study attempted to shed light on the role played by REM sleep in
implicit memory consolidation. This was done by depriving subjects of
REM sleep and examining the consequences. This procedure is
problematic as it has various affects on the organism other than
depriving it of REM sleep (see Horne & McGrath). Therefore, the control
condition involves waking the subject up the same number of times
and for the same duration of time as in the REMD condition. According
to the sleep data of table 1 in the results section, it is obvious by
looking at the very significant difference of REM sleep percentage
between the two conditions that the manipulation (REMD) was
successful in depriving only one group of REM sleep while awakening
the subjects for about the same number of times on the two
experimental nights. Unfortunately, some variables are much more
difficult to control, such as total sleep time (TST) and sleep efficiency.
As subjects were their own controls and all good sleepers, it was
expected that their sleep would be relatively identical on both nights
outside of the experimental manipulation. Yet, although they were
awakened for about the same number of times for approximately five
minutes, it is possible (or even intuitively probable) that falling asleep
is more “difficult” or takes more time, after being awakened from REM
sleep than from SWS. The fact is that on the NREM deprivation night
subjects had more sleep, and not much could be done about it. The
32
question is, could this explain differences of performance between the
two sleep conditions on the implicit memory task? We think not. If this
were the case, we would expect to find better performance following
the NREM deprivation night than the NREM deprivation night on the
control task, but this was not the case.
The control task was designed to test whether the subjects would
show more cognitive fatigue following REM deprivation than following
NREM deprivation. No significant difference was found on this task
between the two experimental nights using a paired t-test (t(12)=1.626;
p<.13). Note that performance on the control task following the night
of REM deprivation was better than that following NREM deprivation.
This makes it safe to say that the inferior performance on the implicit
memory task following REM deprivation was not due to greater fatigue
following that night. In addition, similar to the findings on the control
task, the percentage of correct responses on the unstudied words
following REM deprivation was also higher than that following NREM
deprivation, thus supporting the claim that subjects were not more
exhausted and/or worn-out following REM deprivation.
Could the significant difference found for the percentage of SWS
between the two nights explain the lower priming scores following REM
deprivation? If so, we would need to ask whether it is reasonable that
the more SWS subjects had - the worse they performed on the implicit
task. Such a claim would mean that SWS disrupts learning, and does
not seem probable.
33
Hence, it appears that as hypothesized, REM sleep does play a role in
the consolidation of implicit memory traces. However, it is interesting
to note that REM deprivation does not totally abolish this process of
consolidation, as can be seen by the existence of some degree of
priming following the REMD condition. Nonetheless, these results
strongly suggest that newly acquired memories are susceptible to
further elaboration during REM sleep. Furthermore, these results
indicate that information-processing abilities exist during REM sleep
and that what is processed during REM sleep can be transferred to the
waking state and can find behavioral expression.
It would have been preferred to include an explicit condition in this
experiment, yet as was already mentioned this was not possible.
However, these stimuli have already been used in an experiment
including both memory conditions (Goshen-Gottstein & Peres, in
preparation), and have yielded the classical dissociation between
explicit and implicit performance. Therefore, it is quite safe to assume
that the memory task employed in this study was an implicit memory
task.
In conclusion, it is clear that the role played by REM sleep in memory
consolidation is far from being clear. The mechanisms by which REM
sleep can modulate newly acquired memories are still not understood,
as well as further questions regarding the characteristics of the task,
the span of time during which REM sleep can play a role and the nature
of the organism performing the task. Addition research is necessary in
order to expand out knowledge of this intriguing phenomenon.
34
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