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

12

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).

13

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.

17

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.

18

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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