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Sleep. 2008 February 1; 31(2): 197–203. | PMCID: PMC2225575 |
Copyright © 2008 Associated Professional Sleep Societies, LLC. Enhancement of Declarative Memory Performance Following a Daytime Nap
Is Contingent on Strength of Initial Task Acquisition Matthew A. Tucker, PhD and William Fishbein, PhD Laboratory of Cognitive Neuroscience and Sleep, Department of Psychology, Program in Cognitive Neuroscience, The City College of the City University of New York, New York, NY Received April 2007; Accepted October 2007. Study Objectives: In this study we examined the benefit of a daytime nap containing only NREM
sleep on the performance of three declarative memory tasks: unrelated paired
associates, maze learning, and the Rey-Osterrieth complex figure.
Additionally, we explored the impact of factors related to task acquisition
on sleep-related memory processing. To this end, we examined whether testing
of paired associates during training leads to sleep-related enhancement of
memory compared to simply learning the word pairs without test. We also
examined whether strength of task acquisition modulates sleep-related
processing for each of the three tasks. Subjects and Procedure: Subjects (11 male, 22 female) arrived at 11:30, were trained on each of the
declarative memory tasks at 12:15, and at 13:00 either took a nap or
remained awake in the sleep lab. After the nap period, all subjects remained
in the lab until retest at 16:00. Results: Compared to subjects who stayed awake during the training-retest interval,
subjects who took a NREM nap demonstrated enhanced performance for word
pairs that were tested during training, but not for untested word pairs. For
each of the three declarative memory tasks, we observed a sleep-dependent
performance benefit only for subjects that most strongly acquired the tasks
during the training session. Conclusions: NREM sleep obtained during a daytime nap benefits declarative memory
performance, with these benefits being intimately tied to how well subjects
acquire the tasks and the way in which the information is acquired. Citation: Tucker MA; Fishbein W. Enhancement of declarative memory performance
following a daytime nap is contingent on strength of initial task
acquisition. SLEEP 2008;31(2):197–203. Keywords: Sleep, nap, declarative, memory, NREM sleep, slow wave sleep IT IS BECOMING INCREASINGLY CLEAR THAT NREM SLEEP, ESPECIALLY SLOW WAVE SLEEP (SWS), IS
IMPORTANT FOR THE PROCESSING OF HIPPOCAMPUS-dependent declarative memories, 1–6 with SWS hypothesized to provide the optimal electrophysiological
and biochemical state for this type of processing. 7,8 When sleep occurs in the
form of a short daytime nap, it is very common to obtain only NREM sleep, without
entering REM sleep, which would usually occur at least 90 minutes into the sleep period.
The few studies examining the effect of daytime naps on memory have made use of this
knowledge, demonstrating that daytime naps containing only NREM sleep (including SWS)
facilitate verbal declarative memory (semantically related paired associates), 9 with one study showing that paired associates improvement is contingent on
whether subjects obtained SWS during the nap. 10 These findings represent a first step forward in our understanding of how daytime
naps benefit declarative memory processing. However, there are many questions still to
be explored. To this end, the present study examines the benefits of a daytime NREM nap
on a spectrum of declarative memory tasks, and begins to assess the importance of
factors related to task acquisition and their potential to modulate sleep-related memory
processing. To more broadly assess the declarative memory benefits of NREM sleep obtained during a
daytime nap, subjects were trained on 3 well-known declarative (hippocampus-dependent)
memory tasks. The first task was an unrelated paired associates task, a more difficult
counterpart to the commonly used related paired associates task. 3,4
The task comprises pairs of common words that lack an inherent semantic relationship
(e.g., shirt–paper). Two nonverbal declarative memory tasks that do not rely
strongly on previously learned concepts were also evaluated: the Rey-Osterrieth complex
figure test (ROCFT; a measure of visuospatial declarative memory) and a maze learning
task adapted from the task used by Brenda Milner on a large sample of hippocampal lesion
patients including HM. 11 Both of these tasks are void of semantically charged landmarks, objects, or
verbal material that would have been previously learned by subjects. To date, no studies
have used this particular maze learning task, and only 2 have examined the effect of
sleep on memory using the ROCFT. In epileptic patients it was shown that performance on
the ROCFT correlated positively with low frequency EEG spectral power (<1.25 Hz) overnight, 12 and in schizophrenic patients the amount of SWS correlated positively with
overnight ROCFT performance. 13In the present study we also explored the extent to which different methods of
information encoding modulate the effect of sleep on memory. The impetus for exploring
encoding factors was based on two studies by Smith, et al. 14,15 who found
that only when rats successfully acquired an operant conditioning or passive avoidance
task was there an increase in subsequent paradoxical sleep. These findings suggested for
the first time that the extent of task acquisition may be an important modulator of the
effect of sleep on memory processing. Support for this general finding comes from a
recent PET study demonstrating that the strength of acquisition of a serial reaction
time task is correlated with increased brain activation (regional cerebral blood flow)
during post-acquisition REM sleep. 16 Similarly, it was shown that stronger acquisition of a motor adaptation task not
only correlates with an increase in slow wave activity (SWA) during subsequent sleep,
but this increase in SWA is correlated with enhanced performance following sleep. 17 Given these findings, it becomes clear that the individual's success in
acquiring a task may be an important factor in understanding how sleep facilitates
memory formation. In addition to the assessment of individual differences in acquisition, the level of task
acquisition can be experimentally manipulated to assess the preferential effect of sleep
for information that is more strongly acquired. A recent study by Schmidt et al. 18 has shown that not only does spindle density increase significantly during a
daytime nap following the encoding of a difficult (but not an easy) paired associates
task, but that this increase in spindle density correlates with improvement in paired
associates recall. To assess the importance of task acquisition in modulating sleep-related memory
processing, we created 2 encoding conditions within the paired associates task. To date,
almost all sleep-dependent consolidation studies have employed a
“study-test” paradigm, 19 whereby subjects learn a list of word pairs, and then perform cued recall tests
until a specified performance criterion is met (e.g., 60% correct or one
perfect recall trial 2,3,20). However, it
is still unclear whether immediate testing leads to enhanced paired associates encoding,
which in turn allows sleep to more strongly facilitate memory processing, or whether
sleep imparts the same performance benefits to subjects that simply learn the word pairs
without immediate testing. Interestingly, in a recent study that did not examine
sleep/wake differences it was shown that when subjects were tested immediately after
learning declarative information (a text passage), recall after one week was superior to
recall of subjects that underwent multiple study sessions without being tested. 19 To add to our understanding of the nature of task acquisition and its potential
to modulate the effects of sleep on memory, subjects in the present study were
immediately tested on a subset of the word pairs during the training session (referred
to as “tested” word pairs), while the remaining word pairs were
studied without immediate test (referred to as “untested” word
pairs). In the present study, performance on all 3 declarative tasks was assessed following a
3.5-h training-retest interval that included a daytime NREM nap or no nap. To test the
extent to which task acquisition factors modulate sleep-related memory processing,
subjects were not only exposed to 2 modes of paired associates encoding, but for each
task subjects were also divided post hoc into high and low performers based on training
performance (i.e., those performing in the top and bottom half of the sample based on a
median split). This allowed for an analysis of the effect of the subjects'
ability to acquire each of the 3 tasks as well as the effect of 2 different modes of
paired associates acquisition (tested vs. untested) on sleep-related memory processing. Subjects A sample of 39 undergraduate students of diverse ethnic composition participated
in the study. Six of the original 39 subjects were excluded from statistical
analysis because they either did not obtain SWS (n = 3), they entered
REM sleep (n = 2), or did not sleep during the nap period (n
= 1). From the final sample of 33 subjects (11 males, 22 females,
mean age = 23.3 y), 16 subjects were assigned to the nap condition
and 17 to the no-nap condition. All subjects were medication free and abstained
from caffeine and alcohol 24 h prior to participation. A sleep log was obtained
from all subjects indicating bedtime, wake time, and total sleep time for the 3
nights prior to the study. All subjects were paid for their participation. Procedure Subjects arrived at the sleep laboratory at 11:30 (). Between 11:30 and 12:00 subjects were shown the
laboratory sleep chambers, signed the consent form, and completed a demographic
information form. At 12:00, 9 electrodes were applied to record sleep, including
central electroencephalography (EEG; C3-A2 and C4-A1), electro-oculography
(EOG), and chin electromyography (EMG). To create similar experimental
conditions, all subjects, including no-nap subjects, had the same 9 electrodes
applied, and subjects were not informed of group assignment (nap or no-nap)
until after the training session. Subjects trained on the 3 declarative memory
tasks at a computer in sound-attenuated rooms from 12:15 to 12:45. The order of
task presentation was fully counterbalanced across subjects. After the training
session, subjects were assigned to the nap or no-nap group. At 13:00, nap
subjects entered individual sleep chambers to take a nap. At the same time,
no-nap subjects entered other sleep chambers and sat quietly for a period of 10
to 12 minutes, a time period comparable to that experienced by nap subjects
prior to sleep onset. This condition was imposed primarily to address the issue
of rehearsal of information that might occur with nap subjects prior to sleep
onset. After this 10 to 12 min-period, no-nap subjects were taken to a separate
room to watch a television program (e.g., an episode of Seinfeld) until nap
subjects joined them at approximately 14:00. Nap subjects attempted to sleep for
a period of approximately one hour. No subjects were awakened from SWS. After
the sleep period, nap subjects joined the no-nap subjects to watch a movie until
the retest session at 16:00. At 16:00, all subjects were retested on the same 3
tasks presented in the same order as during the training session. Sleep data for the nap group are presented in Table 1. Sleep log data revealed no differences between nap and
no-nap subjects in amount of time awake prior to the study (P =
0.47), total sleep time the night before the study (P = 0.28), and
average total sleep time for the 3 nights prior to the study, (P =
0.17) ( Table 2). Tasks
Semantically Unrelated Paired Associates
Sixty word pairs were created from common objects (e.g.,
“alligator” and “cigar”), and
were randomly paired to eliminate semantic relationships between the pairs.
Subjects were instructed to visualize the 2 words interacting with each
other, such that, in the case of
“alligator–cigar” they might imagine an
alligator smoking a cigar. Each word pair was presented serially for 2
seconds with a 100 ms interval between word pairs. All word pairs were
presented in Times New Roman font (font size = 54). After
presentation of all word pairs, subjects completed a cued recall test,
during which they were presented the stimulus (first) word of 20 of the word
pairs (randomly selected from the 60 presented pairs), and were asked to
type the target word that completed the word pair. No feedback about whether
each answer was correct or incorrect was given after subjects entered each
response during the cued recall test. After completion of the 20 tested word
pairs subjects viewed all 60 word pairs once more, this time presented each
for one second, with a 100 ms interval. At retest subjects were shown, in
random order, the stimulus words for all 60 word pairs, and were asked to
recall as many of the target words as possible.
Maze Learning Task
The maze task is a computerized version of the “bolt head
maze” used by Brenda Milner with the patient HM and a large
sample of hippocampal lesion patients. 11 Our maze is a 13x13 array of squares, with each square representing
either a correct step in the path of the maze, or a wall. Subjects start at
the “start” button in the lower left hand corner and
move left-right or up-down (but not diagonally) clicking each square with a
mouse. If a subject is on the correct path, each square lights up green. If
the subject hits a “wall” the square lights up orange.
With each forward mouse click the preceding square returns to its original
gray color. The first time through the maze subjects progress blindly from
start to finish, but with each subsequent trial, subjects commit more of the
path to memory. The maze program displays the time and the number of errors
per trial. During the training session subjects completed 5 maze trials,
recording on a response sheet the trial time and number of errors at the end
of each trial. At retest subjects completed 8 maze trials. The number of
maze trials at training and retest was based on a pilot study showing that 5
training trials produced substantial learning (subjects improved by
approximately 38 errors from the first to last training trial) without
reaching plateau, while 8 trials at retest allowed for a more exhaustive
assessment of memory.
Rey-Osterrieth Complex Figure Test
The Rey-Osterrieth complex figure test (ROCFT) is a standard
neuropsychological test used primarily as a clinical assessment tool to
screen for brain injury that also measures visuospatial integration capacity
and short-term visual memory. In this study subjects were presented the
complex figure and were given 5 min to copy the entire figure onto a blank
sheet of paper. If subjects finished copying the figure before the allotted
time they were instructed to go over their work for the remainder of the
time. At retest, subjects were again given 5 min to copy the figure from
memory. Administration of the ROCFT differed from traditional methods in
that recall was assessed approximately 3.5 h after the baseline session
(instead of the usual 20-min interval), and all subjects were informed that
that they would be retested on the figure later in the day. Scoring of the
complex figure was based on a modified version of the Boston Qualitative
Scoring System (BQSS), 21 such that the 6 configural elements, 9 clusters, and 6 details were
given a 0, 0.5, or 1 point score. Zero was scored if less that half of the
element was represented, or if orientation and position criteria were
violated. A score of 0.5 was given if greater than 50% but less
that 100% of the element was represented or if only orientation
or position was violated. One point was given if 100% of the part
was represented and orientation and position criteria were met. A total of
21 points could be obtained on this task. Entire Sample
Unrelated Paired Associates
As expected, the number of tested word pairs recalled following the training
session was similar for nap and no-nap subjects (nap group: 7.4 ±
0.8, no-nap group: 9.5 ± 1.3 (mean ± SEM,
t31 = 1.31, P = 0.2).
At retest, when high and low performing subjects were combined, recall of
tested word pairs was shown to improve significantly from baseline training
to retest for the nap group (+1.6 ± 0.7,
t15 = 2.23, P = 0.04),
and this recall enhancement was significantly greater than no-nap subjects,
whose recall actually decreased compared to their baseline training
performance (−0.3 ± 0.4; sleep group (nap vs. no-nap)
by time (training vs. retest) interaction, F1,31
= 5.26, P = 0.03) (). For the 40 untested word pairs, the same 2x2 ANOVA
could not be conducted, because subjects were not tested on these word pairs
during training, only at retest. Therefore, we conducted an analysis of
covariance, using training performance on the tested word pairs as a
covariate, which revealed no difference in recall between nap and no-nap
subjects at retest, (nap group: 8.6 ± 1.1, no-nap group: 9.2
± 1.8, one-way ANCOVA, F1,30
= 1.60, P >0.2) ().
Maze Learning
The nap and no-nap group performed similarly during baseline training for
number of errors committed per trial (nap group: 39.2 ± 5.3,
no-nap group: 31.3 ± 4.3, t31
= 1.17, P >0.2) and average time to complete each trial
(nap group: 103.0 ± 9.6 seconds, no-nap group: 90.9 ±
8.3 seconds, t31 = 0.96, P
>0.3). Both groups improved significantly from training to retest for
reduction in errors and for average time to complete each trial (all paired
samples t-tests for the nap and no-nap group, P
<0.001). When high and low performing subjects were combined, nap
subjects demonstrated a nonsignificant 39% greater reduction in
errors and a 33% greater reduction in time to complete the maze
trials compared to no-nap subjects (error reduction: nap group: 16.8
± 3.8, no-nap group: 12.1 ± 2.5, sleep group by time
interaction F1,31 = 1.13, P
= 0.30; time improvement (seconds); nap group: 33.9 ±
7.1, no-nap group: 25.4 ± 5.4, sleep group by time interaction
F1,31 = 1.06, P =
0.31).
Complex Figure Test
During baseline training all subjects copied every detail (100%)
of the complex figure within the 5-min time limit, except 3 who were
excluded from this analysis. When high and low performers were combined, nap
and no-nap subjects accurately recalled a similar number of complex figure
elements (nap group: 14.8 ± 1.11, no-nap group: 13.7 ±
0.82; t28 = 0.75, P >
0.4). Entire Sample Divided into High and Low Performers
Unrelated Paired Associates
The sample was divided into 2 groups: subjects that performed in the top half
(high performers), and subjects performing in the bottom half (low
performers) of the sample based on a median split of recall of the 20 tested
word pairs during the training session. Within the group of high performers,
nap subjects demonstrated enhanced recall of the tested word pairs compared
their waking counterparts (nap group [n =
9]: 1.7 ± 1.0, no-nap group [n =
8]: −1.3 ± 0.6; sleep group by time
interaction, F1,15 = 5.66, P
= 0.03; a), while
sleep had no facilitating effect on recall for subjects in the low
performing group (nap group [n = 7], no-nap
group [n = 9]; sleep group by time
interaction, P >0.4). Within the high performing group the percentage
of SWS obtained during the nap correlated positively with paired associates
performance (r = 0.63, P = 0.06; ), while the correlation was negative for the
low performers (r = −0.12).
Maze Learning
High performing nap subjects (i.e., subjects performing in the top half of
the sample based on a median split for number of errors committed per trial
during the training session) demonstrated greater improvement at retest than
subjects in the high performing no-nap group for reduction in number of
errors committed (nap group [n = 8]: 12.1
± 1.3, no-nap group [n = 8]: 6.8
± 1.0; sleep group by time interaction,
F1,14 = 10.81, P =
0.005; b) and improvement in
time to complete each trial (nap group [n =
8]: 22.4 ± 2.5, no-nap group [n
= 8]: 11.8 ± 3.5; sleep group by time
interaction, F1,14 = 6.03, P
<0.03). For the low performers (nap group [n =
8], no-nap group [n = 9]), sleep
subjects did not improve more than their waking counterparts on both
performance measures (sleep group by time interactions, P >0.5).
Complex Figure Test
When the sample was divided into high and low performers based on a median
split of the number of elements recalled at retest, high performing nap
subjects recalled significantly more of the complex figure than high
performing no-nap subjects (nap group [n =
8]: 17.9 ± 0.40, no-nap group [n
= 7]: 16.6 ± 0.47;
t13 = 2.14, P = 0.05;
c). Recall in the low
performing nap (n = 8) and no-nap group (n = 9) was
similar, P >0.9.
Analysis of Task Specificity for Each High Performing
Group
Sleep-related memory enhancement within high performing groups was
task-specific (i.e., there was not a single group of high performing
individuals demonstrating sleep-related enhancement across all 3 tasks).
Independent samples t-test revealed that, while each group
of high performers showed a clear sleep-related performance benefit for the
specific task which they performed well on, these benefits did not transfer
to the other 2 tasks (P >0.18 for all comparisons), except for high
performers on the ROCFT who also showed a sleep-dependent performance on the
paired associates task (P = 0.03). Studies have shown that recall of semantically related word pairs (e.g., Clock-Hands)
following a period of sleep is greater than when recall follows an equivalent period
of wakefulness. 3,9 The present study extends this general finding by
examining the benefit of a brief (~45 min) NREM-only daytime nap on unrelated paired
associates performance. Consistent with previous studies that employ a study-test
paradigm, we observed sleep-dependent enhancement of recall of the tested word
pairs. In contrast to tested word pair performance, performance on the untested word
pairs was similar between nap and no-nap subjects at retest. In response to this
intriguing finding, we proffer the hypothesis that a test session immediately
following the learning of this hippocampus-dependent task serves to more effectively
prime relevant hippocampal and neocortical networks for subsequent sleep-dependent
information processing. While the neurophysiological mechanisms of underlying this sleep-dependent memory
enhancement are not fully understood, theories of sleep-related memory consolidation
clearly suggest that the electrophysiological and biochemical brain state produced
during NREM sleep should be an optimal time for declarative memory
consolidation. 7,8 Buzsaki suggests that a
“hippocampo-neocortical dialog” occurs primarily during SWS to
strengthen the memory trace, with the hippocampus generating spontaneous sharp
wave-ripple (SPW-R) complexes believed to provide efferent potentiation of cortical
targets activated during information encoding. 22 Acetylcholine levels, which are at their lowest during SWS, have also been
shown to be necessary for optimal declarative memory processing. 4,23Following from this physiological model of sleep-dependent memory consolidation, one
implication of the study-test method would be that hippocampal and neocortical
networks activated during presentation of the word pairs are reactivated during
immediate recall during the training session, which better primes these networks for
subsequent NREM sleep-related processing. Indeed, a number of imaging studies reveal
that localized cortical regions (especially inferior prefrontal cortex) activated
during the encoding of word stimuli 24,25 are reactivated
during immediate retrieval, 26–28
possibly strengthening the initially activated cortical circuits. Conversely, if
word pairs are untested, sleep-related facilitation of performance would not be
expected, because relevant, learning-related hippocampal/neocortical networks would
not have been adequately activated for subsequent sleep-related memory processing.
While this notion remains speculative, it is concordant with the current findings,
as well as existing hypotheses regarding the physiological basis of sleep-dependent
memory processing. Examining the sample as a whole, we found that the nap and no-nap group performed
similarly on the nonverbal declarative memory tasks (ROCFT and maze learning), which
was unexpected given the fact that declarative memory tasks have been shown
consistently to benefit more after periods of NREM sleep compared to equivalent
periods of wakefulness, 3,9,29 and that performance on declarative tasks has been correlated with
SWS-related hippocampal activity. 5,6 However, one doesn't have
to look far to see that this finding is clearly related to how well subjects
performed the tasks during the training session. For each task, nap subjects that
performed in the top half of the sample during training showed clear sleep-dependent
performance benefits compared to their non-napping counterparts, whereas a
similarity of performance was observed between nap and no-nap subjects in the low
performing groups. One possible interpretation of this important finding is that
subjects that demonstrate greater facility to learn each of the tasks are better
equipped physiologically to benefit from sleep-related mnemonic processes. Indeed,
strong positive associations are beginning to emerge between general measures of
aptitude (e.g., Raven's Advanced Progressive Matrices and the
Multidimensional Aptitude Battery) and sleep-related events such as stage 2 spindle
count 30,31 and number of rapid eye movements. 30 In a related vein, two studies have shown that fast learning rats show
increased REM sleep following successful acquisition of a shuttle avoidance task 14 and an operant conditioning task. 15 These findings suggest that there may be inherent physiological differences
between subjects that may in part determine whether sleep will confer greater
performance benefits. It is relevant to note here that even though the beneficial effect of a daytime nap
on paired associates recall was shown for the entire sample, when subjects were
divided into high and low performers, as with the nonverbal declarative tasks, we
found that the strength of this overall effect is also concentrated in the
difference between high performing nap and no-nap subjects, while we found no
difference in recall performance for the low performing nap and no-nap subjects. Not
only do high performers benefit more from sleep than their non-napping counterparts,
but this performance gain is correlated with percentage of SWS obtained during the
nap, strengthening the general finding that SWS-related processes make a unique
contribution to memory processing of verbal declarative memory tasks. In summary, the present study demonstrates that a brief bout of NREM sleep (~45 min)
obtained during a daytime nap facilitates memory processing for unrelated paired
associates, and that this enhanced performance is tied to how the word pairs were
learned (i.e., whether they were tested or untested during the training session).
Results for all three declarative memory tasks demonstrate that sleep-dependent
performance enhancement following a daytime nap depends on how well subjects acquire
the tasks during the training session. We would suggest that the findings of the
present study, in combination with findings from previous studies, begin to make a
case that not only does sleep play a special role in memory processing, but that the
benefits of sleep are clearly modulated (across multiple declarative memory tasks)
by the strength with which information is initially acquired. We are grateful for the insightful comments and suggestions provided by Robert
Stickgold, Jessica Payne, and Erin Wamsley at the Center for Sleep and Cognition,
Department of Psychiatry, Harvard Medical School. Special thanks to Rebecca Emery
for programming the maze learning task, and to Barbara Hadrysiewicz for technical
assistance. This research was funded by PSC-CUNY grant# 67648-00 36 to
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