Content uploaded by Sara Mednick
Author content
All content in this area was uploaded by Sara Mednick
Content may be subject to copyright.
REM, not incubation, improves creativity
by priming associative networks
Denise J. Cai
a
, Sarnoff A. Mednick
b
, Elizabeth M. Harrison
a
, Jennifer C. Kanady
c
, and Sara C. Mednick
c,1
Department of aPsychology, University of California at San Diego, La Jolla, CA 92037; bDepartment of Psychology, University of Southern California,
Los Angeles, CA 90033; and cDepartment of Psychiatry, University of California at San Diego, La Jolla, CA 92093
Edited by Thomas D. Albright, Salk Institute for Biological Studies, La Jolla, CA, and approved May 4, 2009 (received for review January 13, 2009)
The hypothesized role of rapid eye movement (REM) sleep, which
is rich in dreams, in the formation of new associations, has
remained anecdotal. We examined the role of REM on creative
problem solving, with the Remote Associates Test (RAT). Using a
nap paradigm, we manipulated various conditions of prior expo-
sure to elements of a creative problem. Compared with quiet rest
and non-REM sleep, REM enhanced the formation of associative
networks and the integration of unassociated information. Fur-
thermore, these REM sleep benefits were not the result of an
improved memory for the primed items. This study shows that
compared with quiet rest and non-REM sleep, REM enhances the
integration of unassociated information for creative problem solv-
ing, a process, we hypothesize, that is facilitated by cholinergic and
noradrenergic neuromodulation during REM sleep.
human 兩implicit 兩memory 兩remote-associates 兩sleep
The night before Easter Sunday of that year I awoke,
turned on the light, and jotted down a few notes on a tiny
slip of paper. Then I fell asleep again. It occurred to me
at 6 o’clock in the morning that during the night I had
written down something most important, but I was
unable to decipher the scrawl. The next night, at 3
o’clock, the idea returned. It was the design of an
experiment to determine whether or not the hypothesis
of chemical transmission that I had uttered 17 years ago
was correct. I got up immediately, went to the labora-
tory, and performed a single experiment on a frog’s
heart according to the nocturnal design.
Otto Loewi, 1938 German, Nobel laureate for his work on
the chemical transmission of nerve impulses.
Creativity has been defined as ‘‘the forming of associative
elements into new combinations which either meet specified
requirements or are in some way useful’’ (1). It has been further
proposed that creative problem solving is reached in four
successive phases: first, intense but unsuccessful confrontations
with the elements of the problem; second, a decision to put the
problem aside; third, a dormant period with no further conscious
work on the problem, e.g., incubation; and finally, a ‘‘flash of
insight’’ in which the solution suddenly enters consciousness
while the individual is dreaming or engaged in idle thought
(2–4). Evidence for the role of these phases in creative problem
solving (e.g., a dormant period or incubation), however, is
inconsistent (5–7). Yet, it has been long hypothesized that
creative problem solving is enhanced by states of mind, such as
sleep or quiet reflection, which foster insights. Furthermore,
several famous anecdotes attribute creative revelations to
dreaming in particular, ranging from musical compositions to
insightful advances in scientific discovery (8).
Evidence for the role of sleep in creative problem solving has
been suggested by prior research, but the most critical questions
about this effect remain unanswered. First, sleep appears to
enhance creative and associative memory processing compared
with wake, but the underlying mechanisms, such as sleep stages,
have not been explored (9–12). The seminal article by Wagner
and colleagues (12) suggested that sleep might facilitate ‘‘cog-
nitive flexibility’’ and lead to increased occurrences of insight;
however, information about the operative sleep stage was not
provided. Second, no study has demonstrated that R EM [a
potentially more facilitative state of mind than non-REM
(NREM)] enhances creativity more than wake, NREM, or
simply the passage of time (i.e., incubation) (13, 14). Circadian
confounds in the timing of testing periods may be a possible
reason for the lack of difference between the REM group and
wake controls. Last, although these studies suggest that exposure
to the elements of a problem before sleep is necessary for insights
to occur, they do not successfully distinguish between improved
memory and enhanced creative processing as the cause of better
performance on these associative tasks (15). In conclusion, prior
studies suggest that sleep, particularly REM, may enhance the
formation of associative networks and the integration of unas-
sociated information, but no study to date has shown REM to
enhance creative processing directly more than any other sleep
or wake state. The present study (i) directly compared REM,
NREM, and wake controls while using a nap paradigm to control
for circadian effects, and (ii) probed contributions of both
memory and associative processing in creative problem solving.
We compared incubation and sleep on three forms of prior
exposure to the elements of a creative problem (repeated
exposure, no exposure, or priming) on the Remote Associates
Test (RAT) (Fig. 1). Using a nap paradigm allowed us specifi-
cally to compare sleep with or without REM with incubation. In
the creativity task (RAT), subjects are required to produce a
word that is associated with three test words that are seemingly
unrelated to each other (1). The exposure conditions were
designed to access three different methods for creative problem
solving. First, the repeated-exposure condition examined the
role of incubation on creative problem solving. Second, the
priming condition examined whether stimulation of information
nodes by an unrelated source can increase solutions to creative
problems. Last, the no-exposure condition examined whether
general creative problem solving can be enhanced with repeti-
tion of the same type of task.
We hypothesized that: (i) incubation alone would increase
creative associations in the repeated condition; (ii) sleep, spe-
cifically REM, is required for associating information primed in
an unrelated task to the solutions for a creativity task; and (iii)
creative problem solving requires prior exposure to problem-
related information, such that no benefit would be seen for items
in the no-exposure condition. To reduce interference effects that
occur during normal waking, a quiet rest group with EEG moni-
toring was used instead of uncontrolled wake or sleep deprivation
groups.
Author contributions: D.J.C., S.A.M., and S.C.M. designed research; D.J.C., E.M.H., and J.C.K.
performed research; D.J.C. and S.C.M. analyzed data; and D.J.C., S.A.M., E.M.H., J.C.K., and
S.C.M. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
1To whom correspondence should be addressed at: University of California at San Diego,
Laboratory of Sleep and Behavioral Neuroscience, Department of Psychiatry, 9116a, 9500
Gilman Drive, La Jolla, CA 92093. E-mail: smednick@ucsd.edu.
10130–10134
兩
PNAS
兩
June 23, 2009
兩
vol. 106
兩
no. 25 www.pnas.org兾cgi兾doi兾10.1073兾pnas.0900271106
Results
Incubation-Dependent Improvements in Performance Are Indepen-
dent of Sleep. Subjects were first tested on the RAT at 9 AM and
retested at 5 PM. To compare sleep and the passage of time,
subjects were administered the same RAT in both the morning
and afternoon sessions. No differences were found between
groups (P⫽0.67, 1-way ANOVA) (Fig. 2), and post hoc analysis
showed that all three groups, NREM sleep, R EM sleep, and
quiet rest, improved similarly on the repeated items compared
with the morning baseline performance [confidence inter val
(CI) 95%, 6.5–38.3%; CI 95%, 10.6–50.2%; and CI 95%, 2.4–
71.0% for the REM, NREM, and rest groups, respectively].
These results indicate that passage of time (i.e., incubation) was
sufficient to increase creative problem solving. This is consistent
with the theory of incubation in which solutions to problems will
emerge spontaneously after not actively working on the problem
for some time (i.e., allowing the problem to incubate) (16).
REM Sleep, Not Incubation nor NREM Sleep, Improved Solutions After
Priming. We tested whether priming of associative networks
would improve creative problem solving with the primed items
and whether REM sleep would enhance this effect compared
with NREM sleep or quiet rest. After the morning RAT,
subjects completed a set of analogies (e.g., CHIPS: SALT Y;
CANDY: S㛭㛭㛭) in which half of the answers (e.g., SWEET) were
also the answers to the afternoon RAT items (e.g., HEART,
SIXTEEN, COOKIES; answer: SWEET).
In contrast to the incubation results, subjects that had REM
sleep displayed a significant improvement above NREM sleep
and quiet rest groups (Fig. 3; P⫽0.04, 1-way ANOVA and post
hoc analysis). Strikingly, although the quiet rest and NREM
sleep groups received the same priming, they displayed no
improvement on the primed RAT items, whereas the R EM sleep
group improved by almost 40% above the morning performance.
Although naps with R EM typically had longer total sleep time
(TST) (see Table 1), surprisingly, TST was not correlated with
performance on the primed R AT items (r⫽.104, P⫽0.53, Fig.
4). We also separated subjects by their TST with a median split
of the data and compared low TST with high TST on the priming
results, which was nonsignificant (t⫽1.4, P⫽0.17). Thus, it is
unlikely that the REM results were the result of TST differences
in the nap. Consistent with previous studies reporting a benefit
Fig. 1. Experimental design. Subjects were administered the creative prob-
lem solving test in the morning and then a word analogy priming task. After
an intervening polysomnographically recorded sleep or quiet rest period,
subjects were tested on the three prior exposure conditions: repeated expo-
sure (white box), primed exposure (gray box), or no exposure (black box).
Memory tests for the analogy solutions followed.
Fig. 2. Incubation-dependent improvements in performance are indepen-
dent of sleep. NREM sleep, REM sleep, and quiet rest similarly improved
performance on the repeat items compared with the morning baseline per-
formance (CI 95%, 6.5–38.3%; CI 95%, 10.6 –50.2%; and CI 95%, 2.4–71.0% for
the REM, NREM, and rest groups, respectively).
Fig. 3. REM sleep facilitates the use of prior information for creative
problem solving. Subjects who had REM sleep displayed a significant
improvement above NREM and quiet rest groups (P⫽0.047, 1-way ANOVA
and post hoc analysis). Strikingly, although the quiet rest and NREM nap
groups received the same priming, they displayed no improvement on the
primed RAT items, whereas the REM group improved by almost 40% above
the morning performance.
Table 1. Sleep statistics comparing REM and NREM naps
Sleep type NREM group REM group
Total sleep time* 50.2 (⫾4.2) 72.9 (⫾2.9)
Stage 1, NS 5.4 (⫾1.4) 3.9 (⫾1.0)
Stage 2, NS 24.6 (⫾3.0) 31.4 (⫾2.0)
SWS, NS 20.0 (⫾4.2) 23.3 (⫾2.8)
REM* 0.2 (⫾2.3) 14.3 (⫾1.6)
Results are shown as mean (⫾SEM). *,P⬍0.001; NS, not significant.
Cai et al. PNAS
兩
June 23, 2009
兩
vol. 106
兩
no. 25
兩
10131
NEUROSCIENCEPSYCHOLOGY
of sleep on cognition (17–20), we find that it was not the quantity
(i.e., TST), but the quality (i.e., specific sleep stages) that led to
improved performance. These results suggest that REM en-
hanced the formation of associative networks and the integration
of unassociated information, compared with quiet rest and
NREM sleep.
Creative Problem Solving Requires Prior Exposure. Because daytime
sleep has been shown to increase alertness and improve a range
of cognitive functions (perceptual, verbal, and motor learning;
declarative and implicit memory) (18, 21–24), we tested whether
sleep or quiet rest might enhance general creativity on new RAT
items. Baseline assessments were measured on the morning
RAT. In the PM session, subjects were tested on new RAT items.
Surprisingly, no group (NREM, R EM, quiet rest) differences
were found on the new RAT items (P⫽0.261 1-way ANOVA)
(Fig. 5), and no improvement in PM performance above baseline
was observed in the three groups (CI 95%, ⫺13.0 to 41.2%; CI
95%, ⫺16.0 to 35.4%; and CI 95%, ⫺15.4 to 51.0% for the REM,
NREM, and rest groups, respectively). Although daytime sleep
has been shown to improve performance on some cognitive tasks
and to increase alertness and restore homeostatic drive, neither
NREM nor REM sleep improved general creative problem
solving in the absence of prior exposure (e.g., priming).
REM Improvements in Creative Problem Solving Are Not Caused by
Improved Memory. Previous studies have shown that sleep facil-
itates the retention of declarative memories (25–27). We, there-
fore, examined whether enhancement on the RAT items after
priming and REM sleep was caused by memory of the answers
in the priming task. To address memory, recognition and cued
recall were assessed for answers to the morning analogies during
the afternoon session. The process dissociation procedure (28)
was also used to investigate how sleep may act on implicit and
explicit memory processes.
Surprisingly, yet consistent with the incubation findings, no
difference was observed among the three groups (NREM,
REM, and quiet rest) for any of the memory measures, including
recognition (P⫽0.283, 1-way ANOVA), cued recall (P⫽0.353,
1-way ANOVA), explicit (P⫽0.435, 1-way ANOVA), and
implicit (P⫽0.229, 1-way ANOVA). Interestingly, all three
groups (rest, NREM naps, R EM naps) had ⬎90% correct on the
recognition test, suggesting that all groups formed memories of
the answers from the morning analogies, i.e., priming. NREM
sleep, REM sleep, and quiet rest groups were indistinguishable
on the memory measures [recognition (P⫽0.28, 1-way
ANOVA), cued recall (P⫽0.35, 1-way ANOVA), explicit (P⫽
0.43, 1-way ANOVA), and implicit (P⫽0.22, 1-way ANOVA)
memory]. Performance on these memory measures was not
correlated with performance on the primed RAT items (Fig. 6).
Importantly, although all groups had similar memory for primed
answers, only subjects with REM sleep promoted generalization
of the analogy answers to new and useful solutions on an
unrelated creative problem-solving task.
Discussion
Here, we report that REM sleep can improve creative problem
solving. We found that: (i) the passage of time (i.e., incubation
period) improves problem solving for previously exposed items,
and this was independent of the sleep condition; (ii) sleep
enhanced creative problem solving for items that were primed
before sleep, but this was only true for naps that included REM
sleep; (iii) REM sleep improvements in creative problem solving
Fig. 4. Amountof sleep does not contribute to creative problem solving. TST
and improvement on primed RAT items were not significantly correlated (r⫽
0.104, P⫽0.53, trend line shown).
Fig. 5. REM sleep does not improve creative problem solving without prior
exposure. No group differences were found on the new RAT items (P⫽0.261
1-way ANOVA), and PM performance was not different from baseline in the
any of the three groups (CI 95%, ⫺13.0 to 41.2%; CI 95%, ⫺35.4 to 16.0%; and
CI 95%, ⫺51.0 to 15.4% for the REM, NREM, and rest groups, respectively).
Although daytime sleep has been shown to improve a range of cognitive
functions (perceptual, verbal, and motor learning; declarative and implicit
memory) and to increase alertness and restore homeostatic drive, neither
NREM nor REM sleep improves general creative problem solving in the ab-
sence of prior exposure (e.g., priming).
Fig. 6. REM sleep improvements in creativity are dissociated from memory.
Creative problem solving performance in the priming condition (yaxis) and
memory tasks (cued recall and recognition) are shown. The three groups
perform equally well on all memory tasks, although REM sleep improvements
in creativity are only seen in performance for primed unrelated items.
10132
兩
www.pnas.org兾cgi兾doi兾10.1073兾pnas.0900271106 Cai et al.
are not the result of selective improvements in memory; and (iv)
general problem-solving abilities were not improved in wake or
sleep conditions. These findings have important implications for
how sleep, specifically REM sleep, might foster the formation of
associative networks.
A longstanding, critical issue in sleep and cognition research
is whether improvements in behavioral performance are the
result of sleep-specific enhancement or reduction of interfer-
ence. Experiences during waking have been shown to interfere
with memory consolidation (29). Thus, performance benefits
observed after sleep may be the result of lack of interference. For
example, a recent study found that a quiet wake interval pro-
vided benefits for auditory tone sequence learning similar to
those from a sleep interval, and both were better than the active
wake interval (30). Our methods control for interference effects
by comparing sleep periods with quiet rest periods. Subjects were
relaxed on a recliner, with polysomnographic monitoring, and
they listened to instrumental music of their choice for a time
interval equal to the naps. By controlling for verbal input, we can
be confident that performance across sleep and wake groups was
not caused by a difference in verbal interference during the nap,
but specifically by processes occurring during incubation.
Current models for why we sleep posit an important role of
sleep in memory consolidation (31–34). While controlling for
circadian effects, the present study found that sleep specifically
enhanced the associative network for primed solutions but did
not improve memory consolidation. Although other studies have
reported that sleep enhances explicit verbal memory (22, 35), our
memory measures were not comparable with these recall tasks
because exposure to the verbal material was primed and not
explicitly presented. Furthermore, not only were NREM sleep,
REM sleep, and quiet rest groups indistinguishable on the
memory measures, performance on these memory measures was
not correlated with per formance on the primed RAT items. This
indicates that the improvement on the primed RAT was not a
consequence of the REM sleep group simply remembering the
primed words better than the other groups. These results are
consistent with the previous finding that memory strength of
previously encountered insight problems is not directly related to
the solution acquisition to those problems (36).
The results support the hypothesis that the brain is subcon-
sciously spreading activation of previously activated nodes. Prior
literature suggests that during a ‘‘dormant period’’ between two
active encounters with a problem, the memor y trace of a target
item, and the progression of this target through other relevant
stored information generate spreading activation through a
network (16). For example, by priming the solution SWEET
before sleep, the SWEET node is activated, and during subse-
quent REM sleep, the associative nodes (in this case HEART,
SIXTEEN, COOKIE) are more likely to be activated and
increased above threshold. Therefore, when the three words that
were previously unrelated (HEART, SIXTEEN, COOKIE) are
seen, there will be an increased probability of the node SWEET
being chosen as the solution. We propose that the most optimal
dormant period occurs during REM sleep, which provides the
most spreading of activation.
One possible mechanism for the spreading-activation model
involves cholinergic and noradrenergic neuromodulation that
occurs specifically during REM sleep. During wake, higher levels
of norepinephrine and acetylcholine inhibit recurrent connec-
tions in the neocortex. During REM sleep, however, high levels
of acetylcholine in the hippocampus suppress feedback from
hippocampus to the neocortex, whereas lower levels of acetyl-
choline and norepinephrine in the neocortex could facilitate the
spread of activity within neocortical areas without strong hip-
pocampal influence (37). This is supported by behavioral evi-
dence from amnesiacs that activation of this associative network
during sleep is independent of the medial temporal lobe struc-
tures and may reflect reactivation of remote memories that are
less dependent on the hippocampus (38). In this theoretical
framework, REM sleep would allow neocortical structures to
reorganize associative hierarchies, in which information from
the hippocampus would be reinterpreted in relation to previous
semantic representations or nodes.
We propose that REM sleep is important for assimilating new
information into past experience to create a richer network of
associations for future use. Fluid interpretation is a hallmark of
a creative mind, from idle word play to the abstraction of shapes
that led to the solving of neurochemical transmission or the
structure of the benzene ring. These findings on the role of REM
sleep in creative problem solving underscore the Nobel Laureate
Friedrich A. Kekule’s recommendation: ‘‘Let us learn to dream.’’
Experimental Procedures
General procedures are outlined in this section. Deviations from this proce-
dure are described in each section.
Subjects. A total of 77 native English speakers between the ages of 18 and 35
with no personal history of neurological, psychological, or other chronic illness
gave informed consent to participate in the experiment, which was approved
by the Institutional Review Board of the University of California at San Diego.
Subjects were required to sleep an average of 6 h per night for the 5 days
leading up to the experimental day and at least 6.5 h the night before the test
day. Subjects filled out sleep diaries and wore actigraphs 5–7 days before
testing as subjective and objective measures of sleep–wake activity. Subjects
were restricted from consuming caffeine and alcohol 24 h before and during
the experiment day.
Materials
RAT is a paper-and-pencil task adapted from Mednick (1). Each RAT item contains
a triplet of words presented horizontally along with a blank space. Each item
requires the subject to combine or relate the three words drawn from mutually
remote associative clusters (e.g., COOKIES, SIXTEEN, HEART: 㛭㛭㛭㛭㛭). The subject is
required to find a fourth word that could serve as an associative link between
these three words. The answer to this item is SWEET (cookies are sweet, sweet
sixteen, sweetheart). The three test words HEART, SIXTEEN, COOKIE are associ-
ated with the solution SWEET by formation of a compound (sweetheart), by a
syntactic association (sweet sixteen), and by a semantic relationship (cookies
are sweet). Thus, reaching a solution requires ‘‘creative thought’’ because the
first, most highly probable associate to each of the items is often not correct,
so the solver must think of more distantly related information to connect the
three words. Performance on the RAT correlates reliably with other estab-
lished insight problems (39).*
Subjects were read the instructions aloud and given four practice items to
ensure understanding of the task. The score was calculated as the proportion
of items answered correctly. Subjects completed two versions of the RAT, one
in the morning and one in the afternoon. The two versions were counterbal-
anced across sessions. In the morning session, subjects completed the AM RAT,
and AM scores were used as baseline.
Analogies. Analogies (e.g., FAST:SLOW as HARD:E㛭㛭㛭), were administered in
the AM session. The first letter of each answer was given. Half of the analogy
answers served as primes for the answers to the RAT administered during the
PM session. There was no time limit for completing the analogies. The mean
log HAL word frequency (40) for all words used in the analogies was 1.58 (SD ⫽
0.73). The mean word length was 5.36 letters (SD ⫽1.75).
General Method. All subjects were tested on the RAT twice in 1 day (Fig. 1). At
0900, subjects were administered the RAT followed by the analogies. Subjects
returned at 1300, at which time they were randomly assigned to a nap or a
quiet rest group. Subjects in the nap group took a polysomographically
recorded (PSG) nap (90 min of sleep maximum or up to2hinbed), whereas
those in the rest condition listened to instrumental music with PSG monitoring
for 90 min. At 1630, subjects returned for testing of the afternoon RAT.
*Dallob PI, Dominowski RL (April, 1993) Erroneous Solutions to Verbal Insight Problems:
Effects of Highlighting Critical Material. Paper presented at the 73rd Annual Meeting of
the Western Psychological Association, Portland, OR.
Cai et al. PNAS
兩
June 23, 2009
兩
vol. 106
兩
no. 25
兩
10133
NEUROSCIENCEPSYCHOLOGY
Experiment 1.
RAT.
Subjects completed 30 RAT items. They were given 40 min
to complete all of their responses.
Analogies.
Two versions with 30 analogies each were administered in the AM
session. Fifteen analogies in the AM had the same answers as 15 items in the
PM RAT.
Study procedure.
In the morning session, subjects completed the AM RAT and
then filled in responses to 30 analogies. In the PM RAT, 15 of the items were
primed during the AM analogies. The other 15 PM RAT items were unprimed.
A total of 25 subjects, REM (n⫽10), NREM (n⫽6), and rest (n⫽9), participated
in experiment 1.
Experiment 2.
RAT-S.
Two shortened versions of the RAT were used, each with
15 items. These versions were created by dividing Version A of the RAT into
odd and even items. The two versions were counterbalanced across sessions.
Subjects were given 20 min to complete all of their responses. The morning
RAT-S was used as a baseline performance measure. In the afternoon session,
two RAT-S forms were administered. One form was the same form as the
morning (i.e., uncued RAT-S), and the other form had the 15 answers cued
from the morning analogies (i.e., cued RAT-S).
Analogies.
Subjects completed 75 analogies. Fifteen correct answers were
primes for the afternoon cued-RAT-S. The remaining 60 analogy answers were
used in the afternoon session to test for memory retention with three distinct
methods. Twenty correct answers were tested on a recognition test, 20 correct
answers were tested on an inclusion test, and 20 correct answers were tested
on an exclusion test (see below for test description).
Inclusion and exclusion tests.
A modified version of the process-dissociation
procedure (15) was used to dissociate between explicit and implicit processes
for verbal memory. For the inclusion test, subjects were given 20 stem com-
pletions and asked to complete them with words they recalled from the
answers to the morning analogies. If they could not recall the word, they were
asked to fill in the stem with the first word that came to mind. For the exclusion
test, subjects were also given 20 stem completions and asked to complete with
words that were NOT answers to the morning analogies. If they could not
recall the word, they were to fill in the stem with the first word that came to
mind. The 40 words were counterbalanced across the inclusion– exclusion test
and condition. Explicit memory was calculated as inclusion ⫺exclusion. Im-
plicit was computed as exclusion/[1⫺(inclusion ⫺exclusion)] (28).
Study procedure.
At 0900, subjects were administered the RAT-S, followed by
the analogies. Subjects returned at 1300, at which time they were randomly
assigned to a nap or a quiet rest group. At 1700, subjects returned to execute
the cued RAT-S, noncued RAT-S, recognition, inclusion and exclusion tests. A
total of 52 subjects, REM (n⫽18), NREM (n⫽6), and rest (n⫽28) participated
in experiment 2.
Statistical Analyses. Three tests of percentage improvement on RAT perfor-
mance (repeat exposure, primed exposure, no exposure) were examined with
a 2-tailed, 1-way ANOVA by using three levels of the variable Group (REM,
NREM, quiet rest). Percentage improvement was calculated as (number of
correct responses on afternoon RAT ⫺number of correct responses on morn-
ing baseline RAT)/(number of correct responses on morning baseline RAT).
Percentage improvement was computed for each individual and then aver-
aged across subjects for each group. CI values were set at 95%, with a 2-tailed
probability to examine whether percentage improvement on the afternoon
RATs differed from 0 (i.e., no improvement). To examine the effect of specific
sleep stages on creative problem solving, we categorized naps by the presence
or absence of REM sleep as indicated by PSG. This segregated the data into
naps with REM, NREM, and quiet rest groups. Performance for new and repeat
exposure was calculated from experiments 1 and 2, respectively. There were
no differences between experiments 1 and 2 for performance in primed-
exposure RAT items [P⫽0.26, 2-way ANOVA (Experiment ⫻Group)], so
percentage improvement for each subject was collapsed across experiments 1
and 2.
ACKNOWLEDGMENTS. We thank Drs. John T. Wixted, Harold Pashler, William
A. Alaynick, David E. Huber, and Sean P. A. Drummond for their insightful
comments. This work was supported by National Institutes of Health Grant
K01 MH080992-01.
1. Mednick SA (1962) The associative basis of the creative process. Psychol Rev 69:220–
232.
2. Wallas G (1962) The Art of Thought (Harcourt Brace, New York).
3. Koestler A (1964) The Act of Creation (Dell, New York).
4. Patrick C (1937) Creative thought in artists. J Psychol 4:35–73.
5. Olton RM (1979) Experimental studies of incubation: Searching for the elusive.
J Creative Behav 13:9–22.
6. Olton RM, Johnson DM (1976) Mechanisms of incubation in creative problem solving.
Am J Psychol 89:617–630.
7. Vul E, Pashler H (2007) Incubation benefits only after people have been misdirected.
Mem Cognit 35:701–710.
8. Stickgold R, Walker M (2004) To sleep, perchance to gain creative insight? Trends
Cognit Sci 8:191–192.
9. Gomez RL, Bootzin RR, Nadel L (2006) Naps promote abstraction in language-learning
infants. Psychol Sci 17:670– 674.
10. Dumay N, Gaskell MG (2007) Sleep-associated changes in the mental representation of
spoken words. Psychol Sci 18:35–39.
11. Ellenbogen JM, et al. (2007) Human relational memory requires time and sleep. Proc
Natl Acad Sci USA 104:7723–7728.
12. Wagner U, et al. (2004) Sleep inspires insight. Nature 427:352–355.
13. Walker MP, et al. (2002) Cognitive flexibility across the sleep–wake cycle: REM-sleep
enhancement of anagram problem solving. Brain Res Cognit Brain Res 14:317–324.
14. Stickgold R, et al. (1999) Sleep-induced changes in associative memory. J Cognit
Neurosci 11:182–193.
15. Scrima L (1982) Isolated REM sleep facilitates recall of complex associative information.
Psychophysiology 19:252–259.
16. Yaniv I, Meyer DE (1987) Activation and metacognition of inaccessible stored infor-
mation: Potential bases for incubation effects in problem solving. J Exp Psychol Learn
Mem Cognit 13:187–205.
17. Mednick S, Nakayama K, Stickgold R (2003) Sleep-dependent learning: A nap is as good
as a night. Nat Neurosci 6:697–698.
18. Nishida M, Walker MP (2007) Daytime naps, motor memory consolidation and region-
ally specific sleep spindles. PLoS ONE 2:e341.
19. Nishida M, Pearsall J, Buckner RL, Walker MP (2008) REM sleep, prefrontal theta, and
the consolidation of human emotional memory. Cereb Cortex 19:1158–1166.
20. Walker MP, et al. (2002) Practice with sleep makes perfect: Sleep-dependent motor skill
learning. Neuron 35:205–211.
21. Mednick SC, Arman AC, Boynton GM (2005) The time course and specificity of percep-
tual deterioration. Proc Natl Acad Sci USA 102:3881–3885.
22. Mednick SC, et al. (2008) Comparing the benefits of caffeine, naps and placebo on
verbal, motor and perceptual memory. Behav Brain Res 193:79– 86.
23. Mednick SC, et al. (2002) The restorative effect of naps on perceptual deterioration.
Nat Neurosci 5:677–681.
24. Monk TH, et al. (2001) Effects of afternoon ‘‘siesta’’ naps on sleep, alertness, perfor-
mance, and circadian rhythms in the elderly. Sleep 24:680– 687.
25. Ellenbogen JM, et al. (2006) Interfering with theories of sleep and memory: sleep,
declarative memory, and associative interference. Curr Biol 16:1290–1294.
26. Gais S, Born J (2004) Declarative memory consolidation: Mechanisms acting during
human sleep. Learn Mem 11:679– 685.
27. Marshall L, Born J (2007) The contribution of sleep to hippocampus-dependent mem-
ory consolidation. Trends Cognit Sci 11:442–450.
28. Jacoby LL (1991) A process dissociation framework: Separating automatic from inten-
tional uses of memory. J Mem Language 30:513–541.
29. Wixted JT (2004) The psychology and neuroscience of forgetting. Annu Rev Psychol
55:235–269.
30. Gottselig JM, et al. (2004) Sleep and rest facilitate auditory learning. Neuroscience
127:557–561.
31. Maquet P (2001) The role of sleep in learning and memory. Science 294:1048–1052.
32. Sejnowski TJ, Destexhe A (2000) Why do we sleep? Brain Res 886:208–223.
33. Stickgold R (2005) Sleep-dependent memory consolidation. Nature 437:1272–1278.
34. Walker MP, Stickgold R (2006) Sleep, memory, and plasticity. Annu Rev Psychol
57:139–166.
35. Tucker MA, et al. (2006) A daytime nap containing solely non-REM sleep enhances
declarative but not procedural memory. Neurobiol Learn Mem 86:241–247.
36. Dougal S, Schooler JW (2007) Discovery misattribution: When solving is confused with
remembering. J Exp Psychol Gen 136:577–592.
37. Hasselmo ME (1999) Neuromodulation: Acetylcholine and memory consolidation.
Trends Cognit Sci 3:351–359.
38. Stickgold R, et al. (2000) Replaying the game: hypnagogic images in normals and
amnesics. Science 290:350–353.
39. Schooler JW, Melcher J (1995) The ineffability of insight. The Creative Cognition
Approach, eds Smith SM, Ward TB, Finke RA (MIT Press, Cambridge, MA), pp 249–268.
40. Balota DA, et al. (2007) The English Lexicon Project. Behav Res Methods 39:445–459
10134
兩
www.pnas.org兾cgi兾doi兾10.1073兾pnas.0900271106 Cai et al.
