2012. Vol.3, No.5, 419-423
Published Online May 2012 in SciRes (
Copyright © 2012 SciRes. 419
Enhancing Effects of Post-Learning Stress on Memory
Mingming Lin1,2, Yoshihiko Tanno2
1Research Fellow of the Japan Society for the Promotion of Science, Tokyo, Japan
2Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, Tokyo, Japan
Received February 23rd, 2012; revised April 26th, 2012; accepted May 29th, 2012
To investigate the enhancing effect of post-learning stress on memory, we requested 38 Japanese under-
graduates to perform a learning task that involved positive, negative, and neutral words with controlled
arousal and subsequently assigned them to a stress group (exposed to acute white noise) or a control
group. After a 10-min filler task, we administered a delayed free recall test and a recognition test. We
found that exposure to acute stress after learning significantly enhanced recognition memory of words,
but found no differences in memory scores for stimuli of varying valence. We accordingly propose that
post-learning stress, though enhancing memory performance, may not depend on word valence when
stimulus arousal is controlled. This is the first study to find that post-learning stress enhances memory af-
ter a short delay, and it has several implications with regard to traumatic memories in stress-related dis-
Keywords: Post-Learning Stress; Memory; Valence; Arousal
Stressful events are remembered well, and are particularly
vivid for individuals with stress-related disorders, such as
post-traumatic stress disorder (PTSD) (Berntsen, Willert, &
Rubin, 2003). Researchers investigating laboratory stress have
recently reported that people remember well not only the mem-
ory of a stressor itself but also the memory that is created im-
mediately before or after stress. This effect was thought to be
stress-enhanced memory consolidation (Wolf, 2008). However,
there are some incongruities in different studies in the effect of
acute stress on emotional memory and neutral memory.
With regard to the effect of stress on memory consolidation,
many studies have found that stress after learning (i.e., post-
learning stress) can enhance memory performance. These stud-
ies have used stimuli, such as words (Smeets, Otgaar, Candel,
& Wolf, 2008), pictures (Cahill, Gorski, & Le, 2003; Yonelinas,
Parks, Koen, Jorgenson, & Mendoza, 2011; Preuss & Wolf,
2009), or a short film or story (Andreano & Cahill, 2006;
Beckner, Tucker, Delville, & Mohr, 2006). In contrast, other
studies have found that stress before learning (i.e., pre-learning
stress) both enhances and impairs memory. For instance, Kir-
schbaum, Wolf, May, Wippich, and Hellhammer (1996) found
that pre-learning stress impaired memory, while some re-
searchers have reported that such pre-learning stress tended to
impair neutral memory while either enhancing or having no
influence on positive and negative emotional memory (Jelicic,
Geraerts, Merckelbach, & Guerrieri, 2004; Smeets, Jelicic, &
Merckelbach, 2006). Studies on pre-learning stress have found
that stress affords greater benefits to emotional memory than to
neutral memory; however, the observed effects of pre-learning
stress may have been caused by the mixed influence of stress
on the initial encoding and the consolidation of learning mate-
rials (Schwabe, Wolf, & Oitzl, 2010). Therefore, the use of a
post-learning manipulation appears to be desirable to determine
the effect of stress on memory consolidation.
However, there is a controversy in studies of post-learning
stress as to whether acute stress enhances neutral or emotional
memories. Some previous studies have reported that acute
stress selectively enhances only negative, not neutral, memories,
after using both negative emotional and neutral materials (Ca-
hill et al., 2003; Smeets et al., 2008). Others have reported an
enhancement of neutral memories after using both negative and
neutral materials (Yonelinas et al., 2011), or relatively neutral
materials alone (Andreano & Cahill, 2006; Beckner et al.,
2006). However, to determine whether post-learning stress
enhances emotional or neutral memory, the enhancing memory
effect should be investigated using three-valence materials
(neutral, negative, and positive). The use of positive material
should be considered to prevent the mood-congruence effect
(i.e., people retrieve more negative memories in response to a
negative mood that may have been induced by stress manipula-
tion; Blaney, 1986). Preuss and Wolf (2009) used positive,
negative, and neutral pictures and reported that post-learning
stress enhanced the recall of neutral, but not emotionally posi-
tive or negative, items. This result is incongruent with those of
previous studies that found that post-learning stress had an
enhancing effect on negative memory. It remains unclear as to
whether post-learning stress, which is thought to affect memory
consolidation, has a greater enhancing effect on emotional
memory or on neutral memory.
A possible limitation of previous studies is that they followed
the traditional protocol in which participants were exposed to
acute stress after a learning task, followed by a long delay
(hours to days) before the memory test was administered. To
the best of our knowledge, no study has investigated whether
post-learning stress affects memory after a shorter delay. Fur-
thermore, in previous studies, participants spent most of this
period outside the laboratory. Therefore, a concern with most
studies is that the participants may have been influenced by
some stressful events after leaving the laboratory and that these
events may have had a greater effect on memory than did the
stress manipulation they experienced in the laboratory setting.
This uncontrollable influence may also have caused the incon-
gruence in these studies’ findings on stress effects.
In an attempt to overcome the aforementioned shortcomings
and resolve the controversies in the literature, the present study
uses three-valence (positive, negative, and neutral) stimuli,
while conducting all procedures involving the delayed memory
test within a controlled laboratory environment, in order to
investigate whether post-learning acute stress enhanced emo-
tional memory or neutral memory. To the best of our knowl-
edge, this is the first study to test the post-learning stress effect
following a short delay after the administration of the stressor.
Furthermore, we used two-character compound words as learn-
ing materials in our memory task. Each word consists of two
Chinese characters, and thus, all words were of uniform length;
this condition circumvented the possibility of memory impair-
ment due to the word-length effect (Baddeley, Thomson, &
Buchanan, 1975) which might influence the effect of acute
stress on memory performance. We expected that our new pro-
tocol would eliminate the uncertainty regarding the influence of
extraneous variables, which was seen in previous studies.
We randomly assigned 38 Japanese undergraduate students
(18 females and 20 males), with a mean age of 19.2 years (SD =
1.42, range: 18 - 26), to a stress group (n = 19, nine females and
ten males, mean age: 19.0, SD = 0.94, range: 18 - 21) or a con-
trol group (n = 19, nine females and ten males, mean age: 19.5,
SD = 1.78, range: 18 - 26). The study was approved by the local
ethics committees of the University of Tokyo. All the partici-
pants gave written informed consent before the experiment
began and were well debriefed on completion of the study.
Materials an d Apparatu s
The target stimulus list in the learning task comprised 24
two-character compound words, which included eight neutral
words, eight positive words, and eight negative words. All
words were chosen from the list provided by Gotoh and Ohta
(2001), who investigated the affective valence, frequency of use,
ease of learning, and imagery of two character compound
words. Furthermore, to prevent the serial position effect, two
series of three filler words, which had neutral, negative, and
positive valence, were each placed before and after the targets.
Arousal of these words was investigated in preliminary research
(n = 18). A one-way analysis of variance (ANOVA) showed
that all three word categories (neutral, positive, and negative)
differed significantly with regard to valence (neutral: M = 3.73,
SD = 0.05; positive: M = 1.95, SD = 0.17; negative: M = 5.99,
SD = 0.24; on a 7-point scale, ranging from 1 (“extremely posi-
tive”) to 7 (“extremely negative”); F (2, 21) = 1120.81, p
< .001). The score of arousal did not differ significantly (neu-
tral: M = 4.06, SD = 0.45; positive: M = 4.24, SD = 0.44; nega-
tive: M = 4.25, SD = 0.36; on a 7-point scale ranging from 1
(“extremely low arousal”) to 7 (“extremely high arousal”); F (2,
21) = 0.53, p = .60). Furthermore, no differences were found in
the frequency of use, ease of learning, and imagery; all ps
> .10.
For the recognition test, another 24 “new” words were cho-
sen from the same list. These words were similar to the “old”
words, which were presented in the learning task. A 2 (old vs.
new) × 3 (neutral vs. positive vs. negative) ANOVA showed
that the new words did not differ significantly from the old
words with regard to valence, arousal, frequency of use, ease of
learning, and imagery; all ps > .10.
All stimuli were presented at the center of a 12.1-inch black
computer screen in a 60-point white Gothic font. The entire
experiment was programmed in MATLAB 7.0.4, using the
Psychophysics Toolbox extensions (Brainard, 1997; Pelli,
Subjective Stress Measure
Subjective stress was measured using the Japanese version of
the Profile of Mood State Brief Form (POMS-BF; Yokoyama,
2005). POMS is a widely used self-report measure for typical
and persistent mood reactions to current situations. POMS-BF
comprises 30 items across six subscales: Tension-Anxiety, De-
pression-Dejection, Anger-Hostility, Fatigue, Confusion, and
Vigor. The participants indicated the extent to which they
agreed with adjectives describing their current mood or feelings,
on 5-point scales (0: “not at all”; 4: “extremely”). The subjec-
tive stress scores were calculated using the following formula:
Tension-Anxiety + Depression-Dejection + Anger-Hostility +
Fatigue + Confusion Vigor.
Stress Manip ul a tion
Participants in the stress group were exposed to 80-dB white
noise through a headset for 5 min continuously. Noise stress is
a stress manipulation that has been widely used in previous
studies (e.g., Carter & Beh, 1989; Smith, Whitney, Thomas,
Perry & Brockman, 1997), and known to affect cardiovascular
function such as blood pressure. Noise stress allows us to ex-
pose participants to acute stress during a task, without inter-
rupting their operation of that task.
After filling out the consent form, participants were in-
structed to perform several computer tasks while wearing
headphones. They were informed that they might hear some
sound from the headphones while performing these tasks. Ini-
tially, participants performed a learning task, in which the word
stimulus was presented at the center of the computer screen for
2000 ms, after a fixation cross was presented for 500 ms. The
inter-trial interval was 1000 ms. The presentation order of both
the 24 target words and two series of filler words were ran-
Immediately after the learning task, the participants per-
formed a 5-min calculation filler task, in which stimuli were
also presented on a computer screen. In this task, the partici-
pants were required to press keys on the keyboard to give their
answers. Those in the stress group were exposed to 80-dB
white noise during this task, while the control group was not
exposed to any sound. Using POMS, we measured subjective
stress before and after this filler task.
After another 10-min filler task, the participants performed a
delayed free recall task followed by a recognition task, in which
the 48 word stimuli were randomly presented at the center of a
computer screen, in a similar manner to the learning task, for a
maximum of 2000 ms, or until the participant responded. When
Copyright © 2012 SciRes.
each word was shown, the participant was required to decide
whether the word was “old” or “new” by pressing the “F” or
“J” key, respectively, within 2000 ms. The experiment lasted
for approximately 60 min, and all participants were tested indi-
Subjective Stress
Subjective stress was indexed by an increase in the scores of
POMS (increase = POMS before stress/control task—POMS
after stress/control task). The mean subjective stress scores are
shown in Figure 1. A two-sample t-test showed that the par-
ticipants in the stress group had higher subjective stress than
those in the control group (stress group: M = 8.47, control
group: M = –2.00), t(36) = 4.16, p < .001 (two-tailed)). The
results showed that the stress manipulation was effective.
Memory Performance: Delayed Recall
Numbers of correctly-recalled target items were added up
separately for neutral, positive, and negative words, respec-
tively. The proportion of correct recall was calculated by di-
viding correctly-recalled numbers by the total amount of pre-
sented target-word numbers for each valence (neutral: M = .26,
positive: M = .24, negative: M = .24 in the stress group; neutral:
M = .18, positive: M = .21, negative: M = .18 in the control
group). Recall performance was analyzed using a 2 (Group:
stress group vs. control group) × 3 (Valence: neutral vs. posi-
tive vs. negative) ANOVA with valence as a repeated factor.
The ANOVA showed that delayed recall score in the stress
group (M = .24, SD = .14) tended significantly higher than in
the control group (M = .19, SD = .13), as demonstrated by a
tendency of significant main effect of Group, F(1, 36) = 3.01, p
= .09. No other significant main effects of Valence, F(2, 72) =
0.11, p = .89, or Group × Valence interaction, F(2, 72) = 0.44, p
= .65, were detected.
Memory Performance: Recognition
Recognition score was calculated as the discrimination (hit
rate, proportion of old items correctly recognized, minus false
alarms rate, proportion of new items falsely identified as old).
A higher recognition score indicates enhanced recognition per-
formance. Mean recognition performance is shown in Figure 2.
Recognition performance was analyzed using a 2 (Group: stress
group vs. control group) × 3 (Valence: neutral vs. positive vs.
negative) ANOVA, with valence as a repeated factor. The
ANOVA yielded a significant main effect of Group, F(1, 36) =
5.42, p < .05, and of Valence, F (2, 72) = 3.50, p < .05. The
main effect of Group showed that the total score of recognition
in the stress group (M = .68, SD = .20) was significantly higher
than that in the control group (M = .56, SD = .26), regardless of
valence. Bonferroni corrected post hoc analyses on Valence
showed that the recognition performance of positive words
tended significantly higher than that of negative words (p
= .08). However, no significant interactive effects, F(2, 72) =
1.61, p = .21, were detected.
The main purpose of this study was to examine the enhanc-
Figure 1.
Mean subjective stress scores for both the stress group
and the control group. Error bars indicate ±1 SE.
Figure 2.
Mean recognition performance as a function of valence and groups.
Error bars indicate ±1 SE.
ing effect of post-learning stress on the memory of words. It
was the first investigation to test post-learning stress effect in a
short time delay, and used uniform-length words of three va-
lences (positive, negative and neutral) as learning material to
prevent word-length effect. We found that acute white noise
stress enhanced memory performance significantly in a recog-
nition test, regardless of valence.
Participants in the stress group exhibited a significant subjec-
tive stress response following exposure to white noise. With
regard to the effect of acute stress on word memory perform-
ance, the results suggest that exposure to acute stress after
learning significantly enhanced recognition memory, and
tended to significantly enhance delayed recall memory. This
finding of an effect of enhancing memory is in line with previ-
ous studies. Furthermore, recognition performance tended
higher for positive than for negative words, regardless of
groups. The higher positive memory is thought to result from a
positive bias, where healthy people prefer to have better mem-
ory of positive things than of negative ones (Matlin & Stang,
We could not find differences in memory scores for positive,
negative, and neutral word stimuli. There was no stress-caused
selective enhancement of emotional memory or neutral memory.
This result is incongruent with previous research, in which
selective enhancement of emotional negative memory (Cahill et
al., 2003; Smeets et al., 2008) or neutral memory (Preuss &
Wolf, 2009; Yonelinas et al., 2011) was reported. One possible
explanation for this result is that post-learning stress enhances
word memory performance, but relies on material arousal and
Copyright © 2012 SciRes. 421
not on the valence of stimuli. Both the valence and arousal of
the material mediate the processing of emotional memory
(Lang, Newhagen, & Reeves, 1996), and arousal ranges from
calming to exciting, while valence ranges from positive to
negative. In examining the relationship between the effect of
acute stress on emotional memory, especially pre-learning
stress and acute stress on memory retrieval, Wolf (2009) as-
serted that arousal might be more important than valence with
regard to the occurrence of stress effects. Stress is much more
likely to selectively affect the memory of high arousing mate-
rial than low arousing material. We controlled the arousal level
of learning words stimuli used in this study, so this effect of
acute stress on material arousal might have caused a null effect
between neutral and emotional memory performance. Therefore,
there is a possibility that the effect of stimulus arousal may
have been responsible for the incongruent results of previous
studies regarding whether post-learning stress enhances mem-
ory of emotional stimuli (Cahill et al., 2003; Smeets et al., 2008)
or neutral stimuli (Preuss & Wolf, 2009; Yonelinas et al., 2011).
In other words, using highly arousing emotional stimuli would
enhance emotional memories owing to acute stress, while using
emotional and neutral stimuli of the same arousal level (or per-
haps more highly arousing neutral stimuli) would enhance neu-
tral memory.
However, in the present study, the enhancing effect on mem-
ory observed in the stress group was only a non-significant
tendency with regard recall performance, but was significant
with regard to recognition performance. In previous studies
reporting an enhancing effect in recall performance using word
stimuli, the percentage of correct stem cued recall was above
50% (Smeets et al., 2008), and in those that reported using free
recall of slide stimuli, the correct recall performance was over
37% (Cahill et al., 2003). In the current study, the total recall
percentage across all participants was only 22%. One potential
explanation for this is that the free recall test was too difficult;
consequently, the effect of acute stress on recall would have
been hard to observe, owing to the floor effect. Another reason
could be that the enhancing effect of stress may have appeared
in the recognition test, which was administered after the de-
layed recall test. This finding of enhanced recognition is in
accordance with the results of Yonelinas et al. (2011), who also
administered a recognition test after a free recall test.
Despite the scope for further research in this area, the present
paper—to the best of our knowledge—is the first to show an
enhancing effect of post-learning stress following only a short,
10-min delay after the administration of the stressor. With re-
gard to the mechanisms of post-learning stress, previous studies
have stated that stress modulates memory consolidation so as to
enhance memory performance; however, it is not clear whether
stress effects reflect the “systems” or “synaptic” forms of con-
solidation. Yonelinas et al. (2011) stated that synaptic forms
might lead to an enhancing effect of post-learning stress two
hours after the administration of the stress. Our finding of en-
hancement after a short 10-min delay may substantiate the the-
ory of synaptic consolidation.
Evidence of the effect of stress on memory would be ex-
pected to improve understanding of memory consolidation with
regard to stress-related disorders such as PTSD. On the basis of
the evidence of enhanced memory consolidation as a result of
stress, Schwabe et al. (2010) have postulated that the extreme
arousal associated with a traumatic event leads to “over-con-
solidation.” Our findings suggest that because the enhancing
effect of stress on memory consolidation would start shortly
after learning, administering a treatment intended to prevent
consolidation, immediately after a stressful event, may help
patients overcome traumatic memories.
Finally, some limitations of this study should be mentioned.
First, we used only arousal-controlled words, that is, words that
elicit little emotional arousal. To determine the effect of mate-
rial arousal, further studies that use both low- and high-arousal
three-valence learning materials should be conducted. Second,
it remains unclear whether acute stress directly affects recogni-
tion memory, or whether the recalled memory, which was af-
fected by stress, indirectly affects recognition memory. Addi-
tional investigations should use only a recognition test to pro-
vide answers. Finally, it is unclear whether the enhancement of
memory after a short time delay in this study will be sustained
for a long time, as reported by previous studies where long-time
delays (hours to days) were considered. Further research that
compares short and long time delays is necessary and will
proffer some evidence in response to this question.
In summary, using positive and negative emotional materials
and neutral materials, we found that the administration of acute
noise stress after a learning task enhanced memory performance
of words after a short delay. However, in this study, there was
no selective enhancement among negative, positive, and neutral
memory. The arousal level of the learning material may be
responsible for this result. This finding suggests that at least in
some conditions, post-learning stress will enhance memory
performance regardless of the valence of memory materials.
We would like to thank Hironori Akechi and Masanori Ko-
bayashi for their helpful comments on the manuscript.
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