Acta Psychologica 160 (2015) 127–133
Contents lists available at ScienceDirect
Acta Psychologica
journal homepage: www.elsevier.com/ locate/actpsy
Post-learning stress enhances long-term memory and differentially
influences memory in females depending on menstrual stage
Phillip R. Zoladz a,⁎, David M. Peters a, Chelsea E. Cadle a, Andrea E. Kalchik a, Rachael L. Aufdenkampe a,
Alison M. Dailey a, Callie M. Brown a, Amanda R. Scharf a, McKenna B. Earley a,
Courtney L. Knippen a, Boyd R. Rorabaugh b
a
b
Department of Psychology, Sociology, & Criminal Justice, Ohio Northern University, Ada, OH 45810, USA
Department of Pharmaceutical & Biomedical Sciences, Raabe College of Pharmacy, Ohio Northern University, Ada, OH 45810, USA
a r t i c l e
i n f o
Article history:
Received 6 June 2015
Received in revised form 17 July 2015
Accepted 20 July 2015
Available online xxxx
Keywords:
Stress
Learning
Memory
Sex
Menstrual
Emotion
a b s t r a c t
Most work has shown that post-learning stress enhances long-term memory; however, there have been
recent inconsistencies in this literature. The purpose of the present study was to examine further the effects of
post-learning stress on long-term memory and to explore any sex differences that may exist. Male and female
participants learned a list of 42 words that varied in emotional valence and arousal level. Following encoding,
participants completed a free recall assessment and then submerged their hand into a bath of ice cold (stress)
or lukewarm (no stress) water for 3 min. The next day, participants were given free recall and recognition
tests. Stressed participants recalled more words than non-stressed participants 24 h after learning. Stress also
enhanced female participants' recall of arousing words when they were in the follicular, but not luteal, phase.
These findings replicate previous work examining post-learning stress effects on memory and implicate the
involvement of sex-related hormones in such effects.
© 2015 Elsevier B.V. All rights reserved.
1. Introduction
Stress exerts powerful effects on learning and memory, and understanding these effects may lend insight into cognitive symptoms associated with stress-related psychological disorders, such as post-traumatic
stress disorder (PTSD) and major depression. Researchers have frequently
dichotomized stress-memory interactions into the effects of stress on
consolidation versus the effects of stress on retrieval, as these two phases
of memory processing seem to be differentially influenced by stress
(Roozendaal, McEwen, & Chattarji, 2009). Indeed, most research has
reported that stress enhances consolidation and impairs retrieval, despite
similar mechanisms, such as corticosteroid and noradrenergic interactions in the amygdala, underlying both (Beckner, Tucker, Delville, &
Mohr, 2006; Cahill, Gorski, & Le, 2003; Felmingham, Tran, Fong, &
Bryant, 2012; Nielson, Yee, & Erickson, 2005; Preuss & Wolf, 2009;
Roozendaal, 2003).
More recently, researchers have discovered that the effects of stress
on consolidation depend on whether the stress is administered before
or after learning, as well as the temporal proximity of the stress to learning. For instance, pre-learning stress that is experienced in the context
of learning (i.e., temporally associated with learning) often enhances
⁎ Corresponding author at: Ohio Northern University, Department of Psychology,
Sociology, & Criminal Justice, 525 S. Main St. Hill 013, Ada, OH 45810, USA.
E-mail address: p-zoladz@onu.edu (P.R. Zoladz).
http://dx.doi.org/10.1016/j.actpsy.2015.07.008
0001-6918/© 2015 Elsevier B.V. All rights reserved.
long-term memory (Diamond, Campbell, Park, Halonen, & Zoladz,
2007; Schwabe, Bohringer, Chatterjee, & Schachinger, 2008; Zoladz
et al., 2011; Zoladz et al., 2014), while pre-learning stress that is experienced outside the context of learning (i.e., temporally separated from
learning) often impairs long-term memory (Zoladz, Clark, et al., 2011;
Zoladz et al., 2013). Post-learning stress, on the other hand, almost
unequivocally enhances long-term memory (Cahill et al., 2003;
Felmingham, Tran, Fong, & Bryant, 2012; Nielson & Powless, 2007;
Nielson et al., 2005; Preuss & Wolf, 2009); however, such enhancement
declines as the stress is temporally removed from the learning experience (Nielson & Powless, 2007).
Although the effects of stress on learning and memory could be
perceived as adaptive when memory is enhanced and maladaptive
when memory is impaired, we would contend that all effects of stress
on learning and memory serve an adaptive role (Zoladz, Park, &
Diamond, 2011). When stress is experienced in the context of learning,
long-term memory is enhanced because, hypothetically, the stress
experience signals the brain that what is occurring is important to
remember, which results in a “Now Print” mechanism (Livingston,
1967), or emotional tag, that enhances memory formation. This enables
the individual to remember potentially life-threatening aspects related
to the stressor which could aid survival later in life. In support of this
reasoning, pre- and post-learning stress often enhances memory for emotional information, while impairing or having no effect on memory for
neutral information (Jelicic, Geraerts, Merckelbach, & Guerrieri, 2004;
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P.R. Zoladz et al. / Acta Psychologica 160 (2015) 127–133
Payne et al., 2007; Zoladz, Clark, et al., 2011). When stress is experienced
outside the context of learning, long-term memory is impaired because,
hypothetically, the brain, and in particular the hippocampus, is focused
on storing the memory of the stress experience, thereby rendering new
information storage improbable. Though simplistic, this approach to
how stress affects memory consolidation emphasizes the adaptive nature of the stress response and is supported by behavioral, molecular
and electrophysiological studies in humans and non-human animals.
Though many studies have reported that post-learning stress
enhances consolidation, some work has presented conflicting data
suggesting that such stress impairs long-term memory. For instance,
Trammell and Clore (2014) recently reported that post-learning cold
pressor stress (1–3 min duration) impaired long-term (48-h) word
and picture memory in participants. However, in the studies, all participants exhibited relatively poor long-term memory (recalling b 7% of
words studied and only ~ 10% of pictures studied) and, in two of the
three experiments, the difference in recall between stressed and nonstressed participants was only approaching significance (p's = 0.06
and 0.07). Additionally, the investigators examined 48-h memory, as
opposed to the more commonly used 24-h time point. Thus, the
purpose of the present study was to examine further the relationship
between post-learning stress and long-term (24-h) memory and to
assess how manipulating the emotional valence and arousal level of
the learned information could influence such effects. We hypothesized
that post-learning stress would facilitate long-term memory, perhaps
more strongly for emotionally arousing information. Moreover, because
sex differences are prevalent in the stress-memory literature, we also
examined whether post-learning stress differentially affected longterm memory in males and females. Some previous work has reported
greater memory-enhancing effects of stress in females, relative to
males (e.g., Felmingham, Tran, Fong, & Bryant, 2012; Zoladz et al.,
2014); thus, we predicted that females may be more susceptible to
post-learning stress effects on long-term memory. We also ran exploratory analyses on female data to assess whether menstrual cycle stage
interacted with stress effects on memory.
2.2.1. Word presentation
Participants were presented with a list of 42 words, which were selected from the Affective Norms for English Words (Bradley & Lang, 1999).
Based on standardized valence and arousal ratings, we chose 14 neutral
(7 arousing, 7 non-arousing), 14 positive (7 arousing, 7 non-arousing)
and 14 negative (7 arousing, 7 non-arousing) words, which, across
emotional valence and arousal categories, were balanced for word
length and word frequency. As per the methods employed by
Schwabe et al. (2008) and previous work from our own laboratory
(Zoladz, Clark, et al., 2011; Zoladz et al., 2013, 2014), participants
were instructed to read each word aloud and rate its emotional valence
on a scale from −4 (very negative) to +4 (very positive) and its arousal
level on a scale of 0 (not arousing) to 8 (very highly arousing) on a sheet
of paper containing the list of words and the aid of self-assessment
manikins. These manipulations were performed to promote encoding
of the words, and they allowed us to analyze the final memory data
based on participants' own ratings of the words.
According to the Affective Norms for English Words (Bradley & Lang,
1999), the mean (± SEM) valence and arousal ratings for the words
that made up the list were as follows: positive arousing words
(e.g., kiss): valence = 7.79 ± 0.12, arousal = 6.62 ± 0.25; positive
non-arousing words (e.g., cozy): valence = 7.50 ± 0.12, arousal =
3.46 ± 0.16; negative arousing words (e.g., poison): valence = 2.21 ±
0.16, arousal = 6.56 ± 0.27; negative non-arousing words
(e.g., unhappy): valence = 2.40 ± 0.20, arousal = 3.89 ± 0.19; neutral
arousing words (e.g., lightning): valence = 4.93 ± 0.27, arousal =
6.26 ± 0.20; neutral non-arousing words (e.g., poster): valence =
4.90 ± 0.14, arousal = 3.40 ± 0.13.
2.2.2. Immediate memory testing
Immediately following word list encoding, participants were given
5 min to write down as many words as they could remember from
the list of words they just studied. This immediate free recall test was
performed to verify that there were no group differences regarding
short-term memory performance and to avoid a potential floor effect
during long-term memory assessment (e.g., Zoladz, Clark, et al., 2011).
2. Materials and method
2.1. Participants
Fifty-two healthy men and naturally cycling women (27 men, 25
women; age: M = 20.30, SD = 1.17) from Ohio Northern University
volunteered to participate in the experiment. Individuals were excluded
from participating if they met any of the following conditions: diagnosis
of Raynaud's or peripheral vascular disease; presence of skin diseases,
such as psoriasis, eczema or scleroderma; history of syncope or vasovagal response to stress; history of severe head injury; current treatment
with psychotropic medications, narcotics, beta-blockers, steroids or
any other medication that was deemed to significantly affect central
nervous or endocrine system function; mental or substance use disorder; regular nightshift work. Participants were asked to refrain from
using recreational drugs (e.g., marijuana) for 3 days prior to the experimental sessions; to refrain from drinking alcohol or exercising extensively for 24 h prior to the experimental sessions; and, to refrain from
eating or drinking anything but water for 2 h prior to the experimental
sessions. Upon arrival at the laboratory, participants were reminded of
the exclusion criteria and study restrictions and verbally affirmed that
they had adhered to the requirements. Participants were awarded
class credit upon completion of the study. All of the methods for the
experiment were approved by the Institutional Review Board at Ohio
Northern University.
2.2. Experimental procedures
To control for diurnal variations in cortisol levels, all testing was
carried out between 1200 and 1800 h.
2.2.3. Cold pressor test (CPT)
Following immediate memory testing, participants were asked to
submerge their non-dominant hand, up to and including the wrist, in
a bath of water for 3 min. Those participants who had been randomly
assigned to the stress condition (N = 29; 17 males, 12 females) placed
their hand in a bath of ice cold (0–2 °C) water, while participants who
had been randomly assigned to the control condition (N = 23; 10
males, 13 females) placed their hand in a bath of warm (35–37 °C)
water. The water was maintained at the appropriate temperature by a
VWR 1160S circulating water bath. Prior to the actual manipulation,
participants were unaware of the possibility of being exposed to the
CPT. This was done to reduce the likelihood of a stress response occurring in participants prior to CPT exposure. To maximize the stress
response during the CPT, participants were encouraged to keep their
hand in the water bath for the entire 3-min period. However, if a participant found the water bath too painful, he or she was allowed to remove
his or her hand from the water and continue with the experiment. Only
four participants from the stress condition (3 females, 1 male) removed
their hand from the water prior to 3 min elapsing (mean water time =
165.24 s), and all participants from the no stress condition kept their
hand in the water for the entire 3-min period. Exclusion of the data
from the stressed participants who removed their hand from the
water early had no significant effects on the observed results.
2.2.4. Subjective pain and stress ratings
Participants were asked to rate the painfulness and stressfulness of
the water bath manipulation at 1-min intervals on 11-point scales ranging from 0–10, with 0 indicating a complete lack of pain or stress and 10
indicating unbearable pain or stress. If a participant removed his or her
P.R. Zoladz et al. / Acta Psychologica 160 (2015) 127–133
hand from the water before 3 min had elapsed, the remaining data
points were automatically scored as 10s for each measure.
2.2.5. Cardiovascular analysis
Heart rate (HR) and blood pressure (BP) measurements were taken
before encoding (baseline), halfway through the water bath manipulation and 10 min after cessation of the water bath manipulation. Cardiovascular activity was measured with a vital sign monitor (Mark of
Fitness WS-820 Automatic Wrist Blood Pressure Monitor) placed on
the wrist of each participant's dominant hand.
2.2.6. Cortisol analysis
Saliva samples were collected from participants before learning
(baseline) and 22 min following exposure to the water bath manipulation to analyze salivary cortisol concentrations. The samples were collected in a Salivette saliva collection device (Sarstedt, Inc., Newton,
NC). Participants were asked to place a synthetic swab in their mouths
and chew on it so that it would easily absorb their saliva. Following
1 min of chewing, the synthetic swab was collected and placed in the
Salivette conical tube and kept at room temperature until the experimental session was completed. The samples were subsequently stored
at − 20 °C until assayed for cortisol. Saliva samples were thawed and
extracted by low-speed centrifugation. Salivary cortisol levels were
determined by enzyme immunoassay (EIA; Cayman Chemical Co., Ann
Arbor, MI) according to the manufacturer's protocol.
2.2.7. Delayed memory testing
Twenty-four hours following encoding, participants returned to the
laboratory for an unexpected free recall assessment (they had been told
to return to the lab the next day to complete paperwork) and were
given 5 min to write down as many words as they could remember
from the list of words that they studied on the previous day
(i.e., delayed free recall). Then, participants sat quietly for 10 min,
after which they were given a recognition test. Participants were presented with a list of words containing 42 “old” words (i.e., words that
were presented on the previous day) and 42 “new” words (i.e., words
that were not presented on the previous day) and were instructed to
label each word as “old” or “new.” The “new” words were matched to
the “old” words on emotional valence, word length and word frequency,
according to the ratings obtained from the Affective Norms for English
Words (Bradley & Lang, 1999). To assess participants' ability to discriminate between “old” and “new” words, we calculated a sensitivity index
(d' = z[p(hit)] − z[p(false alarm)]) for each category of word
(i.e., positive arousing words, positive non-arousing words, negative
arousing words, etc.) to be used for statistical analysis.
2.3. Statistical analyses
Mixed-model ANOVAs were used to analyze all physiological and
behavioral data; the between-subjects factors utilized in these analyses
were stress and sex, and the within-subjects factors were word valence
and arousal (for recall and recognition analyses) or time (for physiological and subjective ratings analyses). We also performed exploratory
analyses on the memory data from female participants to determine
whether menstrual cycle stage influence any observed effects. In order
to do so, we divided female participants into follicular [0–14 days
since last period; N = 12 (8 stress, 4 no stress)] or luteal [≥ 15 days
since last period; N = 13 (4 stress, 9 no stress)] phases of the menstrual
cycle (Nielsen, Ahmed, & Cahill, 2013). This division was based on selfreport data obtained from female participants regarding how many
days it had been since their last period. In these analyses, stress and
menstrual stage served as the between-subjects factors. The analyses
of participants' valence and arousal ratings and memory for the words
(i.e., immediate free recall, delayed free recall, and recognition) were
performed based on categorizing the words (i.e., distributing the
words to positive arousing, positive non-arousing, negative arousing,
129
etc. groups) according to participants' subjective valence and arousal
ratings that were obtained during the study. The resulting categories
matched almost identically those produced from the standardized
ratings obtained from the Affective Norms for English Words. Each
valence-arousal category had 7 words, for a total of 42 words.
Alpha was set at 0.05 for all analyses, and Bonferroni-corrected post
hoc tests were employed when necessary. SPSS (version 18.0; SPSS,
Inc.) was used to perform all statistical analyses.
3. Results
3.1. Physiological responses (see Table 1)
3.1.1. Heart rate
During the water bath manipulation, stressed participants exhibited
an increase in HR, while non-stressed participants exhibited a decrease
in HR (significant Condition × Time interaction: F(2,86) = 5.30, p =
0.007, η2 = 0.11, confirmed by post hoc tests with p b 0.05). Overall,
participants' HR decreased over time (significant effect of time:
F(2,86) = 11.71, p b 0.001, η2 = 0.21, confirmed by post hoc tests
with p b 0.05). Males also exhibited greater baseline HR than females
(significant Sex × Time interaction: F(2,86) = 3.79, p = 0.026, η2 =
0.08, confirmed by post hoc tests with p b 0.05).
3.1.2. Blood pressure
Stressed participants exhibited greater systolic and diastolic BP than
non-stressed participants during the water bath manipulation (SYSTOLIC:
significant effect of time: F(2,86) = 5.86, p = 0.004, η2 = 0.12; significant
Condition × Time interaction: F(2,86) = 3.11, p = 0.049, η2 = 0.07,
confirmed by post hoc tests with p b 0.05; DIASTOLIC: significant effect
of time: F(2,86) = 10.11, p b 0.001, η2 = 0.19; significant
Condition × Time interaction: F(2,86) = 3.40, p = 0.038, η2 = 0.07, confirmed by post hoc tests with p b 0.05). Male participants also exhibited
greater systolic and diastolic BP than female participants (SYSTOLIC: significant effect of sex: F(1,43) = 26.25, p b 0.001, η2 = 0.38; DIASTOLIC:
significant effect of sex: F(1,43) = 21.99, p b 0.001, η2 = 0.34).
3.1.3. Salivary cortisol (see Fig. 1)
Stressed participants exhibited greater salivary cortisol levels than
non-stressed participants after the water bath manipulation (significant
effect of time: F(1,43) = 6.22, p = 0.017, η2 = 0.13; significant
Condition × Time interaction: F(1,43) = 11.24, p = 0.002, η2 = 0.21,
confirmed by post hoc tests with p b 0.05).
3.2. Subjective ratings of water bath manipulation
Stressed participants reported greater pain (STRESS: M = 5.93,
SEM = 0.35; NO STRESS: M = 0.46, SEM = 0.41) and stress (STRESS:
M = 5.25, SEM = 0.47; NO STRESS: M = 1.01, SEM = 0.54) ratings
than non-stressed participants throughout the water bath manipulation
Table 1
Cardiovascular activity before, during and after the water bath manipulation.
DV/condition
Heart rate (bpm)
Stress
No stress
Pre
70.79 (1.98)
75.91 (4.93)
During
Post
72.81 (2.43)
69.15 (3.14)
62.93 (1.56)
68.48 (2.80)
Systolic blood pressure (mm Hg)
Stress
119.72 (2.13)
No stress
123.59 (2.90)
135.67 (4.73)⁎
124.75 (4.67)
124.28 (3.41)
122.57 (2.61)
Diastolic blood pressure (mm Hg)
Stress
74.00 (2.07)
No stress
78.68 (2.50)
88.52 (3.34)⁎
80.85 (3.43)
77.34 (1.90)
74.81 (2.47)
Data are presented as means ± SEM.
⁎ p b 0.05 relative to the no stress group.
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P.R. Zoladz et al. / Acta Psychologica 160 (2015) 127–133
effect of valence: F(2,96) = 283.31, p b 0.001, η2 = 0.86). In addition,
arousing words were given more positive ratings than non-arousing
words (significant effect of arousal: F(1,48) = 4.17, p = 0.047, η2 =
0.08). The latter effect appeared to depend on the valence of the words
and the sex of the participant. For instance, positive, but not negative
or neutral, words were rated more positively if they were arousing
in nature (significant Valence × Arousal interaction: F(2,96) = 13.22,
p b 0.001, η2 = 0.22, confirmed by post hoc tests with p b 0.05). In addition, males rated arousing words more positively than non-arousing
words, while females did not (significant Sex × Arousal interaction:
F(1,48) = 6.76, p = 0.012, η2 = 0.12, confirmed by post hoc tests with
p b 0.05).
Fig. 1. Salivary cortisol levels before and after exposure to the water bath manipulation.
Stressed participants exhibited significantly higher cortisol levels than non-stressed participants following the water bath manipulation. Data are expressed as means ± SEM.
*p b 0.05 relative to no stress.
3.3.2. Arousal ratings
Arousing words were rated as more arousing than non-arousing
words (significant effect of arousal: F(1,48) = 94.71, p b 0.001, η2 =
0.66). Positive words were rated as more arousing than negative words,
which were rated as more arousing than neutral words (significant effect
of valence: F(2,96) = 43.92, p b 0.001, η2 = 0.48).
3.4. Memory testing (see Figs. 2 and 3)
(PAIN RATINGS: significant effect of condition: F(1,45) = 103.39,
p b 0.001, η2 = 0.70; STRESS RATINGS: significant effect of condition:
F(1,45) = 35.25, p b 0.001, η2 = 0.44).
3.3. Word list ratings
3.3.1. Valence ratings
Positive words were given more positive ratings than neutral words,
which were given more positive ratings than negative words (significant
3.4.1. Immediate free recall
For the immediate free recall test, there were no significant differences in overall memory performance between participants assigned
to the stress and no stress groups (no significant effect of condition:
F(1,45) = 3.21, p = 0.08, η2 = 0.07). However, there was a significant
Condition × Valence interaction, F(2,90) = 4.51, p = 0.014, η2 = 0.09,
indicating that participants assigned to the stress group recalled
more neutral words than participants assigned to the no stress group
Fig. 2. Immediate and delayed free recall performance. Overall, there were no significant group differences in immediate free recall (inset a); however, a significant Condition × Valence interaction was noted, revealing that participants in the stress group recalled more neutral words than participants in the no stress group. As shown in insets b (data expressed as a percentage
of immediate free recall performance) and c (raw data expressed as a percentage of total words), stressed participants recalled significantly more words on the delayed free recall assessment
than non-stressed participants. This effect was independent of the valence or arousal level of the words. Data are expressed as means ± SEM. *p b 0.05 relative to no stress.
P.R. Zoladz et al. / Acta Psychologica 160 (2015) 127–133
131
F(1,21) = 4.77, p = 0.04, η2 = 0.19, confirmed by post hoc tests with
p b 0.05; significant Condition × Arousal × Menstrual Stage interaction:
F(1,21) = 16.10, p = 0.001, η2 = 0.43, confirmed by post hoc tests with
p b 0.05).
Fig. 3. Delayed free recall performance in females as a function of stress, menstrual cycle
and arousal levels of the words. Non-stressed females exhibited greater memory for
arousing words, relative to non-arousing words, during the luteal phase, and stressed
females exhibited greater memory for arousing words, relative to non-arousing words,
during the follicular phase. Stressed females also exhibited greater memory for nonarousing words, relative to non-stressed females, during the luteal phase. Data are
expressed as means ± SEM, and sample sizes have been provided for each group.
*p b 0.05 relative to non-arousing words; β = p b 0.05 relative to no stress.
(confirmed by post hoc tests with p b 0.05). Overall, participants recalled
more negative words than positive and neutral words (significant effect
of valence: F(2,90) = 5.50, p = 0.006, η2 = 0.11). Participants also
recalled more arousing words than non-arousing words, although this
effect was only evident in male participants (significant effect of arousal:
F(1,45) = 9.52, p = 0.003, η2 = 0.18; significant Sex × Arousal interaction: F(1,45) = 6.57, p = 0.014, η2 = 0.13, confirmed by post hoc tests
with p b 0.05).
The analysis of immediate free recall performance in females (which
included menstrual stage and condition as factors) revealed no significant main effects or interactions.
3.4.2.2. Percent of immediate recall. Because we observed some group
differences in immediate free recall performance, we also analyzed the
delayed free recall performance as a percent of immediate free recall
(i.e., (delayed recall/immediate recall) ∗ 100). This analysis corroborated our findings from the raw data analysis by revealing that stressed
participants recalled more words overall than non-stressed participants
(significant effect of condition: F(1,48) = 7.90, p = 0.007, η2 = 0.14).
Overall, participants recalled more negative words than positive and
neutral words (significant effect of valence: F(2,96) = 7.96, p = 0.001,
η2 = 0.14). Participants also recalled more arousing words than nonarousing words, particularly when they were negative or neutral in valence (significant effect of arousal: F(1,48) = 6.88, p = 0.012, η2 = 0.13;
significant Valence × Arousal interaction: F(2,96) = 9.46, p b 0.001,
η2 = 0.17, confirmed by post hoc tests with p b 0.05).
The analysis of delayed free recall performance expressed as a percent
of immediate free recall in females revealed that the effects observed
when analyzing the raw data remained significant. Stressed females
recalled more words overall than non-stressed females (significant effect
of condition: F(1,21) = 7.80, p = 0.011, η2 = 0.27), and more importantly, the three-way Condition × Arousal × Menstrual Stage interaction
described above remained significant, F(1,21) = 5.30, p = 0.032, η2 =
0.20, confirmed by post hoc tests with p b 0.05.
3.4.3. Delayed recognition (see Fig. 4)
There were no significant differences between the recognition
performance of stressed and non-stressed participants (no significant
effect of condition: F(1,48) = 1.38, p = 0.247, η2 = 0.03). Participants
did recognize more arousing than non-arousing words when they
were negative or neutral in valence (significant Valence × Arousal
interaction: F(2,96) = 7.65, p = 0.001, η2 = 0.14, confirmed by post
hoc tests with p b 0.05). The analysis of delayed recognition in females
revealed no significant main effects or interactions.
3.4.2. Delayed free recall
4. Discussion
3.4.2.1. Raw data. Stressed participants recalled more words overall than
non-stressed participants (significant effect of condition: F(1,48) =
6.87, p = 0.012, η2 b 0.13). Overall, participants recalled more negative
and neutral words than positive words (significant effect of valence:
F(2,96) = 14.30, p b 0.001, η2 = 0.23). Participants also recalled more
arousing words than non-arousing words, particularly when they
were negative or neutral in valence (significant effect of arousal:
F(1,48) = 27.71, p b 0.001, η2 = 0.37; significant Valence × Arousal
interaction: F(2,96) = 4.97, p = 0.009, η2 = 0.09, confirmed by post
hoc tests with p b 0.05).
The analysis of raw delayed free recall performance in females
revealed that stressed females recalled more words overall than nonstressed females (significant effect of condition: F(1,21) = 13.84, p =
0.001, η2 = 0.40). Overall, female participants recalled more positive
and neutral words than negative words (significant effect of valence:
F(2,42) = 8.31, p = 0.001, η2 = 0.28) and more arousing words than
non-arousing words (significant effect of arousal: F(1,21) = 6.97, p =
0.015, η2 = 0.25). More interestingly, stress exerted differential effects
on emotional memory in females, depending on stage of the menstrual
cycle. Specifically, stress enhanced memory for arousing words, relative
to non-arousing words, when females were in the follicular stage, while
enhancing memory for non-arousing words, relative to non-stressed
female memory for non-arousing words, when in the luteal phase.
Non-stressed females exhibited greater memory for arousing words,
relative to non-arousing words, when in the luteal, but not follicular,
phase (significant effect of menstrual stage: F(1,21) = 9.88, p =
0.005, η2 = 0.32; significant Arousal × Menstrual Stage interaction:
Most studies examining the effects of post-learning stress on longterm memory have reported facilitative effects (Beckner et al., 2006;
Cahill et al., 2003; Preuss & Wolf, 2009). However, there is some
research in this literature reporting no effects or an impairment of
long-term memory (e.g., Trammell & Clore, 2014). The purpose of the
present study was to examine further the effects of post-learning stress
on long-term memory and to explore whether sex and menstrual cycle
Fig. 4. Recognition memory during the 24-h test. No significant group effects were
observed for recognition memory. Data are expressed as means ± SEM.
132
P.R. Zoladz et al. / Acta Psychologica 160 (2015) 127–133
stage influenced such effects. We found that post-learning stress
enhanced 24-h free recall, even when memory performance was
expressed as a percent of immediate free recall performance. This enhancement was independent of sex, as well as the valence and arousal
level of the words. We also found that emotional memory in females
was differentially affected by post-learning stress, depending on
which stage of the menstrual cycle they were experiencing at the time
of stress. Specifically, stress enhanced memory for arousing words,
relative to non-arousing words, in females who were in the follicular
phase and enhanced memory for non-arousing words, relative to nonstressed female memory, in females who were in the luteal phase.
Together, our results replicate the majority of post-learning stress research and extend these findings to implicate female hormonal mechanisms in such effects.
4.1. Neurobiological mechanisms of post-learning stress
We purposely induced post-learning stress as close in time as possible to word list learning in order for the stressor to be experienced in the
context of learning. That we observed an enhancement of long-term
memory as a result of this manipulation is consistent with previous
research revealing that the timing of stress relative to learning is important in dictating the types of effects observed on long-term memory
(Diamond et al., 2007; Quaedflieg, Schwabe, Meyer, & Smeets, 2013;
Zoladz, Clark, et al., 2011; Zoladz et al., 2014). Physiologically, stress
results in the activation of two major systems, the sympathetic nervous
system and the hypothalamus-pituitary-adrenal axis. Activation of
these two systems results in increased adrenergic and corticosteroid
activity, respectively, which can exert biphasic effects on cognitive
processing. When the stress-induced increases in adrenergic and corticosteroid activity converge in time with learning, research suggests that
these mechanisms, coupled with amygdala activity, facilitates memory
processing in structures such as the hippocampus, which enables
phenomena such as flashbulb memories to occur (Diamond et al.,
2007; Schwabe, Joels, Roozendaal, Wolf, & Oitzl, 2012). Consistent
with this idea, we found that CPT exposure in the present study resulted
in significant increases in cardiovascular measures, indicators of autonomic and adrenergic activity, and salivary cortisol concentrations.
These effects were produced with a relatively brief (3-min) stressor,
suggesting that even brief stress of a particular intensity can promote
memory consolidation. The CPT is a physiologically-based stressor, as
it produces a stress response via cold-induced pain. However, the effects
of the CPT on cortisol levels, learning and memory are comparable
to those induced by other stressors, such as psychosocial stress
(e.g., Trier Social Stress Test).
can impact the acquisition and extinction of emotional memory.
Felmingham, Fong, and Bryant (2012) reported that heightened progesterone, which typically peaks in the mid-late luteal phase, is positively
correlated with memory recall of threatening images and may mediate
cortisol response. Similarly, a study examining sex differences in acoustic startle response found that females in the late luteal phase exhibited
enhanced startle response compared to both males and females in the
follicular phase (Armbruster, Strobel, Kirschbaum, & Brocke, 2014).
One hypothesis put forth to explain progesterone's enhancing effects
for arousing material is that heightened progesterone levels increase
sensitivity to sources associated with threat or danger (Conway et al.,
2007; Derntl et al., 2008). There appears to be a plausible interaction
occurring between progesterone and cortisol, such that in the absence
or diminished levels of one hormone, the heightened levels of the
opposing chemical acts in such a way as to mimic the effects of the
other. This could explain why females in the follicular phase (low
progesterone) exhibited greater delayed recall for arousing words
only in the stressed condition (high cortisol), while females in the luteal
phase (high progesterone) had enhanced delayed recall for arousing
material when in the control condition (low cortisol).
4.3. Caveats
Although the present results indicate that post-learning stress might
differentially influence females depending on menstrual stage, it is important to emphasize that the analyses performed on such measures
here were exploratory in nature and consisted of relatively small sample
sizes (as indicated in Fig. 3). Furthermore, we did not measure the levels
of progesterone or estradiol in females, and our measure of menstrual
stage was based on self-report. Therefore, although our findings are suggestive of a link between menstrual cycle activity and stress-memory
interactions, further research is clearly warranted to substantiate
these claims.
4.4. Conclusions
We have provided additional evidence that post-learning stress
facilitates long-term memory, an effect that, at least in the present
study, is independent of the emotional nature of the learned information. We have also shown that females are differentially affected by
post-learning stress depending on stage of the menstrual cycle. These
findings further validate post-learning stress-induced enhancements
of long-term memory and implicate female sex hormones in such
effects.
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