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Previous studies have shown that retrieval practice leads to better long-term memory than additional study of a material (a phenomenon termed the testing effect). In this study, we compared the effectiveness of these learning strategies when the final test occurs under stress (such as in an exam). Participants studied word pairs; then half of the material was repeatedly studied, whereas the other half was repeatedly tested. Following a 7-day delay, participants were exposed to either a psychosocially stressful situation or a control task, followed by an associative recall task that tested memory for all items. Multiple measures were used to assess stress levels: emotional state assessments as well as assays of salivary cortisol and alpha-amylase levels. Results are in favour of the ecological validity of retrieval-based learning. Participants recalled more retested items than restudied items regardless of being exposed to a stressful situation and the hormonal (cortisol) response to stress.Copyright
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The Testing Effect is Preserved in Stressful Final Testing Environment
ÁGNES SZŐLLŐSI
1
*, ATTILA KERESZTES
2
, BÁLINT NOVÁK
3
, BARNABÁS SZÁSZI
4
,
SZABOLCS KÉRI
1,5
and MIHÁLY RACSMÁNY
1,6
1
Department of Cognitive Science, Budapest University of Technology and Economics, Budapest, Hungary
2
Center for Lifespan Psychology, Max Planck Institute for Human Development, Berlin, Germany
3
Department of General Psychology, Pázmány Péter Catholic University, Budapest, Hungary
4
Institute of Psychology, Eötvös Loránd University, Budapest, Hungary
5
National Institute of Psychiatry and Addictions, NyírőGyula Hospital, Budapest, Hungary
6
Research Group on Frontostriatal Disorders, Hungarian Academy of Sciences, Budapest, Hungary
Summary: Previous studies have shown that retrieval practice leads to better long-term memory than additional study of a mate-
rial (a phenomenon termed the testing effect). In this study, we compared the effectiveness of these learning strategies when the
nal test occurs under stress (such as in an exam). Participants studied word pairs; then half of the material was repeatedly stud-
ied, whereas the other half was repeatedly tested. Following a 7-day delay, participants were exposed to either a psychosocially
stressful situation or a control task, followed by an associative recall task that tested memory for all items. Multiple measures were
used to assess stress levels: emotional state assessments as well as assays of salivary cortisol and alpha-amylase levels. Results are
in favour of the ecological validity of retrieval-based learning. Participants recalled more retested items than restudied items re-
gardless of being exposed to a stressful situation and the hormonal (cortisol) response to stress.Copyright © 2017 John Wiley &
Sons, Ltd.
To nd ways to make our memories more resistant to forget-
ting is a fundamental goal not only in memory research but
also in our everyday life. Testing, or retrieval practice, has
been a learning technique of special interest because previ-
ous studies have pointed out the active role of retrieval in
memory retention (Roediger & Karpicke, 2006a; Tulving,
1967). The testing effect refers to the long-term retention
benet that results from retrieving a material when compared
with restudying it after initial learning (Roediger &
Karpicke, 2006a, 2006b).
The efciency of retrieval-based learning in laboratory
settings is underscored by a large number of studies (for a re-
view, see, e.g. Roediger & Butler, 2011); furthermore, there
is strong empirical evidence for the benecial effect of test-
ing in educational practice (e.g. McDaniel, Agarwal,
Huelser, McDermott, & Roediger, 2011; McDermott,
Agarwal, DAntonio, Roediger, & McDaniel, 2014;
Roediger, Agarwal, McDaniel, & McDermott, 2011). Re-
sults of these studies are in favour of the ecological validity
of retrieval-based learning as they show that the testing ef-
fect pertains with different materials and test formats widely
used in educational settings (Roediger & Butler, 2011;
Roediger & Karpicke, 2006b). However, a study by Hinze
and Rapp (2014) showed that when restudyretest practice
occurred under high pressure in an educational setting, it
eliminated the testing effect (Hinze & Rapp, 2014). Impor-
tantly, the typical testing situations in everyday life are usu-
ally exams, where despite the considerable stress experi-
enced, it is especially important to recall the previously
acquired knowledge as accurately as possible. To investigate
the relationship between stress and the effectiveness of dif-
ferent learning strategies seems to be especially important,
because it is known that stress and stress hormones clearly
inuence episodic memory retrieval (i.e. the conscious recol-
lection of events).
Experiencing stressful situations triggers the activation of
the hypothalamicpituitaryadrenal axis and the sympathetic
nervous system (Mason, 1968; OConnor, OHalloran, &
Shanahan, 2000). Free salivary cortisol levels and salivary
alpha-amylase (sAA) activity are reliable markers of the ac-
tivations of the hypothalamicpituitaryadrenal axis
(Kirschbaum & Hellhammer, 1994) and the sympathetic ner-
vous system, respectively (Nater et al., 2006). In a typical ex-
periment on the relationship between stress, stress hormones
and human memory, participants are presented with a mem-
ory paradigm following cortisone administration or stress ex-
posure. Most studies found that elevated cortisol levels be-
fore retrieval impair the retrieval of various learning
materials (e.g. Kirschbaum, Wolf, May, Wippich, &
Hellhammer, 1996; de Quervain, Rozendaal, Nitsch,
McGaugh, & Hock, 2000; Wolf et al., 2001; Schwabe &
Wolf, 2014; for reviews, see Lupien, Maheu, Tu, Fiocco,
& Schramek, 2007; Wolf, 2009) and autobiographical events
(Buss, Wolf, Witt, & Hellhammer, 2004; Schlosser et al.,
2010). A wide range of glucocorticoid receptors can be
found in the hippocampus, which structure is known to play
a key role in episodic memory (McEwen, 2008). Results of
functional neuroimaging studies suggest that cortisol de-
creases the activations of the hippocampus resulting in im-
paired ability to access (episodic) information previously ob-
tained (de Quervain et al., 2003; Oei et al., 2007; Pruessner
et al., 2008).
It is important to note that in all the previously mentioned
studies on stress-related memory, participants had no chance
to practise the learning material in a systematic way after ini-
tial learning. Therefore, it is unclear how previous ndings
can be generalized to differences in memory for materials
learnt with different strategies. Because there is a great inter-
subject variability in the way individuals react to stressors
(Miller, Plessow, Kirschbaum, & Stalder, 2013), it seems to
*Correspondence to: Ágnes Szőllősi, Department of Cognitive Science, Bu-
dapest University of Technology and Economics, Egry József Street 1, 1111
Budapest, Hungary.
E-mail: aszollosi@cogsci.bme.hu
Copyright © 2017 John Wiley & Sons, Ltd.
Applied Cognitive Psychology, Appl. Cognit. Psychol. (2017)
Published online in Wiley Online Library (wileyonlinelibrary.com) DOI: 10.1002/acp.3363
be also important to investigate cortisol effects on memory
and their relationship with different learning strategies.
In this study, we aimed to investigate the long-term ef-
fectiveness of restudy and retest practice when the nal
memory test occurred under stress. Following the initial
learning of paired associates, participants practised the
word pairs either by rereading the material (restudy condi-
tion) or by cued recall (retest condition). Feedback was
given for each item during practice, because the inclusion
of feedback is suggested to use in educational practice as
it improves the benecial effect of practice (e.g. Butler,
Karpicke, & Roediger, 2007; Butler & Roediger, 2008).
Following a 7-day retention interval, subjects were exposed
to either psychosocial stressors or a non-stressful control
task. Finally, participantsmemory was tested for all word
pairs they studied previously.
Importantly, to assess stress levels, multiple measures
were used: assays of salivary cortisol and alpha-amylase
levels as well as emotional state assessments. Stress levels
were assessed three times: immediately before the initial
learning phase as well as immediately before and after the
stress inducing (or the control) task.
It has been recently demonstrated that repeated retrieval
practice decreases the involvement of attentional control
(Mulligan & Picklesimer, 2016) and of attentional control-
related brain regions (Keresztes, Kaiser, Kovács, &
Racsmány, 2014; van den Broek, Takashima, Segers,
Fernández, & Verhoeven, 2013) and increases the level of
automatization of recall (Racsmány, Szőllősi, & Bencze,
2017). An important attribute of automatization is that mem-
ories become more resistant to various disturbing effects
(Logan, 1988). Therefore, we could assume that the automa-
tization of retrieval through repeated retrieval practice is an
important protective factor against the negative effects of
acute stress.
MATERIALS AND METHODS
Participants
Sixty-seven Hungarian undergraduate students (native Hun-
garian speakers) participated in the experiment. One partici-
pants baseline salivary cortisol level (45 nmol/l) was more
than three standard deviations away from the mean of the
sample (M= 17.6 nmol/l, SD = 9.1); therefore, this partici-
pant was considered as an outlier. Further, three participants
were excluded from the sample, because they did not provide
enough saliva for cortisol analysis. We analysed the results
of 63 participants (28 men and 35 women; age range: 19
27 years; M
age
= 21.3 years, SD = 1.7). Participants were ran-
domly assigned into one of the two experimental groups. On
experimental day 2, they were exposed to either a stressful
situation (stress group; n= 30; 13 men; M
age
= 21.4 years,
SD = 1.5) or a control task (control group; n= 33; 15 men;
M
age
= 21.2 years, SD = 1.8).
Subjects were recruited at different universities in Buda-
pest, Hungary, and received either extra course credits or
money for their participation (type of compensation was
equally distributed between the experimental groups). The
study was approved by the Ethical Committee of the Buda-
pest University of Technology and Economics, Hungary.
Memory task
Participants were presented with a computer-controlled
learning paradigm, while seated at approximately 70 cm
from a computer display. The experiment was performed
using PRESENTATION
®
software (version 14.3, www.
neurobs.com). We used word pairs as stimuli, because in
tasks using paired associates as stimuli, it is easy to provide
feedback to the participants and to control for the time inter-
val between study and test (Roediger & Karpicke, 2006b).
Stimuli were 40 neutral SwahiliHungarian word pairs trans-
lated from Nelson and Dunlosky (1994).
The memory task consisted of two main phases, sepa-
rated by a 7-day retention interval: a learning phase (initial
learning and practice) and a nal test phase. In the initial
learning phase, participants were presented with all word
pairs in random order [5000 milliseconds per word pair;
inter-stimulus interval (ISI): 500 milliseconds] on the com-
puter screen, with the Swahili word on the left and its Hun-
garian equivalent on the right, and were instructed to mem-
orize as many word pairs as they could. Because the
retention benet of testing increases as a function of the
number of practice trials (e.g. Rawson & Dunlosky, 2011;
Vaughn & Rawson, 2011; Wiklund-Hörnqvist, Jonsson, &
Nyberg, 2014), our subjects practised the word pairs in
six cycles immediately after the initial learning phase.
Word pairs were randomly assigned into a restudy (20
word pairs) or a retest condition (20 word pairs). Each
practice cycle consisted of a restudy, a retest and a feed-
back block (the order of the restudy and retest blocks var-
ied randomly across the learning cycles). In the restudy
blocks, participants saw 20 Swahili words together with
their Hungarian meanings in random order (8000 millisec-
onds per word pair; ISI: 500 milliseconds). In the retest
blocks, 20 Swahili words were presented in random order
on the computer screen, and participants were instructed
to type the Hungarian meanings of the words using the
keyboard of the computer. They had a maximum of
8000 milliseconds to complete one word pair. Based on
the results of earlier experiments using retrieval practice
manipulations, delayed feedback seems to be more bene-
cial to memory retention than immediate feedback (e.g.
Butler et al., 2007; Butler & Roediger, 2008) probably be-
cause memory retention is better when the stimulus presen-
tation is spaced or distributed (Dempster, 1989). Therefore,
in our experiment (following some previous studies, e.g.
Keresztes et al., 2014), feedback was not given after each
trial, but at the end of each practice cycle. In the feedback
blocks, all 40 word pairs were presented randomly for the
participants (1500 milliseconds per word pair; ISI: 500 mil-
liseconds). In order to eliminate the effect of self-testing
during the 7-day retention interval, participants were in-
formed that the purpose of the second experimental session
would be to examine social cognition.
Seven days after the rst experimental session, partici-
pantsmemory for all 40 word pairs was tested in the nal
test phase. Swahili words were presented in random order,
Á. Szőllősi et al.
Copyright © 2017 John Wiley & Sons, Ltd. Appl. Cognit. Psychol. (2017)
and participants were asked to type their Hungarian equiva-
lents. They had a maximum of 8000 milliseconds to com-
plete one word pair.
Stress and control procedure
Because testing is typically a socially stressful situation in
educational settings, we decided not to use a physically but
a socially stressful procedure. Therefore, participants in the
stress group were exposed to the Trier Social Stress Test
(TSST; Kirschbaum, Pirke, & Hellhammer, 1993), which
was developed to induce moderate psychosocial stress in
humans in laboratory settings. Participants had 5 minutes
to prepare for giving a 5-minute speech in front of two ob-
servers (a male and a female) who had been introduced as
a board of experts in non-verbal behaviour. Following the
5-minute preparatory phase and the 5-minute speech, partic-
ipants were given a 5-minute arithmetic task. We told them
that audio and video recordings would also be made for later
analysing their behaviour (no recording was actually made).
Participants in the control group were exposed to a standard-
ized control version of the TSST (Het, Rohleder, Schoofs,
Kirschbaum, & Wolf, 2009), which was developed to be as
similar as possible to the original stress-inducing procedure
but without any socially stressful components (observers as
well as audio and video recorders).
Saliva sampling and cortisol/alpha-amylase analyses
Saliva samples were collected from each participant three
times: once on the rst experimental day and twice on the
second experimental day. Samples were collected using
Eppendorf Safe-Lock Tubes (1.5 ml) and were kept at room
temperature until the end of the experimental sessions, and
then at 10 °C until analysis (for a maximum of 12 weeks).
Free salivary cortisol concentrations and sAA activity were
determined by Salimetrics immunoassay.
Subjective assessment
Following each saliva sampling, participants completed the
Hungarian version of the state form of the State-Trait Anxi-
ety Inventory (STAI-s; Spielberger, Gorsuch, Lushene,
Vagg, & Jacobs, 1983; Hungarian: Sipos, Sipos, &
Spielberger, 1994) including 20 questions on the current
level of anxiety. Participants were asked to rate the items
of the questionnaire on a 4-point scale (1 = not at all and
4=very much so). Immediately after the completion of the
STAI-s, participants were asked to ll out the Hungarian ver-
sion of the Positive and Negative Affect Schedule (PANAS;
Watson, Clark, & Tellegen, 1988; Hungarian: Gyollai,
Simor, Köteles, & Demetrovics, 2011) including two sets
of items on positive (10 items) and negative affects
(PANAS-n; 11 items). Participants were instructed to com-
plete the PANAS on their current affective state. They rated
the items on a 5-point scale ranging from 1 = not at all to
5=extremely. Finally, subjects rated how stressful they were
just then (0 = not at all and 100 = very stressful).
General procedure
Participants were asked to refrain from meal, alcohol, caf-
feine, smoking and physical exercise 2 hours prior to the ex-
perimental sessions in order to eliminate any effect of these
factors on salivary cortisol levels and on sAA activity. Ex-
perimental sessions were run between 16:00 and 20:00 in or-
der to avoid any interference with the cortisol circadian cycle
(for a review, see, e.g. Clow, Hucklebridge, Stalder, Evans,
& Thorn, 2010) as well as the circadian rhythm-dependent
change in daily sAA activity (Rohleder, Nater, Wolf, Ehlert,
& Kirschbaum, 2004).
For the experimental procedure, see Figure 1. The rst ex-
perimental session was preceded by a 5-minute preparatory
phase in order to familiarize the participants to the situation
and to minimize the effect of stress-inducing factors (e.g.
new environment) in this initial phase of the experiment. Dur-
ing this preparatory phase, participants gave written informed
consent and completed a preliminary questionnaire including
questions on demographic data and any known neurological
and psychiatric disorders. The preparation was followed by
a stress assessment (saliva sampling and subjective rating),
and then subjects participated in the learning phase of the
memory task (initial learning and the six practice cycles).
The second session (7 days after the rst session) was also
preceded by a preparatory phase that was followed by a
stress assessment (saliva sampling and subjective rating).
Immediately after the stress assessment, participants were
exposed to either the TSST or the control procedure. Al-
though most earlier studies used a delay between the
stress/control manipulation and testing (in order to reach
the cortisol peak), following Hupbach and Fieman (2012),
we aimed to minimize the time interval between the stress-
inducing procedure and the nal test phase of the memory
task in order to preserve the context of the stressful situation
as much as possible (following more an exam-like situation).
Therefore, the TSST/Control-TSST was immediately
followed by the third stress assessment (saliva sampling
and subjective rating) that took 3 to 5 minutes and then,
again with no delay, the nal test of the memory task.
Figure 1. Experimental procedure. Stress assessment: saliva sampling and subjective rating (state form of the State-Trait Anxiety Inventory,
the positive and negative affect schedule and a subjective stress scale); t
1
, immediately before initial learning; t
2
, immediately before stress/
control manipulation; t
3
, immediately after stress/control manipulation; TSST, Trier Social Stress Test
Stress and testing effect
Copyright © 2017 John Wiley & Sons, Ltd. Appl. Cognit. Psychol. (2017)
RESULTS
Stress versus control procedure
The success of the stress induction
Different types of measurements were used to assess the
success of the stress induction (determination of cortisol and
sAA levels from saliva and emotional state assessments;
Figure 2). For all measurements, we conducted a mixed-design
analysis of variance (ANOVA) with stress exposure (stress/
control) as a between-subjects variable and time (t
1
/t
2
/t
3
)asa
within-subjects variable (where t
1
= immediately before initial
learning, t
2
= immediately before the stress/control task and
t
3
= immediately after the stress/control task).
For sAA activity, the ANOVA established the success of
the stress induction. We found a signicant Time × Stress
exposure interaction [F(2, 58) = 44.36, p<.001, η
2
p
= .43].
The contrast analysis showed that sAA activity in the stress
group increased from t
2
to t
3
[F(1, 27) = 40.67, p<.001,
η
2
p
= .60]. For cortisol data, a similar pattern of results
emerged [interaction between time and stress exposure:
F(2, 61) = 3.00, p= .056, η
2
p
= .05], with stressed subjects
cortisol levels showing a trend-level increase from t
2
to t
3
[F(1, 29) = 3.60, p= .068, η
2
p
= .11]. The lower effect sizes
for cortisol levels than for sAA activity could be because
sAA activity reaches its peak considerably faster than sali-
vary cortisol levels (Nater et al., 2005). Note that we did
not use a delay between stress and saliva sampling in order
to preserve the context of the stressful situation.
Mean ratings on the PANAS-n, STAI-s and the subjective
stress scale showed similar patterns. We found signicant
Time × Stress exposure interactions [PANAS-n: F(1,
61) = 6.53, p= .002, η
2
p
= .10; STAI-s: F(1, 61) = 9.15,
p<.001, η
2
p
= .13; subjective stress: F(1, 61) = 7.23,
p= .001, η
2
p
= .11]. Independent samples t-tests established
that scores differed between the stress and the control groups
at t
3
[PANAS-n: t(61) = 3.04, p= .004, d= 0.78; STAI-s:
t(61) = 3.22, p= .002, d= 0.82; subjective stress:
t(61) = 2.81, p= .007, d= 0.72]. Similarly to results obtained
for cortisol and amylase levels, the contrast analysis showed
that stressed subjects received higher scores at t
3
than at t
2
[PANAS-n: F(1, 29) = 0.34, p= .028, η
2
p
= .16; STAI-s:
F(1, 29) = 16.21, p<.001, η
2
p
= .36; subjective stress: F(1,
29) = 20.04, p<.001, η
2
p
= .41]. Altogether, this pattern of
results conrmed that the stress induction was successful.
Memory performance
In order to test whether initial test performance differed be-
tween the groups at the end of the rst (learning) phase of
the experiment, we compared recall success in the last retest
cycle between the stress and the control condition (stress
group: M= 85.7%, SD = 17.1; control group: M= 91.4%,
SD = 12.5). We found no signicant difference between
the groups [t(61) = 0.94, p= .352, d= 0.24].
A mixed-design ANOVA was conducted on recall rate in
the nal test phase of the memory task with study condition
(restudy/retest) as a within-subjects variable and stress expo-
sure (stress/control) as a between-subjects variable. For re-
call rates, a signicant main effect of study condition was
found [F(1, 61) = 44.01, p<.001, η
2
p
= .42]. Post-hoc anal-
yses established that participants recalled more retested items
than restudied items in both groups [stress group:
t(29) = 5.66, p<.001, d= 1.03; control group:
t(32) = 3.80, p<.001, d= 0.66; Figure 3(A)]. Stress expo-
sure had no effect on recall performanceneither the main
effect of stress exposure [F(1, 61) = 0.88, p= .351,
η
2
p
= .01] nor the interaction between the independent vari-
ables (Stress exposure × Study condition) was signicant
[F(1, 61) = 1.41, p= .240, η
2
p
= .02].
Figure 2. The impact of stress exposure as shown by different measures. An increase could be seen from t
2
to t
3
in stressed subjects(A) sAA
activity (p<.001), (B) salivary cortisol levels (p= .068), (C) subjective stress levels (p<.001), (D) STAI-state scores (p<.001) and (E)
PANAS-negative scores (p= .028). (F) No signicant group difference was found in participantspositive affective state as measured by the
PANAS-positive subscale. Error bars represent the standard error of the mean. PANAS, Positive and Negative Affect Schedule; STAI, State-
Trait Anxiety Inventory; t
1
, immediately before initial learning; t
2
, immediately before stress/control manipulation; t
3
, immediately after stress/
control manipulation
Á. Szőllősi et al.
Copyright © 2017 John Wiley & Sons, Ltd. Appl. Cognit. Psychol. (2017)
In brief, despite the successful stress induction, stress (im-
mediately before retrieval) had no effect on memory perfor-
mance. Furthermore, retrieval practice led to better long-term
memory retention than rereading both in the stress and the
control groups.
Cortisol responders versus non-responders
Composition of the cortisol responder and the
non-responder group
On a post-hoc basis, we classied each participant into either
a cortisol responder or a non-responder group (irrespective
of whether they were exposed to the stress-inducing task or
the control procedure). The cut-off point we used was
adapted from Weitzman et al. (1971). Participants in the re-
sponder group (n= 24; 10 men; also member of the stress
group: n= 16) showed an increase of at least 2.5 nmol/l in
their cortisol levels immediately after the stress/control pro-
cedure when compared with their own baseline levels imme-
diately before the stress exposure or the control task. The
remaining 39 participants (18 men; also member of the stress
group: n= 14) were assigned into the non-responder group.
Memory performance
The 2 × 2 ANOVA (Study condition × Cortisol response) re-
vealed a signicant main effect of study condition [F(1,
61) = 40.00, p<.001, η
2
p
= .40] and of cortisol response
[F(1, 61) = 6.00, p= .017, η
2
p
= .09] indicating that repeated
retrieval led to superior long-term memory performance
when compared with rereading and that subjects who
showed a cortisol response performed worse (in general)
on the long-term recall test than non-responders. The Study
condition × Cortisol response interaction was not signicant
[F(1, 61) = 1.00, p>.99, η
2
p
<.01].
Post-hoc analyses showed that cortisol responders recalled
fewer items both in the restudy [t(61) = 2.05, p= .045,
d= 0.52] and the retest conditions [t(61) = 2.44, p= .018,
d= 0.62]. Despite this, recall rate for the retested word pairs
was higher than for the restudied items in the responder
group [t(23) = 3.65, p= .001, d= 0.74] and also in the
non-responder group [t(38) = 5.50, p<.001, d= 0.88;
Figure 3(B)].
Because non-responders showed better memory than cor-
tisol responders in the nal test phase, we tested on a post-
hoc basis whether the two groups differed in their initial test
performance (i.e. during the retest cycles of the practice
phase; Figure 4). We conducted a mixed-design ANOVA
with a within-subjects factor of cycle (16) and a between-
subjects factor of cortisol response (responders/non-re-
sponders). Whereas the Cycle × Cortisol response interaction
was not signicant [F(1, 61) = 0.63, p= .679, η
2
p
= .01], cycle
and cortisol response had main effects on recall rate
[F(1, 61) = 419.38, p<.001, η
2
p
= .87 and F(1, 61) = 4.73,
p= .034, η
2
p
= .07, respectively]. This pattern of results
indicate that non-responders showed better initial learning
performance than cortisol responders (irrespective the pres-
ence of any stressors in this phase of the experiment).
In a following analysis, we compared the proportion of
correct initial test items on nal test between cortisol re-
sponders (M= 61.0%, SD = 18.0) and non-responders
(M= 70.1%, SD = 17.2), and we found a signicant differ-
ence between the groups [t(61) = 2.00, p= .050, d= 0.51].
These ndings indicate that besides their relatively low ini-
tial learning performance, cortisol responders showed higher
forgetting rate when compared with the non-responder
group.
Figure 3. Recall rates in the nal test phase of the memory task. Comparison of recall rates for the restudied and the retested word pairs (A)
between the stress group and the control group and (B) between cortisol responders and non-responders. Error bars represent the standard error
of the mean
Figure 4. Recall rates of cortisol responders and non-responders in
the six retest cycles of the practice phase. Error bars represent the
standard error of the mean
Stress and testing effect
Copyright © 2017 John Wiley & Sons, Ltd. Appl. Cognit. Psychol. (2017)
In sum, cortisol responders recalled fewer word pairs than
non-responders in the nal test phasebecause of their dif-
ference in initial learning success and forgetting rate. Never-
theless, retrieval practice seemed to be a more efcient strat-
egy than rereading even if individuals showed an increase in
their cortisol levels (responders) and even if they did not
(non-responders).
DISCUSSION
The main objective of our study was to test whether the long-
term benet of retrieval practice (retest) compared with re-
reading (restudy) is insensitive to stress exposure. Partici-
pants showed an increase in their negative affective state
(as measured by the PANAS-n subscale, the state form of
the STAI and a subjective stress scale) and sAA activity im-
mediately after stress exposure when compared with the con-
trol groupconrming the success of the stress induction.
Memory for the retested word pairs was better than for the
restudied word pairs irrespective of whether participants
were presented with psychosocial stressors or not.
Importantly, although stress treatment had no signicant
effect on our participantsmemory performance, the compo-
sition of a cortisol responder and a non-responder group pro-
vided an opportunity to test cortisol effects on memory. Cor-
tisol responders performed worse (in general) on the nal
memory test than non-responders because of their difference
in initial learning performance and forgetting rate. Individ-
uals with cortisol response showed lower learning rates than
non-responders during practice, and cortisol response was
associated with higher long-term forgetting. These ndings
suggest that cortisol response did not have an exclusive ef-
fect on retrieval. It seems that there is a general relationship
between individual differences in cortisol responsiveness
and the success of learning irrespective of the presence of
any stressors. In fact, previous studies have shown that there
is a relationship between glucocorticoid levels, the volume
of the hippocampus and memory performance (e.g.
Lindauer, Olff, Van Meijel, Carlier, & Gersons, 2006;
Lupien et al., 1998; Travis et al., 2016; for reviews, see, e.
g. Frodl & OKeane, 2013; Kim & Diamond, 2002). Accord-
ingly, in our study, greater cortisol responsiveness was asso-
ciated with reduced learning rate might be due to differential
hippocampal functioning in cortisol responders versus non-
responders. Nevertheless, despite their relatively low initial
learning performance and high forgetting rate, retrieval-
based learning was more benecial for long-term retention
than restudy practice in cortisol responders as well.
In a recent study, Smith, Floerke, and Thomas (2016) in-
vestigated the impact of acute psychosocial stress on the test-
ing effect. Similarly to our results, the authors found a strong
testing effect and no stress effects on memory immediately
after the stress exposure. However, in this study, stress had
a detrimental impact on the recall of the restudied items but
not on the recall of the retested items 20 minutes after stress
induction. In our study, cortisol response had a negative ef-
fect not only on the recall of restudied items but also on
the recall of retested items. A possible solution of this contra-
diction is an important methodological difference between
the present study and the study of Smith et al. (2016): in
our study, feedback was administered during practice. It
has been widely demonstrated that feedback during practice
enhances the retention benet of testing (e.g. Butler et al.,
2007, Butler & Roediger, 2008; Kang, McDermott, &
Roediger, 2007). In our experiment, recall improved steadily
during retrieval practice as a consequence of feedback, indi-
cating that some new learning occurred during practice.
Thus, elevated cortisol levels during nal recall acted on
memories acquired through the combination of study (as a
consequence of feedback) and retest. However, and impor-
tantly, cortisol did not inuence the benecial effect of re-
trieval practice over restudy as suggested by the fact that
we found no difference in the magnitude of the testing effect
between responders and non-responders. A possible aim of
future studies should be to compare the effect of cortisol re-
sponse (and stress) on retrieval-practised memories using
paradigms with and without feedback during testing.
In another study, Hinze and Rapp (2014) have demon-
strated that when retrieval practice occurred under high pres-
sure, the testing effect has become eliminated. At a rst
glance, the ndings of Hinze and Rapp (2014) seem to con-
tradict our results and also the results of Smith et al. (2016).
However, these contradictory ndings may stem from im-
portant methodological differences between these studies.
First, Hinze and Rapp (2014) did not manipulate and mea-
sure the level of acute stress. Instead, they manipulated the
pressure on task performance and the importance of the test
during practice. In contrast, our study and also the study of
Smith et al. (2016) manipulated the level of acute stress only
before the nal test and held constant the importance of the
task. These factors (such as the motivation level of the partic-
ipants and the level of anxiety) could have differential ef-
fects. Considering the results of Hinze and Rapp (2014), it
could be the case that the testing effect is unaffected by acute
stress only when the source of the stressor is not related to
the importance of the task and to the motivational level of
the participants.
Another important methodological difference is the
amount of retrieval practice. Hinze and Rapp (2014) applied
a single quiz-like test on complex scientic texts. In contrast,
in our study, participants repeatedly practised paired-
associate items in a cued recall task, whereas the participants
of Smith et al. (2016) repeatedly retrieved a list of items in a
free recall situation. It has been demonstrated that repeated re-
trieval practice increases the level of automatization of recall
(Racsmány et al., 2017). Because memories become more re-
sistant to various disturbing effects as a result of automatiza-
tion (Logan, 1988), we could assume that the automatization
of retrieval following retrieval practice is an important protec-
tive factor against the negative effects of acute stress.
From an applied perspective, our nding seems to be es-
pecially signicant, because there are several psychosocially
stressful situations in everyday life (e.g. school exams and
job interviews), when it is crucial whether the previously ac-
quired knowledge is accessible or not. The possible aim of
future research should be to investigate whether our results
on the relationship between cortisol levels and the testing ef-
fect can be generalized to real-world educational settings.
Furthermore, in fact, one session of testing more closely
Á. Szőllősi et al.
Copyright © 2017 John Wiley & Sons, Ltd. Appl. Cognit. Psychol. (2017)
represents a typical schooling situation. Because there are
examples of studies demonstrating the retention benetof
testing over restudy following only one practice block (see,
e.g. Hinze & Rapp, 2014), another aim of future studies
should be to investigate the relationship between stress and
the testing effect using one practice session. Finally, it
should be mentioned as a caveat that our conclusion that
acute stress does not harm the effect of retrieval practice is
based on a failure to reject the null hypothesis. Nevertheless,
according to our results, it seems that the long-term retention
benet of retrieval practice in comparison with rereading
(i.e. the testing effect) is insensitive to any aspects of the
stress protocol we used and also to the hormonal response
to stress.
ACKNOWLEDGEMENTS
We thank Petra Kovács, Dóra Molnár-Bakos and Bertalan
Polner for their help in data collection. This work was
supported by the KTIA NAP Grant (ID: 13-2-2014-0020).
Ágnes Szőllősi is supported by the ÚNKP-16-3-III New
National Excellence Program of the Ministry of Human
Capacities, Hungary.
REFERENCES
Buss, C., Wolf, O. T., Witt, J., & Hellhammer, D. H. (2004). Autobiograph-
ical memory impairment following acute cortisol administration.
Psychoneuroendocrinology,29, 10931096. https://doi.org/10.1016/j.
psyneuen.2003.09.006.
Butler, A. C., Karpicke, J. D., & Roediger, H. L. (2007). The effect of type
and timing of feedback on learning from multiple-choice tests. Journal of
Experimental Psychology: Applied,13, 273281. https://doi.org/10.1037/
1076-898X.13.4.273.
Butler, A. C., & Roediger, H. L. (2008). Feedback enhances the positive
effects and reduces the negative effects of multiple-choice testing.
Memory and Cognition,36, 604616. https://doi.org/10.3758/
MC.36.3.604.
Clow, A., Hucklebridge, F., Stalder, T., Evans, P., & Thorn, L. (2010). The
cortisol awakening response: More than a measure of HPA axis function.
Neuroscience and Biobehavioral Reviews,35,97103. https://doi.org/
10.1016/j.neubiorev.2009.12.011.
de Quervain, D. J., Henke, K., Aerni, A., Treyer, V., McGaugh, J. L.,
Berthold, T., Hock, C. (2003). Glucocorticoid-induced impairment
of declarative memory retrieval is associated with reduced blood ow
in the medial temporal lobe. European Journal of Neuroscience,17,
12961302. https://doi.org/10.1046/j.1460-9568.2003.02542.x.
de Quervain, D. J., Rozendaal, B., Nitsch, R. M., McGaugh, J. L., & Hock,
C. (2000). Acute cortisone administration impairs retrieval of long-term
declarative memory in humans. Nature Neuroscience,3, 313314.
https://doi.org/10.1038/73873.
Dempster, F. N. (1989). Spacing effects and their implications for theory
and practice. Educational Psychology Review,1, 309330. https://doi.
org/10.1007/BF01320097.
Frodl, T., & OKeane, V. (2013). How does the brain deal with cumulative
stress? A review with focus on developmental stress, HPA axis function
and hippocampal structure in humans. Neurobiology of Disease,52,
2437. https://doi.org/10.1016/j.nbd.2012.03.012.
Gyollai, A., Simor, P., Köteles, F., & Demetrovics, Z. (2011). Psychometric
properties of the Hungarian version of the original and the short form of
the Positive and Negative Affect Schedule (PANAS).
Neuropsychopharmacologia Hungarica,13(2), 7379.
Het, S., Rohleder, N., Schoofs, D., Kirschbaum, C., & Wolf, O. T. (2009).
Neuroendocrine and psychometric evaluation of a placebo version of
the Trier Social Stress Test.Psychoneuroendocrinology,34,
10751086. https://doi.org/10.1016/j.psyneuen.2009.02.008.
Hinze, S. R., & Rapp, D. N. (2014). Retrieval (sometimes) enhances learn-
ing: Performance pressure reduces the benets of retrieval practice. Ap-
plied Cognitive Psychology,28, 597606. https://doi.org/10.1002/
acp.3032.
Hupbach, A., & Fieman, R. (2012). Moderate stress enhances immediate
and delayed retrieval of educationally relevant material in healthy young
men. Behavioral Neuroscience,126, 819825. https://doi.org/10.1037/
a0030489.
Kang, S. H. K., McDermott, K. B., & Roediger, H. L. (2007). The format
and corrective feedback modify the effect of testing on long-term reten-
tion. European Journal of Cognitive Psychology,19, 528558. https://
doi.org/10.1080/09541440601056620.
Keresztes, A., Kaiser, D., Kovács, G., & Racsmány, M. (2014). Testing pro-
motes long-term learning via stabilizing activation patterns in a large net-
work of brain areas. Cerebral Cortex,24, 30253035. https://doi.org/
10.1093/cercor/bht158.
Kim, J. J., & Diamond, D. M. (2002). The stressed hippocampus, synaptic
plasticity and lost memories. Nature Reviews Neuroscience,3,
453462. https://doi.org/10.1038/nrn849.
Kirschbaum, C., & Hellhammer, D. H. (1994). Salivary cortisol in
psychoneuroendocrine research: Recent developments and applications.
Psychoneuroendocrinology,19, 313333. https://doi.org/10.1016/0306-
4530(94)90013-2.
Kirschbaum, C., Pirke, K. M., & Hellhammer, D. H. (1993). The Trier So-
cial Stress Test’—A tool for investigating psychobiological stress re-
sponses in a laboratory setting. Neuropsychobiology,28,7681. https://
doi.org/10.1159/000119004.
Kirschbaum, C., Wolf, O. T., May, M., Wippich, W., & Hellhammer, D. H.
(1996). Stress- and treatment-induced elevations of cortisol levels associ-
ated with impaired declarative memory in healthy adults. Life Sciences,
58, 14751483. https://doi.org/10.1016/0024-3205(96)00118-X.
Lindauer, R. J. L., Olff, M., Van Meijel, E. P. M., Carlier, I. V. E., &
Gersons, B. P. R. (2006). Cortisol, learning, memory, and attention in re-
lation to smaller hippocampal volume in police ofcers with posttrau-
matic stress disorder. Biological Psychiatry,59, 171177. https://doi.
org/10.1016/j.biopsych.2005.06.033.
Logan, G. D. (1988). Toward an instance theory of automatization. Psycho-
logical Review,95, 492527. https://doi.org/10.1037/0033-
295X.95.4.492.
Lupien, S. J., de Leon, M., de Santi, S., Convit, A., Tarshish, C., Nair, N. P.
V., Meaney, M. J. (1998). Cortisol levels during human aging predict
hippocampal atrophy and memory decits. Nature Neuroscience,1,
6973. https://doi.org/10.1038/271.
Lupien, S. J., Maheu, F., Tu, M., Fiocco, A., & Schramek, T. E. (2007). The
effects of stress and stress hormones on human cognition: Implications
for the eld of brain and cognition. Brain and Cognition,65, 209237.
https://doi.org/10.1016/j.bandc.2007.02.007.
Mason, J. W. (1968). A review of psychoneuroendocrine research on the
sympatheticadrenal medullary system. Psychosomatic Medicine,30,
631653.
McDaniel, M. A., Agarwal, P. K., Huelser, B. J., McDermott, K. B., &
Roediger, H. L. (2011). Test-enhanced learning in a middle school sci-
ence classroom: The effects of quiz frequency and placement. Journal
of Educational Psychology,103, 399414. https://doi.org/10.1037/
a0021782.
McDermott, K. B., Agarwal, P. K., DAntonio, L., Roediger, H. L., &
McDaniel, M. A. (2014). Both multiple-choice and short-answer quizzes
enhance later exam performance in middle and high school classes. Jour-
nal of Experimental Psychology: Applied,20,321. https://doi.org/
10.1037/xap0000004.
McEwen, B. S. (2008). Central effects of stress hormones in healthy and dis-
ease: Understanding the protective and damaging effects of stress and
stress mediators. European Journal of Pharmacology,583, 174185.
https://doi.org/10.1016/j.ejphar.2007.11.071.
Miller, R., Plessow, F., Kirschbaum, C., & Stalder, T. (2013). Classication
criteria for distinguishing cortisol responders from nonresponders to psy-
chosocial stress: Evaluation of salivary cortisol pulse detection in panel
designs. Psychosomatic Medicine,75, 832840. https://doi.org/10.1097/
PSY.0000000000000002.
Stress and testing effect
Copyright © 2017 John Wiley & Sons, Ltd. Appl. Cognit. Psychol. (2017)
Mulligan, N. W., & Picklesimer, M. (2016). Attention and the testing effect.
Journal of Experimental Psychology: Learning, Memory and Cognition,
42, 938950. https://doi.org/10.1037/xlm0000227.
Nater, U. M., La Marca, R., Florin, L., Moses, A., Langhans, W., Koller, M.
M., & Ehlert, U. (2006). Stress-induced changes in human salivary alpha-
amylase activityAssociations with adrenergic activity.
Psychoneuroendocrinology,31,4958. https://doi.org/10.1016/j.
psyneuen.2005.05.010.
Nater, U. M., Rohleder, N., Gaab, J., Berger, S., Jud, A., Kirschbaum, C., &
Ehlert, U. (2005). Human salivary alpha-amylase reactivity in a psycho-
social stress paradigm. International Journal of Psychophysiology,55,
333342. https://doi.org/10.1016/j.ijpsycho.2004.09.009.
Nelson, T. O., & Dunlosky, J. (1994). Norms of paired-associate recall dur-
ing multitrial learning of Swahili-English translation equivalents. Mem-
ory,2, 325335. https://doi.org/10.1080/09658219408258951.
OConnor, T. M., OHalloran, D. J., & Shanahan, F. (2000). The stress re-
sponse and the hypothalamicpituitaryadrenal axis: From molecule to
melancholia. Quarterly Journal of Medicine,93, 323333. https://doi.
org/10.1093/qjmed/93.6.323.
Oei, N. Y. L., Elzinga, B. M., Wolf, O. T., de Ruiter, M. B., Damoiseaux, J.
S., Joost, P., Rombouts, S. A. R. B. (2007). Glucocorticoids decrease
hippocampal and prefrontal activation during declarative memory re-
trieval in young men. Brain Imaging and Behavior,1,3141. https://
doi.org/10.1007/s11682-007-9003-2.
Pruessner, J. C., Dedovic, K., Khalili-Mahani, N., Engert, V., Pruessner, M.,
Buss, C., Lupien, S. (2008). Deactivation of the limbic system during
acute psychosocial stress: Evidence from positron emission tomography
and functional magnetic resonance imaging studies. Biological Psychia-
try,63, 234240. https://doi.org/10.1016/j.biopsych.2007.04.041.
Racsmány, M., Szőllősi, Á., & Bencze, D. (2017). Retrieval practice makes
procedure from remembering: An automatization account of the testing
effect. Journal of Experimental Psychology: Learning, Memory, and
Cognition, (Epub ahead of print, 29 Jul 2017). DOI: https://doi.org/
10.1037/xlm0000423.
Rawson, K. A., & Dunlosky, J. (2011). Optimizing schedules of retrieval
practice for durable and efcient learning: How much is enough? Journal
of Experimental Psychology: General,140, 283302. https://doi.org/
10.1037/a0023956.
Roediger, H. L., Agarwal, P. K., McDaniel, M. A., & McDermott, K. B.
(2011). Test-enhanced learning in the classroom: Long-term improve-
ments from quizzing. Journal of Experimental Psychology: Applied,17,
382395. https://doi.org/10.1037/a0026252.
Roediger, H. L., & Butler, A. C. (2011). The critical role of retrieval practice
in long-term retention. Trends in Cognitive Sciences,15,2027. https://
doi.org/10.1016/j.tics.2010.09.003.
Roediger, H. L., & Karpicke, J. D. (2006a). Test-enhanced learning: Taking
memory tests improves long-term retention. Psychological Science,17,
249255. https://doi.org/10.1111/j.1467-9280.2006.01693.x.
Roediger, H. L., & Karpicke, J. D. (2006b). The power of testing memory:
Basic research and implications for educational practice. Perspectives on
Psychological Science,1, 181210. https://doi.org/10.1111/j.1745-
6916.2006.00012.x.
Rohleder, N., Nater, U. M., Wolf, J. M., Ehlert, U., & Kirschbaum, C.
(2004). Psychosocial stress-induced activation of alpha-amylase: An indi-
cator of sympathetic activity. Annals of the New York Academy of Sci-
ences,1032, 258263. https://doi.org/10.1196/annals.1314.033.
Schlosser, N., Wolf, O. T., Fernando, S. C., Riedesel, K., Otte, C., Muhtz,
C., Wingenfeld, K. (2010). Effects of acute cortisol administration
on autobiographical memory in patients with major depression and
healthy controls. Psychoneuroendocrinology,35, 316320. https://doi.
org/10.1016/j.psyneuen.2009.06.015.
Schwabe, L., & Wolf, O. T. (2014). Timing matters: Temporal dynamics of
stress effects on memory retrieval. Cognitive, Affective, and Behavioral
Neuroscience,14, 10411048. https://doi.org/10.3758/s13415-014-
0256-0.
Sipos, K., Sipos, M., & Spielberger, C. D. (1994). A State and Trait Anxiety
Inventory (STAI) magyar változata (The Hungarian version of the State
and Trait Anxiety Inventory [STAI]). In F. Mérei, & F. Szakács (Eds.),
Pszichodiagnosztikai Vademecum, (pp. 123 148). Budapest: Nemzeti
Tankönyvkiadó.
Smith, A. M., Floerke, V. A., & Thomas, A. K. (2016). Retrieval practice
protects memory against acute stress. Science,354, 10461048. https://
doi.org/10.1126/science.aah5067.
Spielberger, C. D., Gorsuch, R. L., Lushene, R., Vagg, P. R., & Jacobs, G.
A. (1983). Manual for the State-Trait Anxiety Inventory. Palo Alto, CA:
Consulting Psychologists Press.
Travis, S. G., Coupland, N. J., Hegadoren, K., Silverstone, P. H., Huang,
Y., Carter, R., Malykhin, N. V. (2016). Effects of cortisol on hip-
pocampal subelds volumes and memory performance in healthy con-
trol subjects and patients with major depressive disorder. Journal of
Affective Disorders,201,3441. https://doi.org/10.1016/j.
jad.2016.04.049.
Tulving, E. (1967). The effects of presentation and recall of material in free-
recall learning. Journal of Verbal Learning and Verbal Behavior,6,
175184. https://doi.org/10.1016/S0022-5371(67)80092-6.
van den Broek, G. S., Takashima, A., Segers, E., Fernández, G., &
Verhoeven, L. (2013). Neural correlates of testing effects in vocabulary
learning. NeuroImage,78,94102. https://doi.org/10.1016/j.
neuroimage.2013.03.071.
Vaughn, K. E., & Rawson, K. A. (2011). Diagnosing criterion-level effects
on memory: What aspects of memory are enhanced by repeated retrieval?
Psychological Science,22, 11271131. https://doi.org/10.1177/
0956797611417724.
Watson, D., Clark, L. A., & Tellegen, A. (1988). Development and valida-
tion of brief measures of positive and negative affect: The PANAS scales.
Journal of Personality and Social Psychology,54, 10631070. https://
doi.org/10.1037/0022-3514.54.6.1063.
Weitzman, E. D., Fukushima, D., Nogeire, C., Roffwarg, H., Gallagher,
T. F., & Hellman, L. (1971). Twenty-four hour pattern of the episodic
secretion of cortisol in normal subjects. The Journal of Clinical Endo-
crinology and Metabolism,33,1422. https://doi.org/10.1210/jcem-33-
1-14.
Wiklund-Hörnqvist, C., Jonsson, B., & Nyberg, L. (2014). Strengthening
concept learning by repeated testing. Scandinavian Journal of Psychol-
ogy,55,17. https://doi.org/10.1111/sjop.12093.
Wolf, O. T. (2009). Stress and memory in humans: Twelve years of prog-
ress? Brain Research,1293, 142154. https://doi.org/10.1016/j.
brainres.2009.04.013.
Wolf, O. T., Convit, A., McHugh, P. F., Kandil, E., Thorn, E. L., De Santi,
S., de Leon, M. J. (2001). Cortisol differentially affects memory in
young and elderly men. Behavioral Neuroscience,115, 10021011.
https://doi.org/10.1037/0735-7044.115.5.1002.
Á. Szőllősi et al.
Copyright © 2017 John Wiley & Sons, Ltd. Appl. Cognit. Psychol. (2017)
... Subsequently, some pairs are put into a cued recall task (i.e., retrieval practice condition), while others are assigned to restudy (i.e., restudy condition). Finally, all studied pairs include a final cued recall test (Abel & Roediger, 2017;Buchin & Mulligan, 2017;Szőllősi et al., 2017). ...
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Two outstanding achievements of experimental memory research over the past fifty years have been the description of multiple memory systems and the demonstration that recall is the most effective form of long-term learning. The most important contribution of the former was to show that so-called declarative forms of memory can be described with different psychological characteristics and neurological background mechanisms than procedural memory, which plays a fundamental role in skill learning. Perhaps the most successful research trend in recent years has pointed out that memory recall, a declarative test, fundamentally changes memory representation and its long-term accessibility. In this chapter, we try to combine these two research fields and we aim to present the results of behavioral and brain research that support the assumption that declarative recall causes changes in retrieved memory content that are best understood within the mechanisms of the procedural memory system.
... Statistical analysis of the effectiveness of stress induction was the same as in prior studies [e.g., 51,52]. We conducted a mixed design ANOVA on cortisol levels as dependent variable, with TIME (t1, t2, and t3) as a within-subject factor, where t1 = immediately before stress/control procedure, t2 = 15 minutes after stress/control procedure, t3 = 45 minutes after stress/control procedure, and with STRESS EXPOSURE (stress or control) as a between-subject factor. ...
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Acute stress can crucially influence learning and memory processes. One of the key processes underlying human learning and memory is the ability of our brain to rapidly detect and extract regularities from sensory input across time and space leading to effective predictive processing. Here, we aimed to get an in-depth look into the effect of stress on the acquisition of two aspects of regularity extraction. We examined whether and how stress affects the learning (1) of probability-based regularities and (2) of serial order-based regularities in the same experimental design, and (3) the explicit access to the acquired information. Considering that the acquisition of probability-based regularities is a relatively rapid process, we primarily focused on the early phase of the task. We induced stress with the Socially Evaluated Cold Pressor Test in 27 young adults, while 26 participants were enrolled in the control group. Salivary cortisol levels and subjective ratings of affective states showed successful stress induction. After the stress induction, we measured regularity extraction with the cued Alternating Serial Reaction Time task. We found that stress promoted the extraction of probability-based regularities measured by the learning performance in the early phase of the task and did not alter the learning of serial order-based regularities. Post-block reports showed weaker explicit access to the serial order-based regularities in the stress group. Our results can contribute to a process-level understanding on how stress alters learning and memory functions related to predictive processes.
... Statistical analysis of the effectiveness of stress induction was the same as in prior studies (e.g. Guenzel et al., 2014a, Szőllősi et al., 2017. We conducted a mixed design ANOVA on cortisol levels as dependent variable, with TIME (t1, t2, and t3) as a withinsubject factor, where t1 = immediately before stress/control procedure, t2 = 15 minutes after stress/control procedure, t3 = 45 minutes after stress/control procedure, and with STRESS EXPOSURE (stress or control) as a between-subject factor. ...
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Acute stress can crucially influence learning and memory processes. A growing body of evidence shows that stress can induce a shift from cognitively demanding goal-directed to habitual, procedural forms of learning. However, the mechanisms underlying the shift are not yet understood. Here, we aimed to get an in-depth look into the effect of stress on the acquisition of procedural information with disentangling two aspects of procedural learning. We examined whether and how stress affects (1) processes and learning of probability-based information and (2) serial order-based information in the same experimental design, and (3) explicit access to the acquired information. Considering statistical learning, based on prior results, we primarily focused on the early phases of the task. We induced stress with the Socially Evaluated Cold Pressor Test in 27 young adults, while 26 participants were enrolled in the control group. Salivary cortisol levels and subjective ratings of affective states showed successful stress induction. After the stress induction, we measured procedural learning with the cued Alternating Serial Reaction Time task. We found that stress promoted the acquisition of probability-based information and did not alter the learning of order-based information. Post-block reports showed weaker explicit access to the order-based information in the stress group. Our results are in line with the theory of stress-induced memory shift and give a process-level understanding on how stress alters procedural learning.
... Das abrufgeübte Material war folglich vor negativen Stresseffekten auf das Erinnern im finalen Test geschützt. Demgegenüber scheinen im Hinblick auf indirekte Testungseffekte weder das testpotenzierte Lernen noch Vorwärtseffekte durch akuten psychosozialen Stress moderiert zu sein (Pastötter, von Dawans, Domes & Frings, im Druck;Szőllősi et al., 2017). ...
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Der Frage, wie Erinnern das Gedächtnis formt, wurde in der Kognitiven Psychologie in letzter Zeit große Aufmerksamkeit gewidmet. Testungseffekte, die in einer durch Gedächtnisabruf in der Folge verbesserten Zugänglichkeit von Gedächtniseinträgen bestehen, wurden in diesem Zusammenhang insbesondere auch hinsichtlich ihres pädagogischen Potentials diskutiert. Neben erleichterter Zugänglichkeit kann Gedächtnisabruf allerdings auch Vergessen nicht abgerufener Information verursachen. Der aktuelle Stand der Grundlagenforschung zu Abrufeffekten wird in diesem Überblicksartikel dargestellt und eine integrative Betrachtung unterschiedlicher Arten von Abrufeffekten unter Berücksichtigung wichtiger Moderatorvariablen versucht.
... Notably, in contrast to TPL (Szőllősi et al., 2017), the backward testing effect seems to be clearly 359 modulated by retrieval stress (e.g., Smith et al., 2016). This dissociation between studies suggests 360 that different cognitive mechanisms may contribute to direct (backward testing effect) and indirect 361 benefits of testing (TPL, FTE) and that these mechanisms may be differentially affected by stress. ...
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The forward testing effect (FTE) refers to the finding that testing of previously studied information enhances memory for subsequently studied other information. Previous research demonstrated that the FTE is a robust phenomenon that generalizes across different materials and populations. The present study examined whether the FTE is robust under acute psychosocial encoding/retrieval stress. In each of two experimental conditions, participants studied three item lists in anticipation of final cumulative recall testing. In the testing condition, participants were tested immediately on lists 1 and 2, whereas in the restudy condition, they restudied lists 1 and 2. In both conditions, participants were tested immediately on list 3. Acute psychosocial stress was induced in participants prior to the encoding of item lists using the Trier-Social-Stress-Test-for-Groups (TSST-G) protocol. No stress was induced in a control group. Salivary cortisol, alpha amylase, and subjective stress were measured repeatedly to capture the biopsychological stress response. The results showed a significant FTE on list 3 recall, i.e., testing in of lists 1 and 2 enhanced recall of list 3. No significant effect of stress on the FTE was observed, suggesting that the FTE is robust under acute psychosocial encoding/retrieval stress. The discussion provides suggestions for future research directions.
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Introduction The experience of stressful events can alter brain structures involved in memory encoding, storage and retrieval. Here we review experimental research assessing the impact of the stress-related hormone cortisol on long-term memory retrieval. Method A comprehensive literature search was conducted on PubMed, Web of Science and PsycNet databases with the following terms: “stress,” “long-term memory,” and “retrieval.” Studies were included in the review if they tested samples of healthy human participants, with at least one control group, and with the onset of the stress intervention occurring after the encoding phase and shortly (up to one hour) before the final memory test. Results Thirteen studies were included in the qualitative synthesis (N = 962) and were classified according to the time elapsed between stress induction and memory retrieval (stress-retrieval delay), the stress-inducing protocol (stressor), the time of day in which stress induction took place, sex, and age of participants. Most studies induced stress with the Trier Social Stress Test (TSST) between 15 and 25 minutes before the final memory (mostly recall) test and showed significant increases in cortisol levels and memory impairment. Discussion The reviewed studies indicate that stress does impair retrieval, particularly when induced with the TSST, in the afternoon, up to 45 minutes before the onset of the final memory test, in healthy young men. These results may inform future research on the impact of stress-induced cortisol surges on memory retrieval.
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Based on studies demonstrating that testing promotes better long-term retention than restudying (i.e., the testing effect), testing has been recommended as a powerful tool to boost knowledge acquisition in educational settings. However, a factor ubiquitous in real-life learning contexts has been ignored to date: the learner's affective state. To examine whether the learner's affective state influences the testing effect, we conducted two experiments. We employed a standard testing-effect paradigm consisting of an initial study phase and a subsequent restudy/testing phase, and induced negative, neutral, or positive affective states either before participants initially studied short expository texts (Experiment 1) or before they restudied or were tested on them (Experiment 2). After one week, memory for the texts was tested. In both experiments, previously tested material was better remembered than previously restudied material. However, in none of the experiments, did the memory advantage of testing over restudying vary as a function of affect condition. Hence, the present results suggest that testing seems to benefit long-term retention independently of the learner's affective state.
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The “testing effect” refers to the striking phenomenon that repeated retrieval practice is one of the most effective learning strategies, and certainly more advantageous for long-term learning, than additional restudying of the same information. How retrieval can boost the retention of memories is still without unanimous explanation. In 3 experiments, focusing on the reaction time (RT) of retrieval, we showed that RT of retrieval during retrieval practice followed a power function speed up that typically characterizes automaticity and skill learning. More important, it was found that the measure of goodness of fit to this power function was associated with long-term recall success. Here we suggest that the automatization of retrieval is an explanatory component of the testing effect. As a consequence, retrieval-based learning has the properties characteristic of skill learning: diminishing involvement of attentional processes, faster processing, resistance to interference effects, and lower forgetting rate.
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The aim of this study was to examine whether repeated testing with feedback benefits learning compared to rereading of introductory psychology key-concepts in an educational context. The testing effect was examined immediately after practice, after 18 days, and at a five-week delay in a sample of undergraduate students (n = 83). The results revealed that repeated testing with feedback significantly enhanced learning compared to rereading at all delays, demonstrating that repeated retrieval enhances retention compared to repeated encoding in the short- and the long-term. In addition, the effect of repeated testing was beneficial for students irrespectively of working memory capacity. It is argued that teaching methods involving repeated retrieval are important to consider by the educational system.
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More than a decade of research has supported a robust consensus: Acute stress impairs memory retrieval. We aimed to determine whether a highly effective learning technique could strengthen memory against the negative effects of stress. To bolster memory, we used retrieval practice, or the act of taking practice tests. Participants first learned stimuli by either restudying or engaging in retrieval practice. Twenty-four hours later, we induced stress in half of the participants and assessed subsequent memory performance. Participants who learned by restudying demonstrated the typical stress-related memory impairment, whereas those who learned by retrieval practice were immune to the deleterious effects of stress. These results suggest that the effects of stress on memory retrieval may be contingent on the strength of the memory representations themselves.
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Overactivity of the hypothalamic-pituitary-adrenal (HPA) axis in major depressive disorder (MDD) is among the most consistently replicated biological findings in psychiatry. Magnetic resonance imaging (MRI) studies have consistently demonstrated that hippocampal (HC) volume is decreased in patients with MDD. The improved spatial resolution of high field strength MRI has recently enabled measurements of HC subfield volumes in vivo. The main goal of the present study was to examine the relationship between cortisol concentrations over a day and HC subfield volumes in patients with MDD compared to healthy controls and to investigate whether diurnal cortisol measures are related to memory performance. Fourteen MDD patients with moderate or severe episodes were recruited, together with 14 healthy controls. Imaging was performed using a 4.7 T whole-body imaging system. HC subfields and subregions were segmented manually using previously defined protocol. Memory performance was assessed using the Wechsler Memory Scale IV. The salivary cortisol levels were measured over the course of one day. We found that cortisol awakening response to 8 h (CAR-8 h) was higher in MDD patients compared to controls and that this increase in CAR-8 h in MDD patients correlated negatively with left total Cornu Ammonis (CA)1–3 and left HC head volume. In healthy controls mean cortisol levels were negatively associated with right total CA1–3, right HC head, and right total HC volume. In addition, in healthy controls higher CAR-8 h was related to worse performance on the immediate content memory. These results provide the first in vivo evidence of the negative associations between cortisol level, CA1-3 HC subfield volume and memory performance in patients with MDD and healthy controls.
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Memory retrieval often enhances still later memory as evidenced by the testing effect. Divided attention (DA) is known to produce different effects on encoding and retrieval, substantially disrupting the former and often producing little effect on the latter. The present experiments examine whether the mnemonic consequences of retrieval are similarly resilient in the face of distraction or if they have a similar sensitivity to DA as study-based encoding. In 2 experiments, participants initially studied a set of word pairs (Phase 1) then engaged in restudy of some pairs and retrieval practice of others (Phase 2), followed by either an immediate or (24-hr) delayed final cued-recall test (Phase 3). Phase 2 restudy and retrieval practice occurred under full attention (FA) or DA. Phase 2 performance replicated earlier research in finding little effect of DA on retrieval success, and greater disruption to the secondary task in the retrieval than restudy condition. More importantly, the testing effect on the final test (the difference between the retrieval and restudy conditions) was greater in the DA than FA condition. Final recall was substantially reduced by DA in the restudy condition but not in the retrieval condition. This pattern was found for related and unrelated word pairs, with feedback during retrieval practice and without, for immediate as well as delayed final tests, and for high as well as low performance on the secondary task. The encoding effects of retrieval appear to be more resilient in the face of distraction than the encoding effects of restudy. (PsycINFO Database Record
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Academic testing has received substantial support as a useful educational activity with robust retention benefits, given that tests can promote retrieval practice. However, testing can also instantiate performance-related pressure and anxiety that may misappropriate the resources responsible for producing learning benefits. The current project examined the effects of performance pressure on retrieval practice. In two experiments, we instantiated performance pressure with either high-stakes or low-stakes quizzes, and assessed memory and comprehension of content on both quizzes and final tests. Quiz performance was equivalent under high-stakes and low-stakes conditions, demonstrating that learners adapted to high-pressure quizzes. However, final test performance was better after low-stakes versus high-stakes quizzes, and only low-stakes quizzes led to a performance advantage over a rereading control group. Participants additionally exhibited some sensitivity to the difficulty of retrieving under pressure. These data highlight the benefits of retrieval practice but indicate that they can be disrupted under pressure-driven conditions. Copyright © 2014 John Wiley & Sons, Ltd.
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Stress may impair memory retrieval. This retrieval impairment has been attributed to the action of the stress hormone cortisol, which is released with a delay of several minutes after a stressful encounter. Hence, most studies tested memory retrieval 20-30 min after stress, when the stress-induced cortisol increase peaks. In the present experiment, we investigated whether retrieval impairments can also be found at later intervals after stress. To this end, participants learned a list of words on day 1. Twenty-four hours later, they were first exposed to a stressor or a nonstressful control manipulation and completed a recognition test for the words either immediately thereafter, 25 min later, or 90 min later. Our findings showed that stress did not impair memory retrieval when memory was tested immediately after the stressor, before cortisol levels were elevated. However, retrieval performance was impaired 25 min after stress, when cortisol levels peaked, as well as 90 min after the stressor, when cortisol levels had already returned to baseline. The retrieval impairment 90 min after stress appeared to be even stronger than the one after 25 min. These findings suggest that the detrimental effects of stress on retrieval performance may last longer than is usually assumed.
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This article presents a theory in which automatization is construed as the acquisition of a domain-specific knowledge base, formed of separate representations, instances, of each exposure to the task. Processing is considered automatic if it relies on retrieval of stored instances, which will occur only after practice in a consistent environment. Practice is important because it increases the amount retrieved and the speed of retrieval; consistency is important because it ensures that the retrieved instances will be useful. The theory accounts quantitatively for the power-function speed-up and predicts a power-function reduction in the standard deviation that is constrained to have the same exponent as the power function for the speed-up. The theory accounts for qualitative properties as well, explaining how some may disappear and others appear with practice. More generally, it provides an alternative to the modal view of automaticity. (PsycINFO Database Record (c) 2006 APA, all rights reserved)