Emotion

2011, Vol. 11, No. 1, 1219

2010 American Psychological Association

1528-3542/10/$12.00 DOI: 10.1037/a0020288

Emotion Enhanced Retention of Cognitive Skill Learning

Stephan Steidl, Fathima Razik, and Adam K. Anderson
University of Toronto and Rotman Research Institute, Toronto, ON, Canada
Ample evidence suggests that emotional arousal enhances declarative/episodic memory. By contrast,
there is little evidence that emotional enhancement of memory (EEM) extends to procedural skill based
memory. We examined remote EEM (1.5-month delay) for cognitive skill learning using the weather
prediction (WP) probabilistic classification task. Participants viewed interleaved emotionally arousing or
neutral pictures during WP acquisition. Arousal retarded initial WP acquisition. While participants in the
neutral condition showed substantial forgetting of WP learning across the 1.5-month delay interval, the
arousal condition showed no evidence of forgetting across the same time period. Thus, arousal during
encoding determined the mnemonic fate of cognitive skill learning. Emotional enhancement of WP
retention was independent of verbally stated knowledge of WP learning and EEM for the picture contexts
in which learning took place. These results reveal a novel demonstration of EEM for cognitive skill
learning, and suggest that emotional arousal may in parallel enhance the neural systems that support
procedural learning and its declarative context.
Keywords: emotional enhancement of memory, weather prediction task, explicit memory, striatum,
implicit memory

using structural equation modeling demonstrates greater

amygdala-parahippocampal interactions during emotionally arousing relative to neutral event encoding, potentially representing the
neural bases of EEM for declarative/epidsodic memory (Kilpatrick
& Cahill, 2003). Collectively, these studies suggest an interaction
between sympathetic arousal, the amygdala, and a hippocampalbased declarative memory system that supports conscious recollection of past experiences (Kilpatrick & Cahill, 2003; Hamann,
2001; LaBar & Cabeza, 2006; Packard & Cahill, 2001).
Although the psychological and neural bases of EEM have been
extensively studied with respect to declarative/episodic memory,
storage of past events is accomplished through multiple qualitatively distinct memory systems in the brain, each acquiring different types of information (Cohen & Squire, 1980; Knowlton, Mangels, & Squire, 1996; McDonald & White, 1993; Packard, Hirsh,
& White, 1989; Schacter & Tulving, 1994; White & McDonald,
2002). Traditionally, a distinction has been made between a
hippocampus-based declarative and a striatum-based nondeclarative/procedural memory system (Cohen & Squire, 1980). For
example, different versions of a 8-arm radial maze task, designed
to emphasize different forms of learning, have been shown to
dissociate the contributions of the hippocampus (a task based on
spatial cues in the environment) and dorsal striatum (a task based
on stimulusresponse associations), suggesting that each brain area
acquires different information about task situations (McDonald &
White, 1993). These data are consistent with the notion that the
dorsal striatum in rats is associated with stimulus-response habittype learning.
In rodents, the amygdala has been shown to modulate spatial
and cue-based memory tasks in parallel (McGaugh, 2004;
McGaugh, McIntyre, & Power, 2002; Packard & Cahill, 2001;
Packard, Cahill, & McGaugh, 1994). For example, posttraining
intraamygdala injection of the catecholaminergic agonist
d-amphetamine has been shown to enhance retention on both

Emotional events are surrounded with a special subjective vividness and are thought to persist in memory unlike more mundane
events. Both human and animal research has consistently implicated the importance of sympathetic arousal and the amygdala in
this emotional enhancement of memory (EEM) (for review, see
Cahill & McGaugh, 1999). In particular postencoding manipulation of noradrenergic activation in the amygdala appears to mediate the effect of sympathetic activation on memory consolidation
(McIntyre, Power, Roozendaal, & McGaugh, 2003; Roozendaal,
Castello, Vedana, Barsegyan, & McGaugh, 2008). In humans, both
positron emission tomography (PET) and functional MRI (fMRI)
studies have shown that amygdala activation during encoding
(Cahill et al., 1996; Canli, Zhao, Brewer, Gabrieli, & Cahill, 2000;
Dougal, Phelps, & Davich, 2007; Kensinger & Schacter, 2005) and
recall (Sharot, Delgado, & Phelps, 2004) is correlated with greater
explicit memory for emotionally arousing material. In contrast
with valence specific contributions (i.e., positive or negative),
which are more associated with the prefrontal cortices (Kensinger
& Corkin, 2005; Phelps, LaBar, & Spencer, 1997), amygdala
influences on memory formation are most associated with the
intensity of emotional experience, or arousal, common to both
positive and negative events (Cahill & McGaugh, 1999; Hamann,
Ely, Grafton, & Kilts, 1999). Examination of neuroimaging data

This article was published Online First November 8, 2010.

Stephan Steidl, Fathima Razik, and Adam K. Anderson, Department of
Psychology, University of Toronto, and Baycrest Centre, Rotman Research
Institute, Toronto, ON, Canada.
We thank Rifat Alam for help in editing this article. Supported by an
NSERC grant to AKA and an NSERC CGS-D to SS.
Correspondence concerning this article should be addressed to Adam K.
Anderson, Department of Psychology, University of Toronto, 100 St.
George Street, Toronto, ON M5S 3G3 Canada. E-mail: anderson@psych
.utoronto.ca
12

AROUSAL AND COGNITIVE SKILL LEARNING

spatial and cued versions of the water maze task (Packard et al.,
1994). This work from nonhuman animals suggests that sympathetic arousal during emotional states should play a pervasive
neuromodulatory role in enhancing memory formation in putatively different memory systems.
Whereas much evidence supports the role of emotional arousal
and the amygdala in modulating human declarative memory, there
is little evidence to support a similar role in nondeclarative procedural memory. One way habit learning in humans has previously
been assessed is by using the weather prediction task (WP), a
probabilistic classification task in which subjects are required to
classify combinations of visually distinctive cues as predicting one
of two weather outcomes (i.e., sunshine or rain). The cue combinations and their outcomes are probabilistically associated so
explicit memorization of their relationship is difficult. Instead,
performance of this task is more easily accomplished through the
implicit learning of complex cue-outcome contingencies that are
thought to, at least in part, depend on the striatum (Knowlton,
Squire, & Gluck, 1994). Early phases of WP task acquisition are
intact in medial temporal lobe amnesiacs but disrupted in patients
with striatal dysfunction associated with Parkinsons disease
(Knowlton et al., 1994). Event-related fMRI shows medial temporal lobe activation very early on during WP acquisition (Poldrack et al., 2001), that quickly becomes deactivated, while the
striatum comes to dominate (Poldrack et al., 2001; Poldrack,
Prabhakaran, Seger, & Gabrieli, 1999).
Studies in humans have shown that emotions can facilitate as well
as inhibit the use of stimulus-response learning strategies (Thomas &
LaBar, 2008; Schwabe et al., 2007). For example, Thomas and LaBar
(2008) showed that emotional arousal during encoding of skill learning, as indexed by a variant of the WP task (Knowlton et al., 1994),
resulted in more optimal strategy use during a second Session 24 hr
later. However, it remains unclear whether emotional arousal enhances long term memory for procedural learning. A prior study used
the WP task to investigate the effects of emotional arousal during
cognitive skill acquisition on long-term retention (Steidl, Mohi-uddin,
& Anderson, 2006). WP trials were interrupted by intermittent emotional arousal by showing subjects either highly arousing (e.g., a
mutilated body) or neutral (e.g., a building) pictures. Subjects returned
to the lab one week later and were asked to complete another WP
session. While neither initial learning nor 1-week retention of WP
learning was significantly affected, there was a robust enhancement of
recognition memory for the arousing context (i.e., picture recognition)
in which WP learning occurred. This suggested that the effects of
emotional arousal on procedural and declarative/episodic memory
may be dissociable. This potential dissociation between emotional
influence on declarative/episodic and cognitive skill learning, however, is complicated by two factors: (a) this prior study examined
further WP learning as an index of memory, which can obscure how
emotional arousal modulates retention and (b) procedural and declarative memory may have different time courses of forgetting. With
respect to the latter, emotional influences on memory consolidation
are typically manifested as enhanced retention/resistance to forgetting
as delay between study and test increases, with relative maintenance
of memory for emotionally arousing events and more precipitous
forgetting for neutral events (Kleinsmith & Kaplan, 1963; LaBar &
Phelps, 1998; Sharot & Phelps, 2004). As various forms of implicit
memory are maintained in memory over long periods (Schacter,
1987), it may be difficult to visualize EEM for procedural learning

13

because of limited forgetting over shorter study-test delays. Indeed, in

our previous study (Steidl et al., 2006), preliminary data from a small
subset (n 5) of participants suggested EEM for skill learning may
only be present after memory decay following long delays (3 months).
In the present study we followed up this preliminary observation
by examining EEM for WP cognitive skill learning over a long
retention delay (1.5 months) that permits sufficient forgetting. As
emotionally significant pictures evoke both sympathetic arousal
and amygdala activation and have been linked to enhanced memory for surrounding neutral contexts (Canli et al., 2000; Hamann et
al., 1999; Anderson, Wais, & Gabrieli, 2006; Maratos, Dolan,
Morris, Henson, & Rugg, 2001), we hypothesized that emotional
arousal and associated amygdala recruitment evoked by interleaved emotionally arousing pictures should enhance WP memory
when tested at a long delay. This would provide evidence that
EEM extends to the long-term retention of skill learning.

Materials and Method

Participants
Participants were recruited through advertisements posted
throughout the University of Toronto campus as well as through
introductory psychology classes. A total of 44 participants (age
range 1726) participated in the study which involved two
sessions separated by 1.5 months. Participants were randomly
assigned to either the arousal condition (n 21; 10 men), or the
neutral condition (n 23; 16 men). The average test-retest delay
was 46 3 days for the neutral and 46 2 days for the arousal
condition. One participant in the neutral condition was removed
from analysis because of performing 2.5 SDs below the mean at
the end of training (22% accuracy).

The WP Task
All participants performed the weather prediction task on a computer (adapted from Knowlton et al., 1996). The WP task was designed using Super Lab (Version 2.0, Cedrus Inc.) and viewed
through a 17 in. flat screen LCD monitor. Participants were presented
with varying combinations of four types of cues depicting simple
geometric forms: 7 black squares, 10 black triangles, 9 black circles,
or 13 black diamonds. On each trial combinations of one, two, or three
of these cues were presented side by side on the computer screen (14
possible cue combinations; Table 1) and individuals were asked to
predict the weather outcome as either sunshine or rain by pressing one
of two keys indicated on a keyboard. Each of the four cards was
associated with an outcome of rain or sunshine with a fixed probability. Feedback was given after each response to indicate a correct or
incorrect response. In the event of a correct response, participants
heard a high pitch sound and were shown a happy face as well as a
text message informing them that they were correct. In the event of an
incorrect response participants heard a low pitch buzzer tone and were
shown a sad face as well as a text message informing them that they
were incorrect and indicating the correct answer. A total of 150 trials
were presented to each subject. Within each trial, a particular card
configuration was presented for 5 seconds and participants had to
respond within this time. After the selection was entered, feedback
was presented for 2 s. Five self-paced introductory instruction screens
appeared at the beginning of the experiment.

STEIDL, RAZIK, AND ANDERSON

14

Table 1
Weather Prediction Task Probability Structure Taken From
Reber, Knowlton, and Squire (1996)
Cue no.

Cue
arrangement

Frequency

Sun

Rain

1
2
3
4
5
6
7
8
9
10
11
12
13
14

1100
1110
1000
1010
0100
1001
0110
1011
1101
0010
0101
0001
0111
0011

4
1
7
4
5
2
2
2
2
5
4
7
1
4

4
1
6
3
3
1
1
1
1
2
1
1
0
0

0
0
1
1
2
1
1
1
1
3
3
6
1
4

P(Sunshine)
1
1
.86
.75
.60
.50
.50
.50
.50
.40
.25
.14
0
0

Note. The numbers in the cue combination column refer from left to right
to cues 1 to 4: A 1 indicates that a cue is present on a trial, while a 0
indicated that a cue is absent on a trial. Frequency indicates how often a
particular combination occurs out of 50 trials. Sunshine and rain indicated
how often each outcome occurs. The final column indicates the probability
that an outcome (sunshine in this case) will occur.

Emotional arousal was manipulated by showing participants

emotionally arousing or neutral pictures between every third WP
trial (approximately every 20 s). Participants in both arousal and
neutral groups were asked to evaluate the intensity of their emotional response to a presented picture, that is, the subjective correlate of peripheral physiological arousal and amygdala activity
(Anderson et al., 2003; Canli et al., 2000; Hamann et al., 1999) in
response to the question How intense do you feel? As arousal
common to both negative and positive valence most strongly
characterizes amygdala contributions to EEM (Hamann et al.,
1999), we randomized presentations of positive and negative pictures, and as such were not interested in valence specific contributions to memory formation (Kensinger & Corkin, 2004). The
pictures were selected from the International Affective Picture
Systems (IAPS, Lang, Bradley, & Cuthbert, 2005). A total of 50
pictures were presented. In the arousal condition, 80% of the
pictures were selected from those catalogued in the IAPS as having
high valence (20 positive and 20 negative) and high arousal, while
20% of the pictures were neutral with low valence and low arousal.
Inclusion of negative, positive, and neutral pictures was expected
to limit habituation and thus evoke more consistently intense
emotional responses for arousing pictures. Neutral pictures also
served as an additional measure of the influence of evoked emotional arousal on memory for the episodic picture context of WP
learning. For the neutral condition, all selected pictures were
neutral in valence and low in arousal. Neutral pictures depicted
people engaging in everyday situations (e.g., writing, or looking
out of a window), scenery or flora (e.g., plants and trees), or
common objects (e.g., rolling pin, fan, clothing items). In this
paper, the term context will be used to refer to the IAPS pictures
intermittently presented during WP acquisition, as it provides a
direct index of episodic memory for the events surrounding WP
learning.

Transfer Task
After completion of the WP task during Session 1, we administered a transfer task to assess the subjects ability to state the
subjective probability of rain or sunshine (Reber, Knowlton, &
Squire, 1996). Subjects were shown either each of the four single
cue cards individually, the six possible combinations of cue card
pairs, or the three possible combinations of cue card triplets (see
Table 1), and asked the question: If just this card/these cards are
showing, what percentage of time will it be sunny?

Retention Task
Participants were asked to return to the laboratory 1.5 months
after the initial session. To assess retention of previous WP learning, participants were asked to complete 150 WP trials. This
session was conducted as described for Session 1, except that there
was no feedback given or arousal manipulation due to interleaved
pictures.

Picture Recognition Task

Following WP retention testing, participants were given a recognition task for the pictures encountered during the first session,
as an index of contextual memory. Seventy-five pictures were
shown in the recognition task, of which 50 had been previously
seen in Session 1, and 25 were new foil items. The 25 foil items
were matched thematically with previously seen items to increase
memory discrimination difficulty (10 positive, 10 negative, and 5
neutral). Participants in the neutral condition were presented with
50 neutral old pictures and 25 neutral foil items. Subjects in both
groups were asked to indicate whether or not a given picture had
been previously encountered with a yes/no response.

Data Acquisition and Analysis

Analyses described below were first conducted with gender
included as a between-participants factor. However, in no case was
there any main effect or interaction with sex, so data from men and
women were collapsed for statistical analysis.

Picture Context Recognition

The picture recognition data was analyzed for accuracy by
subtracting the proportion of responses to new pictures (i.e., false
alarms) from the proportion of responses to old pictures (i.e., hits).

WP Task
Following prior studies, a response was scored as accurate if it
was associated with the most likely outcome. Performance on trials
that had a 50% chance of being rain or sunshine were not scored,
as they did not provide any indication of learning across trials. The
150 trials were split into 5 blocks of 30 trials each. Consolidation
of implicit learning on the WP task across the 1.5 month period
separating Session 1 and the retrieval test in Session 2 was assessed by comparing the end of Session 1 (block 5) with Session
2. Data were collapsed across the 150 trials in Session 2 as no
feedback was provided to allow a more pure measure of retention.

AROUSAL AND COGNITIVE SKILL LEARNING

Subjects were asked to evaluate the intensity of their emotional

responses to interleaved pictures during WP learning. An independent samples t test comparing self-reported arousal ratings in the
arousing (collapsed across negative and positive) and neutral conditions revealed greater self-reported arousal in the arousal condition (5.7 0.3 and 2.9 0.31 in arousal and neutral conditions,
respectively), t(42) 6.32, p .0001, d 1.95.

Picture Context Recognition

After 1.5 months subjects were given a recognition test for
picture contexts seen during initial WP learning. An independent
samples t test revealed there was a significantly higher number of
hits, t(42) 5.02, p .0001, d 1.44, as well as a trend toward
fewer false alarms, t(42) 2.01, p .051, in the arousing relative
to the neutral condition. Thus, mean corrected picture recognition
(hitsfalse alarms) was significantly more accurate in the arousing
(collapsed across picture types) relative to the neutral condition,
t(42) 5.39, p .001, d 1.66. Specifically, arousing pictures
in the arousing condition (60% hits and 6.6% false alarms) were
better remembered than neutral pictures in the neutral condition
(44.5% hits and 9.5% false alarms), t(42) 5.37, p .001, d
1.66. Moreover, this enhanced memory extended to neutral pictures in the arousal condition (52.4% hits and 6.3% false alarms),
which were better remembered than neutral pictures in the neutral
condition, t(42) 3.47, p .01, d 1.07 (Figure 1a). In
summary, arousal was associated with enhanced memory for surrounding WP picture context.

Weather Prediction
WP acquisition. Data were submitted to a two-way ANOVA
with acquisition block (15) and encoding condition (arousal vs.
neutral) as within and between subject factors, respectively. A
main effect of training block, F(4, 168) 5.86, p .001, 2
0.122 confirmed that overall participants showed significant WP
acquisition across trial blocks, increasing linearly from block 1 to
5, F(1, 168) 23.22, p .001, 2 0.104. A main effect of
condition revealed participants overall performance in the arousal
condition was significantly lower compared to the neutral condition, F(1, 42) 11.41, p .002, 2 0.214 (Figure 1b). In
addition, there was a marginally significant interaction between
arousal condition and training block, F(4, 168) 2.19, p .07.
Separate analysis of the two encoding conditions confirmed successful WP learning across trial blocks, with performance increasing from beginning to end of acquisition (block 1 to 5), in both the
neutral, F(1, 88) 21.31, p .001, 2 0.145 and the arousal

Arousal

60

Arous-Neut
Neutral
50

40

30

70

60

50

Neutral
Arousal

40

20

b1

Encoding condition

b2

b3

b4

b5

Training block

D
80

80

70

70
Percent correct

Arousal Ratings

Corrected recognition (%) sem

Results

B
80

Percent correct

The 14 different cue types were collapsed to represent 5 levels

of cue-outcome predictability (5, 33, 50, 68, and 95%). Transfer
task performance was analyzed using a mixed measures ANOVA
with cue-outcome probability (5 to 95%) as the repeated measures
factors and encoding condition (arousal vs. neutral) as the between
subjects factor.

WP percent correct sem

Transfer Task

15

60

50

60

50

40

40

Study

Test

Study

Test

Time

Figure 1. (A) Remote (1.5 months) picture recognition memory for the
arousal and neutral encoding conditions. Arousal arousing pictures in the
arousal condition; Arous-Neut neutral pictures in the arousal condition;
Neutral neutral pictures in the neutral condition. (B) WP acquisition
curves for neutral and arousal conditions in Session 1. (C) Retention of WP
learning across a 1.5 month delay. Study refers to performance from the
final training block in Session 1. Test retention test. (D) Retention of WP
learning across a 1.5 month delay in participants matched for performance
at the end of Session 1. Study refers to performance from the final training
block in Session 1. Test retention test.

condition, F(1, 80) 4.16, p .05, 2 0.064, but statistically

more robust in the former.
Transfer task. To estimate the influence of arousal on transference of declarative knowledge (i.e., those that participants could
verbally state) regarding contingencies learned in the WP task
(Reber et al., 1996), participants estimated the percent likelihood
of sunshine for each of the cue card combinations. Transfer task
data from one subject from the arousal condition was lost. Estimation of sunshine depended on cue-outcome predictability, F(4,
164) 25.9, p .001, 2 .387. However, there was no main
effect or interaction with encoding condition, Fs 1.10. Both
encoding conditions tended to overestimate the least predictive and
underestimate the most predictive events, even those with cueoutcome contingencies with 95% diagnosticity, F(1, 41), p
.63, (Percent max sunshine 95%, neutral 65.28%, SD
25.37; arousal 61.73%, SD 22.21) where explicit memory
would likely have been greatest.
Retention. Participants returned 1.5 months later and were
asked to complete 150 WP trials without any feedback. This

16

STEIDL, RAZIK, AND ANDERSON

allowed assessment of the effects of arousal level during initial WP

acquisition on long-term retention. Neither subjects in the arousal,
F(4, 80) 1.88 p .12, nor neutral conditions, F(4, 88) 1.61
p .17, showed significant differences across retention trial
blocks; thus, data from the retrieval session was collapsed for
further analyses. To examine retention and its interaction with
encoding condition, data were submitted to a two-way ANOVA
with encoding condition (arousal vs. neutral) and delay (block 5 of
Day 1 vs. 1.5 months collapsed across blocks) as between and
within subject factors, respectively. There was a main effect of
session, F(1, 42) 13.77, p .001, 2 0.247, demonstrating
that the 1.5 month delay resulted in significant forgetting of WP
learning. This main effect of session was modified by a significant
interaction between session and encoding condition, F(1, 42)
10.66, p .003, 2 0.202. While participants in the neutral
condition showed substantial forgetting across the 1.5 month delay
interval, F(1, 22) 22.58, p .001, 2 0.507, the arousal
condition showed no evidence of forgetting across the same time
period, F 1 (Figure 1c).
To examine whether this effect of arousal on retention was an
artifact of enhanced performance in the neutral condition during
initial learning, we removed the top performers in the neutral
condition (n 12, leaving 11) and the bottom (n 11, leaving 11)
performers in the arousal condition to equate performance at the
end of acquisition (Figure 1d). This performance matching resulted
in statistically equivalent levels of overall learning at the end of
acquisition (arousal 62.4, SE 3.1 vs. neutral 64.8, SE
2.3; F(1, 32) 1), as well as matched performance on two indices
of declarative memory: (a) WP acquisition of the most highly
diagnostic cues (95% diagnosticity), F(1, 32) 1; and (b)
verbally declared knowledge in the transfer task performance for
highly diagnostic cues, F(1, 31) 1. Despite this statistical matching between the arousal and neutral conditions at the end of
training, there remained a significant effect of delay, F(1, 32)
8.23, p .008, 2 0.204 as well as an interaction with encoding
condition, F(1, 32) 6.12, p .02, 2 0.160. Participants in the
neutral, F(1, 12) 10.24, p .008, 2 0.460, but not the
arousal condition, F 1, demonstrated robust forgetting 1.5
months later (Figure 1d). Thus, greater retention of WP learning in
the arousal condition was not a reflection of the poorer performance during initial training.

Relation Between WP Acquisition and Retention

We next more closely examined individual data to better understand how emotional arousal may potentially alter retention of WP
learning. Inspection of the individual differences in retention revealed
that half of the arousal group showed evidence of WP performance
increasing over the 1.5 month delay, a much higher level of occurrence relative to the neutral group (52.4 vs. 8.7% of participants,
2(1) 10.06, p .002). Greater incidence of this hypermnesia was
present even after matching performance between the arousal and
neutral groups at the end of acquisition (52.4 vs. 9.1% of participants,
2(1) 7.02, p .009). This greater incidence of memory improvement with time was thus not a reflection of the poorer performance
during initial training. Furthermore, performance at the end of acquisition in performance-matched subjects was significantly correlated
with greater retention in the arousal (r .47, p .05), but not the
neutral group (r .16, p .5). This suggests that greater initial

learning was associated with enhanced remote retention in the arousal

but not neutral encoding conditions.

Relation Between Picture Context Memory

and WP Retention
We next assessed the relationship between WP retention and memory for WP picture contexts. If enhanced WP retention in the arousal
condition was supported by episodic/declarative memory, then WP
retention may correlate with enhanced memory for the picture context. We found that arousal-enhanced WP retention was independent
from picture context memory, r .165, F(1, 19) 1. Further, this
independence characterized memory for WP retention and picture
context memory not only for intrinsically arousing pictures, r .14,
F(1, 19) 1, but also for enhanced memory of neutral pictures
studied in an arousing context, r .19, F(1, 19) 1. This dissociation did not reflect insufficient variability on either WP retention
(SD 17.8%, minmax spread 64.5%) or picture context recognition (SD 11.6%, minmax spread 40%). Thus, evoked emotions during encoding were associated with a parallel but largely
independent enhancement of remote memory for WP learning and
episodic/declarative memory for its associated picture context.

Discussion
Presentation of emotionally arousing pictures at encoding
slowed initial acquisition of probabilistic classification learning in
the WP tasks, a form of cognitive skill learning. By contrast, while
participants in the neutral encoding condition showed substantial
forgetting over a 1.5 month period, participants in the arousal
condition maintained WP performance, suggesting that emotional
arousal enhanced memory retention, decreasing the rate of memory decay. This decreased rate of memory decay was found even
after matching initial acquisition in the arousal and neutral conditions. Emotional arousal experienced during WP learning was also
associated with enhanced remote memory for the picture contexts
in which the WP task was acquired. These results provide evidence
that the modulatory influences of emotional arousal extend to
cognitive skill learning.
The current results are consistent with animal studies showing
amygdala modulation of different mnemonic tasks that putatively
originate from different neural systems (McGaugh, 2004; McGaugh
et al., 2002; Packard & Cahill, 2001; Packard et al., 1994). However,
more recent work suggests the distinction between a hippocampal/
medial temporal lobe-based declarative and a striatal-based procedural memory system is less clear. Evidence suggests that the
dorsomedial portion of the rat striatum, corresponding to the
caudate in primates, is involved in flexible place learning (Devan,
McDonald, & White, 1999; Devan & White, 1999; Yin & Knowlton, 2004; Yin, Knowlton, & Balleine, 2005; Yin, Ostlund, Knowlton, & Balleine, 2005). For example, lesions confined to the
dorsomedial portion of the striatum produce a preference for
cue-based responding in a water maze task (Devan et al., 1999).
Thus, it is unclear to what extent different forms of memory can be
anatomically separated strictly in terms of medial temporal lobe
and dorsal striatal systems. Because the cues and their associated
outcomes in the weather prediction task are probabilistically related, it is difficult to explicitly encode the relation between the
individual stimuli and their associated outcomes. Rather, the sub-

AROUSAL AND COGNITIVE SKILL LEARNING

ject must learn a series of stimulus-response association across

many trials. As such, the task emphasizes nondeclarative memory
processes. However, patients with mild Parkinsons disease who
can perform the task normally relative to controls, show medial
temporal lobe cortical activation unlike controls (Moody,
Bookheimer, Vanek, & Knowlton, 2004), suggesting that both
striatal and declarative-based memory systems can contribute to
learning the WP task. Manipulations designed to disrupt implicit
learning processes have also been shown to have no effect on WP
learning (Price, 2009). In neurologically intact controls, the two
brain areas may in fact compete with one another during task
acquisition. There is also evidence of a change in the underlying
memory systems used with progressive WP training. Patient studies show that early on during training learning depends on an intact
striatum, while later on, learning depends on an intact hippocampus (Knowlton et al., 1994). Functional imaging studies support
this switch in memory systems, showing very early activation in
the medial temporal lobe quickly replaced by engagement of the
striatum (Poldrack et al., 2001) followed by later activation of the
hippocampus (Poldrack et al., 1999; Iaria, Petrides, Dagher, Pike,
& Bohbot, 2003). In the current study, the number of trials used
may have recruited both memory systems across the course of
training. Thus, for these reasons it is possible that the enhanced
long-term retention observed in the arousal condition in the current
study reflects arousal enhancement of both nondeclarative and
declarative memory mechanisms. However, there are a few
sources of evidence to suggest the arousal enhancement of WP
retention reflects, at least in part, a reliance on a nondeclarative
procedural learning mechanism.
The precise timing of a switch between declarative and procedural systems is unclear in the present study. Recent data show that
attentional distraction from a secondary task impairs overall probabilistic classification performance and declarative knowledge of
cue-outcome associations (Foerde, Poldrack, & Knowlton, 2007)
and further blocks the shift from procedural/striatal to declarative/
medial temporal lobe memory systems (Foerde, Knowlton, &
Poldrack, 2006). This is consistent with data showing that stress
during learning facilitates use of procedural relative to declarative
learning strategies in both humans (Schwabe et al., 2007) and
animals (Packard & Wingard, 2004; Wingard & Packard, 2008). In
the present study, the intermittent presentations of picture contexts
and ratings between every few trials of WP training may have
served a similar role. Indeed, verbal statements in the transfer task
at the end of Session 1 regarding the outcomes of even the most
diagnostic cues (95%), where declarative memory should be
most evident, revealed substantial underestimation in both the
neutral and arousal conditions. Further, we assessed the relationship between WP retention and memory for surrounding picture
contexts. Individual differences in emotion enhanced memory for
picture contexts were not associated with greater WP retention.
This suggests retention of probabilistic classification learning was
independent of retrieving information from the original study
context, similar to implicit learning in medial temporal lobe amnesiacs (Knowlton et al., 1996; Reber et al., 1996).
Arousal during initial encoding clearly had a disruptive effect on
WP acquisition, consistent with our previous study (Steidl et al.,
2006). Similarly, Thomas and LaBar (2008) have shown that
arousal during encoding specifically leads to suboptimal strategy
use, particularly in those participants that found the emotional

17

stimuli most anxiety provoking. Studies of explicit memory sometimes show an initial disrupting effect of emotional arousal on
memory for neutral events at immediate test delays (Hurlemann et
al., 2007; Kleinsmith & Kaplan, 1963; Strange, Hurlemann, &
Dolan, 2003), but enhancement at longer delays (Anderson et al.,
2006; Kleinsmith & Kaplan, 1963; Maratos et al., 2001). As the
WP task involves simultaneous acquisition and retrieval, this may
partly contribute to the observed initial deficit in the arousal
condition. Our data suggest that the effects of emotional arousal on
WP learning may be biphasic, characterized by an initial disruption
in acquisition that is contrasted with a later retention enhancement.
Attentional distraction during WP acquisition may have been
greater in the arousal condition (e.g., Anderson, 2005; Most, Chun,
Widders, & Zald, 2005; Schimmack & Derryberry, 2005), as well as
differential engagement of declarative and nondeclarative learning
mechanisms between neutral and arousal groups during encoding
(Foerde et al., 2006, 2007), accounting for significantly poorer
initial performance. Because declarative memory may be more
susceptible to forgetting than skill learning (Steidl et al., 2006),
this could result in differential patterns of forgetting as shown
in the present results. To address this, we performance matched
the arousal and neutral groups at the end of acquisition. Performance was also matched on highly diagnostic cue types where
declarative knowledge would be greatest, as well as verbally stated
knowledge regarding cue-outcome contingencies. As such, the
relative contributions of declarative and procedural learning mechanisms should have been similar across the two groups. Despite
equivalent WP performance at the end of training, these matched
groups demonstrated markedly distinct mnemonic fatesnear
complete retention for the arousal group (Figure 1d), but no
evidence of retention in the neutral condition after the 1.5 month
delay.
Similarly, arousal levels experienced during delayed testing may
have facilitated differential engagement of procedural and declarative strategies between neutral and arousing groups (Schwabe et
al., 2007). Because retention testing took place in the same environment in which subjects were exposed to arousing picture stimuli during acquisition, it is possible that reexposure to this environment during retention testing may have differentially increased
arousal levels in the arousal group. Studies of pure contextual fear
conditioning in humans are very rare. One study has shown that
humans acquire contextual fear conditioning (assessed by both
GSR and subjective anxiety ratings) to a distinct virtual reality
environmental context paired with unpredictable footshock within
an experimental session (Alvarez, Biggs, Chen, Pine, and Grillon,
2008). However, whether contextual fear conditioning is evident
upon delayed exposure to the shock-paired context was not assessed. In the absence of physiological measures of arousal (i.e.,
galvanic skin response) in the current studies, it is difficult to
determine the extent to which such conditioned arousal induced by
reexposure to the training environment may have differentially
contributed to WP performance in the arousal group. Undoubtedly,
future studies would benefit from including measures of physiological arousal during both retention and acquisition.
Whether the neuroanatomical basis of the memory observed in the
current study is of pure striatal or mixed striatal/medial temporal
origin, the present results do appear to reflect a form of memory
distinct from previous demonstrations of EEM (Cahill et al., 1996;
Cahill, Prins, Weber, & McGaugh, 1994; Canli et al., 2000; Dolcos,

STEIDL, RAZIK, AND ANDERSON

18

LaBar, & Cabeza, 2004). Whereas studies of EEM largely focus on

shorter retention intervals and recollection of the episodic context in
which emotions are experienced (Cahill et al., 1994, 1996; Dolcos,
LaBar, & Cabeza, 2004; Kensinger & Corkin, 2004) the present study
demonstrates that emotional arousal enhances remote retention of a
cognitive skill, putatively a nonepisodic form of memory. Emotions
thus not only modulate the subjective experience of remembering but
potentially the neural mechanisms that support a form of memory that
is free from the episodic context in which it was acquired (Bechara et
al., 1995; Tulving, 1987).
In accordance with rat models of EEM (McGaugh, 2004), we
hypothesize that the amygdala plays a central role in the orchestration
of arousal enhancement of multiple forms of memory, as shown here
in the EEM for cognitive skill learning and its episodic picture
context. In rats the dorsal striatum and the hippocampus both receive
anatomical projections from the basolateral amygdala (Finch et al.,
1986; Kelley, Domensick, & Nauta, 1982; Pikkarainen, Rnkk,
Savander, Insausti, & Pitkanen, 1999; Price, 2003; Russchen, Bakst,
Amaral, & Price, 1985; Russchen & Price, 1984) via the stria terminalis and numerous studies converge on the appreciation that the
amygdala plays an important role in the emotional modulation of
memory retention (e.g., McGaugh, 2004). In humans, structural equation modeling of neuroimaging data has demonstrated the neural
bases of EEM for hippocampal-declarative memory (Kilpatrick &
Cahill, 2003), supported by anatomical connectivity between the
amygdala and surrounding anterior temporal lobe (Powell et al.,
2004). By contrast, knowledge of amygdala-striatal functional and
anatomical connectivity in humans is limited. The present findings
suggest modulatory influences on long-term memory for a probabilistic classification task, a putatively striatal based form of cognitive
skill learning. Future work will need to establish whether the present
demonstration of enhanced remote retention of cognitive skill learning does indeed reflect amygdala modulatory influences on striatal
memory systems.

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Received September 14, 2009

Revision received March 12, 2010
Accepted May 5, 2010