Acta Neurol Scand 2007: 116: 355–360 DOI: 10.1111/j.1600-0404.2007.00897.
x Copyright  2007 The Authors
Emotional arousal enhances declarative
memory in patients with AlzheimerÕs disease
Satler C, Garrido LM, Sarmiento EP, Leme S, Conde C, Tomaz C.
Emotional arousal enhances declarative memory in patients with
AlzheimerÕs disease.
Acta Neurol Scand 2007: 116: 355–360.
 2007 The Authors Journal compilation  2007 Blackwell Munksgaard.
Objective – To verify whether the long-term retention of an
emotionally arousing story is stronger than the retention of a neutral
story, and the enhancing effects of emotional arousal on declarative
memory in AlzheimerÕs disease (AD) patients. Method – Twenty
subjects (10 with AD and 10 controls matched for age and educational
level) were studied. After the audiovisual presentation (neutral story),
the subjects rated the narrativeÕs emotionality. Later, they answered a
multiple-choice questionnaire about the stories. Two weeks later, they
watched the emotionally arousing story. Results – Subjects who
watched the emotionally arousing story assigned a score of
emotionality higher than the subjects in the neutral group (P = 0.023).
In addition, the participants remembered more details of the arousing
story, and had a higher score in the questionnaire
(P < 0.001). Conclusions – We demonstrated that an emotionally
arousing content enhances long-term declarative memory in AD.
Furthermore, present finding supports the use of this instrument for
clinical and research purposes.
Introduction
It is well known that memories of happy and sad
moments seem more resistant to the decay of time
than other less striking events. Experimental
studies have demonstrated that emotional arousal
enhances declarative memory in healthy individ-
uals (1–5), amnesic patients (3, 6), and patients
with AD (7–11). These findings suggest that
emotional arousal produced by certain situations
strengthens the consolidation of new information
(12).
Studies on emotion have shown that particular
characteristics of pictures may elicit an emotional
response that varies according to the valence
(positive to negative) and to the arousing property
of the stimuli (from neutral to exciting) (13).
According to this, Ikeda et al. (11) affirm that
fear reinforces memory retention in AD.
Emotional memory has the same characteristics
of declarative memory. It is an episodic memory of
emotional events. Under special circumstances,
Journal compilation  2007 Blackwell Munksgaard
ACTA NEUROLOGICA
SCANDINAVICA
C. Satler1, L. M. Garrido2, E. P.
Sarmiento2, S. Leme3, C. Conde4,
C. Tomaz1
1
Laboratory of Neurosciences and Behavior, IB, and
Faculty of Health Sciences, University of Braslia, Asa
Norte, CEP 70910-900, Braslia, DF, Brazil;
2
Department of Psychology, Universidad Pontificia
Bolivariana, Bucaramanga, Santander, Colombia;
3
Institute of Psychology, University of Braslia, Braslia,
DF, Brazil; 4Faculty of Health Sciences, Universidad
Industrial de Santander, Bucaramanga, Santander,
Colombia
Key words: Alzheimer; emotion; memory; stories
Carlos Tomaz, Laboratory of Neurosciences and
Behavior, IB, and Faculty of Health Sciences, University
of Braslia, Asa Norte, CEP 70910-900, Braslia, DF,
Brazil
Tel.: +55 61 33072175
Fax: +55 61 32741251
e-mail: ctomaz@unb.br
Accepted for publication June 1, 2007
these memories are also referred to as ÔflashbulbÕ
memories (14).
Studies with animal models involving declarative
emotional memory suggest that the amygdaloid
complex (AC) plays a critical role in modulating the
formation of long-term memory associated with
emotionally arousing events (15,16). Findings from
extensive research involving both human and animal
subjects substantiate the notion that modulation of
memory storage for emotionally arousing events
occurs, at least in part, by interaction of endogenous
stress memory systems (especially catecholamines)
and the AC (in particular the basolateral amygdala)
(17). The degree of arousal produced by uncondi-
tional stimulus and not the aversive nature per se,
determines the level of amygdala involvement in a
learning situation. In this way, the amygdala should
be important for long-term memory formation
whenever the learning conditions are sufficiently
emotionally arousing to engage the amygdala,
independent of whether the particular emotions
involved are positive or negative (18).
355
Satler et al.
Different instruments and stimuli have been used
in emotional memory studies, such as memories of
real-life episodes, word lists, facial expressions,
neutral and emotional pictures, short movies with
arousing content, and narrated or visual stories.
In AD, the hallmark feature is the dramatic
memory deficit that occurs early in the disease
process. This deficit is presumed to result from
neuropathological changes in the medial temporal
lobe, regions that are critical for declarative
memory (19). From this result, we know whether
patients show a normal enhancement of emotional
memory. Several results have been found with AD
samples. So far, very few investigations have
demonstrated a marked impairment in memory
enhancement effect for negative pictures. Abrisqu-
eta-Gomez et al. (20) studied recognition of pos-
itive, negative and neutral pictures (pleasant,
unpleasant or indifferent). They confirmed that
emotional content enhanced recognition of pic-
tures in normal subjects, who benefited from the
affective content, while in patients with AD, the
emotional significance attached to the pictures did
not facilitate their recognition. Similar results with
AD patients have been reported in studies with
positives pictures, negative and positive words, and
negative sentences (21). In contrast, other research-
ers have demonstrated a relatively intact enhance-
ment effect for positive pictures (22), negative
stories or film clips (8, 23, 24), and real-life events
(10, 11) in investigations with AD patients.
Ikeda et al. (11) examined patients with AD who
experienced an earthquake in Kobe, Japan,
2 months after the disaster. They verified that
memories related to the earthquake were relatively
well retained in comparison with an event that had
less emotional involvement, suggesting that extra-
ordinary emotional involvement in the experience
enhanced learning and long-term memory.
In a study with word lists (7), all subjects were
given three trials of a three word list. The words
were positive, negative, or neutral in valence and
matched for concreteness, emotionality and pleas-
antness. The results showed that the controlÕs
performance was better than the AD patients.
However, the control group recalled all emotional
words regardless of their valence, while AD
patients recalled significantly more negative
words than positive or neutral. This suggests that
emotional valence is an important variable in
studies with emotional memory involving Alzhei-
merÕs disease.
Thus, the enhancement effect in AD patients
depends on a series of within-group factors: sex,
age, disease severity; and between-group factors:
valence (positive or negative), arousal (calming or
356
exciting), encoding instructions (easy or difficult),
viewing time, semantic coherency, arousal level,
and the complexity of the target events (visual
or ⁄ and auditory).
On the basis of bibliography, it is possible to see
that prior studies that found blunted emotional
memory enhancement in AD used sets of briefly
presented stimuli that lacked semantic coherence.
In contrast, the majority of studies that found an
enhancement effect in AD used stimuli with
semantic coherence that were processed for
longer periods of time. Significant differences had
been found when stimuli with a major complexity
and higher arousal level (a real-life event or a
narrated slide show) were employed. Therefore,
these characteristics could affect whether or not
AD patients demonstrate an enhancement effect.
The recall of narratives has been employed in a
number of memory assessments (1, 2, 6, 25–27) and
is considered a useful measure to assess recall and
recognition (27). Consequently, the aim of this
study was to determine whether long-term retent-
ion of an emotionally arousing story is stronger
than retention of a neutral story and is bigger than
the enhancing effects of emotional arousal on
declarative memory in patients with AD than the
control.
This study follows the line of research that
examines the retention of information of an
emotional experience of relatively no traumatic
intensity, and involves visual and verbal modality.
We administered the same methodological criteria
used by Kazui et al. (8).
Materials and methods
Subjects
All patients and controls were voluntary research
subjects from the University Hospital of Brasilia
(HuB), Brasilia, and gave informed consent prior
to participation, according to the ethical guidelines
for research with humans (196 ⁄ 96 CNS ⁄ MS reso-
lution).
Ten patients (five women and five men) with
probable AD were evaluated. Ten healthy subjects
(seven women and three men) matched for age,
gender and educational level were used as the
control group. The patients with AD had a history
of cognitive decline and memory problems, but
showed normal consciousness.
All participants were examined by neurologists
and psychologist and were given standard
neuropsychological examinations. The inclusion
criteria were those of the National Institute of
Neurological and Communicative Disorders and
 Effects of emotional arousal in AD patients

Stroke ⁄ AlzheimerÕs Disease, and Related Disor-
ders Association for probable AD (28), the Clinical
dementia rating (29) and the Mini-Mental State
Examination adapted to Portuguese (30). Patients
with other specific causes of dementia, brain
lesions, delirium, and depression were excluded.
Material
We employed slide presentations of two short
stories accompanied by a narrative. These stories
had been previously adapted to a Brazilian sample
(2) and kept as close as possible to the original ones.
The stories tell about a mother and son going to
visit the fatherÕs workplace. The slides are the
same, but there is a difference in the story content.
In the neutral version, on their way to visit the
father, they pass by a car accident that calls the
childÕs attention. In the hospital, where the father
works, the child participates in an emergency drill.
In the arousal version, the child suffers a bad car
accident on his way to visit his father and is
critically hurt. He is operated on at the emergency
room. The storyÕs content can be divided into three
phases, with the second phase (slide 5–8) being the
emotionally strongest phase of the story.
The subjects were asked to answer an 11-item
questionnaire about the stories. We did not use
KazuiÕs standard administration methods (8) due to
the patientsÕ memory impairment. Instead, we
selected items for the Portuguese version (2) from a
simplified recall test. One of the main differences
compared to the questionnaire used by Kazui et al.
(8) was that we asked two or three questions for each
slide obtaining the same number of answers (eight)
for each phase. Furthermore, we gave 1 point for a
correct answer and 0 point for an incorrect one.
Procedure
Images were presented to the participants on a
17 in. high-resolution color monitor at a rate of
20 s per slide. The subjects were told to pay
attention to the pictures and the narrative, and to
remember the story. Immediately after the presen-
tation, they were asked to rate the emotional
content of the whole story on a scale of 1 to 4, with
1 indicating Ônot emotionalÕ and 4 indicating
Ôhighly emotionalÕ. Five minutes later, the subjects
were given an 11-item recall test (reduced version).
The photographs were presented one by one again
in the same order; subjects were asked about the
story line. The second part of the experiment was
carried out after an interval of 2 weeks. On this
occasion, the experiment was repeated with the
same sets of images, but with an emotion filled
narrative story instead of the neutral story narra-
tive. We did not separate the groups into two
subgroups due to the fact that all participants
watched the neutral story in the first session and
the arousal story in the second, to prevent influ-
encing the participantsÕ recall. In this way, there
was no emotional influence that could possibly
interfere with their performance.
Data analysis
Results obtained did not fit the requirements for
the parametric statistical analysis. Therefore, the
receiver operating curve (ROC) was used to
evaluate the sensitivity and specificity for a
binary classifier system. Also, the fraction of true
positives (TP) vs the fraction of true negatives (TN)
was verified in the two versions: AD diagnosis or
no Alzheimer (controls) according to previously
established inclusion criterion. ROC test was
applied to analyze each version and each variable
to determine the best exclusion criterion for the
scores applied for each variable (Table 1). Bonfer-
roniÕs test was used to make the comparisons
between and within groups, respectively.
Results
As regards the total number of correct answers for
the questionnaire, an ANOVA of two factors,

Table 1 Results of the ROC analysis for each testÕs variables: sensitivity, specificity, positive predict value (PPV), negative predict value (NPV)

Version Variable ROC value Sensibility Specificity PPV NPV Well classified Inclusion criterion

Arousing C.A. Totals 0.96 0.90 0.90 0.90 0.90 90.00 22.00
C.A. P1 0.86 0.70 0.90 0.88 0.75 80.00 8.00
C.A. P2 0.94 1.00 0.80 0.82 1.00 85.00 7.00
C.A. P3 0.80 1.00 0.50 0.67 1.00 75.00 7.00
A.V 0.48 0.50 0.60 0.56 0.55 55.00 4.00
Neutra C.A. Totals 0.94 0.90 0.80 0.82 0.89 85.00 21.00
C.A. P1 0.87 1.00 0.60 0.71 1.00 80.00 7.00
C.A. P2 0.97 0.80 1.00 1.00 0.83 90.00 8.00
C.A. P3 0.82 0.90 0.60 0.86 0.69 75.00 6.00
N.V 0.76 0.70 0.80 0.78 0.73 75.00 3.00

357
Satler et al.
Version of the stories (Arousal and Neutral) and
Group of participants (Controls and AlzheimerÕs
subjects), showed a significant difference depending
on the version of the stories attributed to the group
of participants (F(1,36) = 36.397, P < 0.001).
Subsequently, BonferroniÕs post hoc test for mul-
tiple comparisons indicated that the participants
with AD displayed lower values of correct answers
in the three phases of the test than the controls
(Fig. 1).
Taking these results together with the data from
the ROCÕs findings, it is possible to affirm that the
control subjects obtained 22 points or more in the
classification of correct answers while the AD
scored less than 22 points.
According to the sensitivity (0.5) and specificity
(0.6) levels, the arousing version did not distinguish
the two groups. On the other hand, exposure to the
neutral version yielded significant ranges of sensi-
tivity (0.7) and specificity (0.8), indicating that this
variable was strongly discriminatory.
Analysis of the scores assigned for emotional
value in the factor group (participants) and the
version of the test, yielded significant differences
attributable to the ÔVersionÕ factor (F(1,36) = 5.64,
P = 0.023), and significant interactions between
factors (F(1,36) = 4.24, P = 0.047).
Within the Alzheimer group, there were no
significant differences attributable to the version,
but when considering the neutral version, the
Alzheimer patients attributed a higher emotional
25
*
20
15
Scores
10
5
0 0
CON-N CON-A ALZ-N ALZ-A
Figure 1. Scores (mean  SEM) regarding the total amount of
correct answers for the questionnaire scores by Control Group
in the two version: neutral (CON-N) and emotional (CON-E),
and the AlzheimerÕs participants in the neutral (ALZ-N) and
emotional version (ALZ-E). *The AlzheimerÕs group showed
less number of correct answers than the control group
(P < 0.05).
358
rating than the controls, differing from the emo-
tional version, which showed no significant differ-
ences for the groups (Fig. 2).
BonferroniÕs analysis (P < 0.05) indicated that
as a whole, the arousing version had a stronger
effect on the scores than on the scores given to the
neutral version. BonferroniÕs analysis (P < 0.05)
indicated that as a whole the arousing version had
an expressive impact on the results.
In general, the total correct answers for phases 1
and 2 showed reasonable discriminative power,
unlike the correct answers for phase 3, that displayed
satisfactory sensitivity, but low specificity.
The differences between the two versions of the
test (arousal and neutral) are centered in the
contents of phase 2, leading to the conclusion of
a significant difference attributable to diagnoses
(F(1,36) = 40.375, P < 0.001), but no significant
differences attributable to the version of the test
(Fig. 3).
BonferroniÕs analysis showed that the partici-
pants with AD displayed lower numbers of correct
answers than the controls. This suggests that the
emotional alert produced no increment to the
mnemonic performance in this group, but both
versions of the test were sensitive to the Alzheimer
diagnosis.
A general analysis of testsÕ results displays that
the variable total number of correct answers is the
best discriminator of the positive or negative
diagnose of Alzheimer type Dementia. This is
4 A>N
3
Rating of emotionality
*
1
CON-N CON-A ALZ-N ALZ-A
Figure 2. Ratings (mean  SEM) of emotionality for neutral
(N) and emotionality (E) arousing narratives by the two
groups: Control group (CON) and Alzheimer group (ALZ).
*Scores for the neutral version assigned by the control group
were smaller that the AlzheimerÕs group (P < 0.05). The scores
assigned to the arousing version were higher than those
assigned to the neutral.

9 stories. A comparative analysis of the stories recall
8 Neutral
Emotional
7
6 *
Recall score
5 aspect of emotional memory (6). Therefore, pre-
4 explain the present results. Several authors (10, 22)
3 behavior and cognition. Thus, we agree with Kazui
2
1
0 showed that the arousing story was better recalled
Control Alzheimer
Groups
Figure 3. Recall scores (mean  SEM) for the questionnaire
related to phase 2 of the stories. *Correct answers for
the control group were higher than the Alzheimer group
(P < 0.001).
demonstrated in phase 2 of the questionnaire in the
Neutral Version (ROC = 0.97), where the expec-
ted best exclusion value is 8 correct answers,
followed by total correct answers in the Arousing
Version (ROC = 0.96), with the best exclusion
criterion of 22.
It is important to emphasize that as the control
group was composed of healthy participants, the
exclusion criterion was used as a normalization
criterion for these experimental conditions. Con-
frontation of these results with ROC confirms that
the variable total correct answers for the arousing
version showed the best exclusion criterion in 22
correct answers.
Discussion
The findings indicate that a narrative with high
emotional content can enhance conscious recall of
information in humans, i.e. declarative memory.
The rating for the emotional content of the
arousing story was significantly higher than the
neutral story, in both the AlzheimerÕs patients and
control subjects. These results confirm that the tool
used in this study is useful for the assessment of
emotional memory in AD.
Unlike the control group, the perception of
higher emotionality had no repercussion on the
mnemonic performance in the AlzheimerÕs
patients. The AD group had lower recall scores
than the normal subjects for both versions of the
Effects of emotional arousal in AD patients
within the AD group showed a higher performance
and recall in the arousing version.
The influence of emotion on memory is not a
purely cognitive or affective phenomenon, but a
property of an aroused physiological activation.
There are biological mechanisms involved in this
sumed damage to AD patientsÕ amygdala may
have described amygdalaÕs role in emotional
et al. (8) that the impairment of the enhancing effects
of emotional arousal on memory reflects the degree
of damage to the amygdala.
A phase-by-phase comparison of the results
than the neutral story only in phase 2, in which the
emotional impact of the arousing story was higher
than that in the neutral one, just for the AD group.
The performance of the control group was lower in
the arousal than in the neutral story. These results
strongly indicate that the enhancing effect of
emotional arousal on declarative memory is pre-
served in patients with AD, also demonstrating
that this emotional variable is more discriminative
in AD.
Analyzing phase 2 in its entirety, it is important
to point out that the AD group was able to
recognize and label emotions associated with the
narrative at a rate not significantly different from
that of the matched controls, although AD patients
judged the emotional version less emotive than the
control subjects. Also, patients were able to iden-
tify the pictures and interpret their meaning as well
as the controls. These arguments are in agreement
with those from previous investigations (23), sup-
porting the idea of preserved emotional processing
in early AD.
When the neutral version was considered, the
AD group attributed a higher emotional score than
the control group. This perception of higher
emotionality did not have any repercussion on
the mnemonic performance in these patients.
However, in the control group, a significant
increment of the mnemonic performance was
verified. This suggests that the emotional alert
produced no significant increase in the mnemonic
performance in the groups, but both versions of the
test were sensitive to the Alzheimer diagnosis. In
this way, the AD group recalled more details of the
arousing story. Although Alzheimer patients had
deficit in story recall, they displayed a better
memory for emotionally negative events when
compared with healthy controls (the emotional
arousal used in the present study was negative in
359
Satler et al.
nature). This conclusion has some important
implications for the management of dementia
rehabilitation and treatment.
In conclusion, our data are in disagreement with
those of Abrisqueta-Gomez et al. (20). The reason
for this discrepancy could be because of the tool
used to assess the benefit from the emotional
content. Abrisqueta-Gomez et al. (20) investigated
AD memory with emotionally charged pictures
that did not have any relation to the subjectsÕ
personal experiences in contrast with our work
tool. However, we agree with these authorsÕ
conclusion that AD patients do not benefit from
the emotional content of stimuli even at mild to
moderate stages of the disease.
The recall results in the present study suggest
that this instrument is a valid tool to examine
emotional memory in subjects with probable AD.
It is also useful in comparing healthy subjects with
dementia patients. A goal for future studies is to
compare the variable recall performance in relation
to the memory decline along the various stages of
the disease process.
Acknowledgements
C. Satler is the recipient of a MSc fellowship from CAPES, and
C. Tomaz of a Researcher fellowship from CNPq, Brazil.
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