Copyright  2007 The Authors

Journal compilation  2007 Blackwell Munksgaard

Acta Neurol Scand 2007: 116: 355360 DOI: 10.1111/j.1600-0404.2007.00897.x

ACTA NEUROLOGICA
SCANDINAVICA

Emotional arousal enhances declarative

memory in patients with Alzheimers disease
Satler C, Garrido LM, Sarmiento EP, Leme S, Conde C, Tomaz C.
Emotional arousal enhances declarative memory in patients with
Alzheimers disease.
Acta Neurol Scand 2007: 116: 355360.
 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 eects of emotional arousal on declarative
memory in Alzheimers 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 narratives 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 nding 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 individuals (15), amnesic patients (3, 6), and patients
with AD (711). These ndings 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) afrm 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,

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 ashbulb

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 unconditional 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 suciently
emotionally arousing to engage the amygdala,
independent of whether the particular emotions
involved are positive or negative (18).
355

Satler et al.
Dierent 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 decit that occurs early in the disease
process. This decit 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. Abrisqueta-Gomez et al. (20) studied recognition of positive, negative and neutral pictures (pleasant,
unpleasant or indifferent). They conrmed that
emotional content enhanced recognition of pictures in normal subjects, who beneted from the
affective content, while in patients with AD, the
emotional signicance 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 researchers have demonstrated a relatively intact enhancement effect for positive pictures (22), negative
stories or lm 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 veried that
memories related to the earthquake were relatively
well retained in comparison with an event that had
less emotional involvement, suggesting that extraordinary 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 pleasantness. The results showed that the controls
performance was better than the AD patients.
However, the control group recalled all emotional
words regardless of their valence, while AD
patients recalled signicantly more negative
words than positive or neutral. This suggests that
emotional valence is an important variable in
studies with emotional memory involving Alzheimers disease.
Thus, the enhancement eect 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 dicult),

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 briey
presented stimuli that lacked semantic coherence.
In contrast, the majority of studies that found an
enhancement eect in AD used stimuli with
semantic coherence that were processed for
longer periods of time. Signicant dierences 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 aect whether or not
AD patients demonstrate an enhancement eect.
The recall of narratives has been employed in a
number of memory assessments (1, 2, 6, 2527) and
is considered a useful measure to assess recall and
recognition (27). Consequently, the aim of this
study was to determine whether long-term retention 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 resolution).
Ten patients (ve women and ve 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

Eects of emotional arousal in AD patients

Stroke Alzheimers Disease, and Related Disorders Association for probable AD (28), the Clinical
dementia rating (29) and the Mini-Mental State
Examination adapted to Portuguese (30). Patients
with other specic causes of dementia, brain
lesions, delirium, and depression were excluded.

attention to the pictures and the narrative, and to

remember the story. Immediately after the presentation, they were asked to rate the emotional
content of the whole story on a scale of 1 to 4, with
1 indicating not emotional and 4 indicating
highly emotional. 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 lled
narrative story instead of the neutral story narrative. We did not separate the groups into two
subgroups due to the fact that all participants
watched the neutral story in the rst session and
the arousal story in the second, to prevent inuencing the participants recall. In this way, there
was no emotional inuence that could possibly
interfere with their performance.

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 fathers workplace. The slides are the
same, but there is a dierence in the story content.
In the neutral version, on their way to visit the
father, they pass by a car accident that calls the
childs attention. In the hospital, where the father
works, the child participates in an emergency drill.
In the arousal version, the child suers a bad car
accident on his way to visit his father and is
critically hurt. He is operated on at the emergency
room. The storys content can be divided into three
phases, with the second phase (slide 58) 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
Kazuis standard administration methods (8) due to
the patients memory impairment. Instead, we
selected items for the Portuguese version (2) from a
simplied 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.

Data analysis

Results obtained did not t the requirements for

the parametric statistical analysis. Therefore, the
receiver operating curve (ROC) was used to
evaluate the sensitivity and specicity for a
binary classier system. Also, the fraction of true
positives (TP) vs the fraction of true negatives (TN)
was veried 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). Bonferronis test was used to make the comparisons
between and within groups, respectively.

Procedure
Results

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

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 tests 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
C.A. P1
C.A. P2
C.A. P3
A.V
C.A. Totals
C.A. P1
C.A. P2
C.A. P3
N.V

0.96
0.86
0.94
0.80
0.48
0.94
0.87
0.97
0.82
0.76

0.90
0.70
1.00
1.00
0.50
0.90
1.00
0.80
0.90
0.70

0.90
0.90
0.80
0.50
0.60
0.80
0.60
1.00
0.60
0.80

0.90
0.88
0.82
0.67
0.56
0.82
0.71
1.00
0.86
0.78

0.90
0.75
1.00
1.00
0.55
0.89
1.00
0.83
0.69
0.73

90.00
80.00
85.00
75.00
55.00
85.00
80.00
90.00
75.00
75.00

22.00
8.00
7.00
7.00
4.00
21.00
7.00
8.00
6.00
3.00

Neutra

357

Satler et al.
Version of the stories (Arousal and Neutral) and
Group of participants (Controls and Alzheimers
subjects), showed a signicant dierence depending
on the version of the stories attributed to the group
of participants (F(1,36) = 36.397, P < 0.001).
Subsequently, Bonferronis post hoc test for multiple 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 ROCs ndings, it is possible to arm that the
control subjects obtained 22 points or more in the
classication of correct answers while the AD
scored less than 22 points.
According to the sensitivity (0.5) and specicity
(0.6) levels, the arousing version did not distinguish
the two groups. On the other hand, exposure to the
neutral version yielded signicant ranges of sensitivity (0.7) and specicity (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 signicant dierences
attributable to the Version factor (F(1,36) = 5.64,
P = 0.023), and signicant interactions between
factors (F(1,36) = 4.24, P = 0.047).
Within the Alzheimer group, there were no
signicant dierences attributable to the version,
but when considering the neutral version, the
Alzheimer patients attributed a higher emotional

rating than the controls, diering from the emotional version, which showed no signicant dierences for the groups (Fig. 2).
Bonferronis analysis (P < 0.05) indicated that
as a whole, the arousing version had a stronger
eect on the scores than on the scores given to the
neutral version. Bonferronis 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 specicity.
The dierences between the two versions of the
test (arousal and neutral) are centered in the
contents of phase 2, leading to the conclusion of
a signicant dierence attributable to diagnoses
(F(1,36) = 40.375, P < 0.001), but no signicant
dierences attributable to the version of the test
(Fig. 3).
Bonferronis analysis showed that the participants 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 tests 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

25

A>N

*
Rating of emotionality

Scores

20

15

10

*
2

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 Alzheimers participants in the neutral (ALZ-N) and
emotional version (ALZ-E). *The Alzheimers group showed
less number of correct answers than the control group
(P < 0.05).

358

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 Alzheimers group (P < 0.05). The scores
assigned to the arousing version were higher than those
assigned to the neutral.

Eects of emotional arousal in AD patients

9
Neutral

Emotional

Recall score

6
5
4
3
2
1
0
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 expected 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. Confrontation of these results with ROC conrms that
the variable total correct answers for the arousing
version showed the best exclusion criterion in 22
correct answers.
Discussion

The ndings 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 signicantly higher than the
neutral story, in both the Alzheimers patients and
control subjects. These results conrm 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 Alzheimers
patients. The AD group had lower recall scores
than the normal subjects for both versions of the

stories. A comparative analysis of the stories recall

within the AD group showed a higher performance
and recall in the arousing version.
The inuence of emotion on memory is not a
purely cognitive or aective phenomenon, but a
property of an aroused physiological activation.
There are biological mechanisms involved in this
aspect of emotional memory (6). Therefore, presumed damage to AD patients amygdala may
explain the present results. Several authors (10, 22)
have described amygdalas role in emotional
behavior and cognition. Thus, we agree with Kazui
et al. (8) that the impairment of the enhancing effects
of emotional arousal on memory reects the degree
of damage to the amygdala.
A phase-by-phase comparison of the results
showed that the arousing story was better recalled
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 eect of
emotional arousal on declarative memory is preserved 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 signicantly dierent from
that of the matched controls, although AD patients
judged the emotional version less emotive than the
control subjects. Also, patients were able to identify the pictures and interpret their meaning as well
as the controls. These arguments are in agreement
with those from previous investigations (23), supporting 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 signicant
increment of the mnemonic performance was
veried. This suggests that the emotional alert
produced no signicant 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
decit 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 benet from the emotional
content. Abrisqueta-Gomez et al. (20) investigated
AD memory with emotionally charged pictures
that did not have any relation to the subjects
personal experiences in contrast with our work
tool. However, we agree with these authors
conclusion that AD patients do not benet 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.

References
1. Botelho de Oliveira S, Martinez Garrido LM, Condes
Cotes CA, Prada Sarmiento EL, Tomaz C. Evaluacion de
la memoria declarativa asociada con contenido emocional en una muestra colombiana. Rev Latinoam Psicol
2004;36:22942.
2. Frank JE, Tomaz C. Enhancement of declarative memory
associated with emotional content in a Brazilian sample.
Braz J Med Biol Res 2000;33:14839.
3. Frank JE, Tomaz C. Lateralized impairment of the emotional
enhancement of verbal memory in patients with amygdalahippocampus lesion. Brain Cogn 2003;52:22330.
4. Frank JE, Tomaz C. Sistema l mbico e a modulacao emocional da memoria. Neurobiologia 2003;66:1320.
5. Taylor SF, Liberzon I, Fig LM, Decker LR, Minoshima S,
Koeppe R. The eect of emotional content on visual
recognition memory: a PET activation study. Neuroimage
1998;8:18897.
6. Cahill L, McGaugh JL. A novel demonstration of enhanced
memory associated with emotional arousal. Conscious
Cogn 1995;4:41021.
7. Fleming K, Kim SH, Doo M, Maguire G, Potkin SG. Memory for emotional stimuli in patients with Alzheimers
disease. Am J Alzheimers Dis Other Demen 2003;18:340
42.
8. Kazui H, Mori E, Hashimoto M et al. Impact of emotion on
memory. Br J Psychiatry 2000;177:3437.
9. Kazui H, Mori E, Hashimoto M, Hirono N. Enhancement of
declarative memory by emotional arousal and visual
memory function in Alzheimers disease. Neuropsychiatry
Clin Neurosci 2003;15:22126.

360

10. Mori E, Ikeda M, Hirono N et al. Amygdalar volume and

emotional memory in Alzheimers disease. Am J Psychiatry
1999;156:21622.
11. Ikeda M, Mori E, Hirono N, Imamura T, Ikejiri Y, Yamashita H.
Amnestic people with Alzheimers disease who remembered
the Kobe earthquake. Br J Psychiatry 1998;172:4258.
12. McGaugh JL. Signicance and remembrance: the role of
neuromodulatory systems. Psychol Sci 1990;1:1525.
13. Lang PT, Bradley MM, Cuthbert BN. Emotion, attention,
and the startle reex. Psychol Rev 1990;97:33795.
14. Brown R, Kulik J. Flashbulb memories. Cognition
1977;5:7399.
15. LeDoux JE. Emotion memory systems in the brain. Behav
Brain Res 1993;58:6979.
16. McGaugh JL. Aect, neuromodulatory systems and memory storage. Handbook of emotion and memory: research
and theory. In: Christianson SA, ed. NJ: Lawrence Erlbaum Associates, 1992;24568.
17. Cahill L. Neurobiological mechanisms of emotionally
inuenced, long-term memory. Prog Brain Res
2000;126:23846.
18. Cahill L, McGaugh JL. Amygdaloid complex lesions differentially aect retention of tasks using appetitive and
aversive reinforcement. Behav Neurosci 1990;104:53243.
19. Kesinger EA, Anderson A, Growdon JH, Corkin S. Eects of
Alzheimers disease on memory for verbal emotional
information. Neuropsychologia 2004;42:791800.
20. Abrisqueta-Gomez J, Bueno OFA, Oliveira MGM, Bertolucci
PHF. Recognition memory for emotional pictures in Alzheimers patients. Acta Neurol Scand 2002;105:514.
21. Kesinger EA, Brierley B, Medford N, Growdon JH, Corkin
S. Eects of normal aging and Alzheimers disease on
emotional memory. Emotion 2002;2:11834.
22. Hamann SB, Monarch ES, Goldstein FC. Memory
enhancement for emotional stimuli is impaired in early
Alzheimers disease. Neuropsychology 2000;14:8292.
23. Boller F, Massioui F, Devouche E, Traykov L, Pomati S,
Starkstein S. Processing emotional information in Alzheimers disease: eects on memory performance and neurophysiological correlates. Dement Geriatr Cogn Disord
2002;14:10412.
24. Maunoury C, Michot JL, Cailet H et al. Specify of temporal amygdala atrophy in Alzheimers disease: quantitative assessment with magnetic resonance imaging.
Dementia 1996;7:104.
25. Adolphs R, Cahill L, Schul R, Babinsky R. Impaired
declarative memory for emotional material following
bilateral amygdala damage in humans. Learn Mem
1997;4:291300.
26. Heuer F, Reisberg D. Vivid memories of emotional events:
the accuracy of remembered minutiae. Mem Cogn 1990;
18:496506.
27. Lezak MD. Neuropsychological assessment. New York:
Oxford University Press, 1995.
28. McKanhann G, Drachman D, Folstein M, Katzman R, Price D,
Stadlan EM. Clinical diagnosis of Alzheimers disease: Report of the NINCDS-ADRDA Work Group under the
auspices of Department of Health and Human Services Task
Force on Alzheimers disease. Neurology 1984;34:93944.
29. Hughes CP, Berg L, Danziger WL et al. A new clinical scale
for the staging of dementia. Br J Psychiatry 1982;140:
56672.
30. Bertolucci PHF, Brucki SMD, Campacci SR, Juliani Y. O
mini-exame do estado mental em uma populacao geral:
impacto da escolaridade. Arq Neuropsiquiatr 1994;52:
17.