AM J ALZHEIMERS DIS OTHER DEMEN OnlineFirst, published on January 26, 2009 as doi:10.1177/1533317508330561
Free Recall and Learning of Emotional
Word Lists in Very Elderly People With
and Without Dementia
American Journal of Alzheimer’s
Disease & Other Dementias1
Volume 000 Number 00
Month 2009 1-8
# 2009 Sage Publications
10.1177/1533317508330561
http://ajadd.sagepub.com
hosted at
http://online.sagepub.com
Ruth E. Nieuwenhuis-Mark, PhD, Kim Schalk, MSc, and
Natalie de Graaf, MSc
An emotional memory advantage has been found across
the life span where recall is better for emotional (as
opposed to neutral) stimuli. Our goal was to design
emotionally valent word lists for easy use by practitioners
and to test whether demented and healthy elderly participants showed an emotional memory advantage with
these lists. Three new word lists (a positive, a negative,
and a neutral list) were constructed. Thirty-eight
controls, 37 with mild cognitive impairment and 20
Alzheimer’s dementia participants’ free recall was tested. Unsurprisingly, controls had better recall overall.
Emotionally valent words were recalled better in
comparison to neutral words in all 3 groups. No recall
advantage for positive versus negative words emerged.
Learning differed among the groups with the Alzheimer’s dementia participants showing flatter learning
curves. The results tentatively suggest that emotional
memory may stay intact longer but that learning of such
lists becomes more difficult as dementia progresses.
M
Both the amygdala and the hippocampus are
involved in, among other functions, memory for
emotional stimuli/events.9
Emotional stimuli tend to be better remembered
(ie, memory for these stimuli is both more accurate
and more quickly processed) on the whole than
neutral stimuli—the so-called emotional memory
advantage (EMA). This effect has been observed for
pictures,10 words,11 autobiographical experiences,12
and sounds.13 Whether there is a valence effect
(negatively valenced stimuli better remembered than
positive or vice versa) remains controversial. It is very
likely that many cognitive and neural processes contribute to the EMA.9 Differences in encoding strategies are believed, by many researchers, to be one of
the possible mechanisms behind the EMA. Emotional information may be more elaborately encoded,
have a wider semantic network, be more easily linked
with autobiographical experiences, and/or may be
more distinctive than neutral items.9 The EMA could
feasibly also be due to retrieval processes where emotion or mood may serve as a retrieval cue, or it may be
due to modulation of consolidation processes. What
the precise mechanism behind the EMA is still not
known. Kensinger et al9 suggested that people who
suffer from amygdala lesions do not show EMAs.
any types of dementia are characterized
by memory impairment. However, as
Fleming et al1 rightly pointed out, memory
is not a unitary concept and different mnemonic
functions depend on different neuroanatomical
regions and/or networks. In relation to dementia, for
example, several studies have suggested that (some)
aspects of implicit memory stay intact long into the
dementia process2,3 while other studies have suggested that memory for emotional stimuli may be to
some extent spared1,4 but see ref 5. Alzheimer’s
dementia (AD) is the commonest form of dementia
and encoding of explicit declarative information is
the primary memory deficit in AD. Such encoding
depends on the integrity of the hippocampus and its
surrounding regions.6 As dementia progresses, the
hippocampus becomes more damaged and episodic
memory in turn becomes more of a problem for these
patients. The amygdala also degenerates in AD.7,8
From the Department of Medical Psychology and Neuropsychology, University of Tilburg, Tilburg, Netherlands.
Address correspondence to: Ruth Elaine Nieuwenhuis-Mark,
Department of Medical Psychology and Neuropsychology, University of Tilburg, Postbox 90153, 5000 LE Tilburg, Netherlands;
e-mail: [email protected].
Keywords:
word lists
dementia; recall; learning; emotional
1
2 American Journal of Alzheimer’s Disease & Other Dementias1 / Vol. 000, No. 00, Month 2009
Following this logic to its conclusion, we may expect
to see EMAs in people with mild AD and less atrophy
of the amygdala in comparison to people with severe
AD and greater atrophy of the amygdala. Kensinger
et al9 found that this was indeed the case when
memory for emotional stories was tested.
Healthy elderly people also show an enhanced
memory for emotional compared to neutral information.1,14,15 Although Kensinger and Corkin16 found
that young participants recalled more negative stimuli in comparison to positive or neutral, several
studies have reported that older adults show a disproportionate enhancement of memory in favor of positive compared to negative stimuli. This phenomenon
has been called the positivity effect.17,18 Kensinger19
went on to show that this positivity effect may only
be obtained when nonarousing words are used.
She found no valence differentiation when arousing
words were used (arousing words were simply
remembered better than neutral words and there was
no positivity effect). Kensinger suggested that aging
alters the processing of nonarousing information due
to the engagement of controlled strategies while
EMAs to arousing stimuli are more likely to be governed by more automatic processes (the latter are
believed to be less affected by aging). According to
Mather and Carstensen,20 the positivity effect could
be explained by the fact that older adults are more
likely to focus on positive information in everyday
life, and less on negative information, in a strategy
designed to enhance their sense of well-being. However, a number of studies have reported a memory
enhancement for negative emotional stimuli in
healthy elderly people as well.14,15
Relatively few studies have been carried out in
this research area in people with mild cognitive
impairment (MCI) or with varying degrees of dementia. Petersen and colleagues21-23 see MCI as an
entity in its own right. They have provided criteria
to assist clinicians when they suspect ‘‘MCI but not
yet dementia’’ in their patients. These authors have
also suggested that subgroups of MCI exist with the
amnesic form being the most likely to develop into
full-blown AD. Marreneca et al24 stated that people
with MCI, like healthy elderly people, were more
likely to remember positively valenced stimuli while
Fleming et al1 found that mild-AD patients were
more likely to remember negative information. There
are therefore some inconsistencies in the literature.
Findings appear to depend heavily on which tasks are
used, the patient populations tested, and crucially,
the stimuli and encoding instructions used.9 Emotional memory advantages tend to be more robust
at delayed rather than at immediate recall and for
recall rather than recognition tasks.25,26
The 8- and 15-word test(s) from the Amsterdam
Dementia Screening (ADS-6) battery27 are routinely
used in neuropsychological assessment in Dutch
hospitals and clinics to assess short-term episodic
memory in early dementia. They are internationally
known as the Rey Auditory Verbal Learning Test.28
Words are read out by the clinician one at a time
and at the end of the first reading the client is
invited to recall as many of the words as possible.
The words are then read out again in a different
order and the client is again asked to recall the
words. The list is read out a total of 5 times and
in this way the total number of words recalled
across the 5 trials, the total number of repetitions,
intrusions, and a learning curve can be obtained
for each client. The data therefore give not only
information on the total recall ability of a patient
but also an indication of how they learn. A delayed
recall and recognition score can also be obtained. In
this study, however, we concentrated on immediate
recall and learning.
The object of this study was to adapt the standard
8-word test to assess emotional memory in healthy
elderly people, a MCI and in an AD population. Our
goal was 2-fold. We wanted to develop lists that
could easily be used by practitioners in the clinic and
we wanted to determine whether our Dutch elderly
population also showed an EMA. Most studies that
have investigated memory for emotionally toned
word lists have used very long lists and/or blocks.
Elderly individuals find such tasks demanding and
floor effects, especially in the demented population,
are typical. Long lists are also not practical to use in
everyday neuropsychological assessment when typically a number of tests are used to derive the overall
cognitive functioning of a patient.
We expected to see better recall overall in the
healthy control group compared to the other 2
groups with the MCI group showing a better memory
overall than the AD group. We also expected to see
EMAs in all 3 groups with recall better for the emotional than for the neutral words. Furthermore, a
positive valence advantage for the controls and MCI
groups8,24 and a negative valence advantage for the
AD group was hypothesized.1 Finally, we had no
specific expectancies with regard to the number of
repetitions and intrusions the participants would
make per list, nor did we predict how they would
learn the lists. We know of no other study that has
looked at learning in dementia using emotional
word lists.
Emotional Word List Recall in Dementia / Nieuwenhuis-Mark et al 3
Table 1A. The 4 Word Lists Used: Dutch Words and Their (English) Translations
Word List
Standard
Gordijn (Curtain)
Vogel (Bird)
Potlood (Pencil)
Bril (Spectacles)
Winkel (Shop)
Spons (Sponge)
Rivier (River)
Kleur (Color)
Neutral
Positive
Negative
Lucht (Sky)
Leeuw (Lion)
Borst (Breast)
Gedicht (Poem)
Dokter (Doctor)
Fles (Bottle)
Circus (Circus)
Vloed (Flood)
Lente (Spring)
Engel (Angel)
Komedie (Comedy)
Muziek (Music)
Baby (Baby)
Paradijs (Paradise)
Cadeau (Present)
Strand (Beach)
Afval (Garbage)
Blaar (Blister)
Kerkhof (Graveyard)
Geweer (Gun/Rifle)
Wesp (Wasp)
Brand (Fire)
Snee (Cut/Incision)
Vergif (Poison)
Materials and methods
Participants
This study included 95 participants who were either
residents from 2 separate nursing homes in the Netherlands or recruited from the general population.
They were divided into 3 groups—38 controls, 37
MCI, and 20 AD. Mini-Mental State Examination
scores were obtained for all participants (MMSE29).
The controls had MMSE scores over 24 (mean ¼
27.4, SD ¼ 1.7), had never received the diagnosis
of dementia, lived in the community and had never
suffered from a neurological or psychiatric disorder.
They were also not taking psychiatric medications.
These are also the criteria recommended by Petersen
et al23 for choosing control participants in dementia
studies. Some researchers suggest a cutoff of 26 and
on average our controls scored above this more lenient criterion thus making them comparable to other
control groups found in the literature. The MCI
group had MMSE scores ranging from 20 to 24
(mean ¼ 21.5, SD ¼ 2.0), lived in the community
and had not (yet) received a diagnosis of dementia
but who were believed to be functioning at a lower
level (especially on memory) than the controls.
The AD group had all received diagnoses of AD as
defined by Diagnostic and Statistical Manual of
Mental Disorders, Fourth Edition (DSM-IV) criteria.
These diagnoses were made on average 1 month
before this study was carried out by a multidisciplinary team including a clinical neuropsychologist. The
MMSE scores of the AD group ranged from 10 to 21
(mean ¼ 16.2, SD ¼ 3.9).
The groups were matched on age (controls: mean
age ¼ 81.5, SD ¼ 6.4; MCI: mean age ¼ 83.4, SD ¼
5.3; AD: mean age ¼ 83.8, SD ¼ 5.0), and on number of years of education (mean for all groups ¼ 9
years). We could not however match the groups
according to gender: there were more women in the
MCI and AD groups (30 in the MCI and 17 in
the AD) than in the control group (24). None of the
participants were anxious or depressed (as assessed
by the Hospital Anxiety and Depression Scale,
HADS30,31). Informed consent was obtained from
all participants or their family members prior to
participation.
Materials
Three new word lists, each 8 words in length, were
developed using the Affective Norms for English
Words list (ANEW32) and then translated into
Dutch. The words were carefully chosen according
to their valence (pleasantness) level and were
matched on word length, word frequency, concreteness, arousal/emotionality, imagability, and
meaningfulness (as measured using the MRC
Psycholinguistic Database33). Positive, neutral, and
negative lists were therefore constructed. The 4
word lists and their descriptive statistics are shown
in Table 1A and B.
The standard 8-word test was less arousing
than the 3 newly constructed lists [F(3,27) ¼ 4.4,
P < .025]. The neutral, positive, and negative word
lists were matched on all variables (including arousal) and only differed on valence [F(2,22) ¼ 77.9,
P < .001].
Procedure
Participants were presented with the 3 new lists plus
the standard 8-word test in 1 session with a 5-minute
pause between each of the 4 lists. The instructions followed those provided with the standard 8-word test
from the ADS-6 (see Introduction for a detailed explanation of this test),27 with each word list presented for
5 trials each, so that a testing session consisted of a
total of 20 trials and 160 words. Participants were
asked to recall as many words as they could at the end
4 American Journal of Alzheimer’s Disease & Other Dementias1 / Vol. 000, No. 00, Month 2009
Table 1B. Stimulus Characteristics for the 4 Word Lists (Means and Standard Deviations)
Word List
Standard
Length
Frequency
Valence
Arousal
Concreteness
Meaningfulness
Imagability
Table 2.
Neutral
5.8 (1.0)
64.1 (63.9)
6.2 (1.1)
3.8 (0.7)
569 (55)
729 (73)
584 (44)
5.3
71.9
5.6
5.5
550
655
570
(0.9)
(83.7)
(1.1)
(1.1)
(61)
(60)
(65)
Positive
Negative
5.9 (1.2)
114.0 (125.6)
7.9 (0.6)
5.3 (0.3)
465 (108)
642 (54)
556 (63)
5.1 (0.8)
66.8 (84.9)
3.0 (0.5)
5.6 (1.1)
551 (66)
724 (16)
572 (69)
Recall Means (Standard Deviation) for the 3 Groups in Each of the Critical Conditionsa
Group
Total recall
Nonemotional
Emotional
Separate word lists recall
Standard
Neutral
Positive
Negative
HADS scores
Anxiety
Depression
Controls
MCI
AD
104 (17.3)
25.0 (5.0)
25.4 (6.1)
72.2 (15.4)
16.8 (3.7)
18.8 (4.7)
49.5 (22.9)
11.1 (5.9)
12.4 (5.4)
26.3
25.0
26.5
26.3
17.8
16.8
18.5
19.2
12.9
11.1
13.1
12.4
(4.3)
(5.0)
(4.8)
(6.1)
3.2 (2.5)
2.9 (2.3)
(3.7)
(3.7)
(4.8)
(5.5)
3.7 (3.7)
3.8 (3.1)
(7.2)
(5.9)
(6.2)
(5.7)
2.8 (2.7)
2.5 (1.8)
Abbrevations: MCI, mild cognitive impairment; AD, Alzheimer’s disease
a
Hospital Anxiety and Depression Scale (HADS) scores for the 3 groups are also provided.
of each trial in any order that they remembered them.
The order of the lists was counterbalanced across participants in each group in an attempt to control for
possible order effects. Total number of correct
responses per trial and overall for the 4 word lists were
recorded as were the total number of repeats and
intrusions for each of the lists per subject.
Results
Table 2 shows the mean total recall scores for the 3
groups over the 4 word lists plus the average ‘‘emotional score’’ (average across the positive and negative lists) and ‘‘non-emotional score’’ (total neutral
list score). Also depicted in Table 2 are the recall
means for each of the word lists and the mean HADS
anxiety and depression scores per group.
Compared to the norms available for the standard 8-word test (derived from a healthy elderly population), controls scored at the 60th percentile, while
the MCI group scored at the 20th percentile and the
AD group scored below the 10th percentile. No
norms (yet) exist for the new word lists.
An analysis of variance (ANOVA) was carried out
for the total recall scores for the 3 groups collapsed
over word lists and this revealed a main group effect
[F(2,94) ¼ 67.0, P < .001]. Post hoc tests revealed that
the controls recalled significantly more words over all
word lists than both the MCI and the AD group and
the MCI group recalled significantly more words than
the AD group (P < .001 for all comparisons).
A second ANOVA was conducted to investigate
whether there was an EMA. The average of the positive and negative lists was calculated per subject
(positive total þ negative total/2), and these values
were compared to that person’s total recall score on
the neutral list. In this way, we could compare an
‘‘emotional recall score’’ with a ‘‘non-emotional recall
score’’ irrespective of the valence of the words (there
is controversy in the literature as to whether a positive or negative advantage is seen in healthy and/or
demented groups—see Introduction). An EMA was
found [F(1,92) ¼ 6.4, P < .025], with better recall for
emotional words versus neutral words. This was the
case for all 3 groups—there was no group x recall
score interaction.
Emotional Word List Recall in Dementia / Nieuwenhuis-Mark et al 5
A third ANOVA of 3 (groups) by 4 (word lists—
total scores) revealed a main effect of word list
[F(3,276) ¼ 6.5, P < .001] and post hoc tests
revealed that participants performed best on the
standard, positive, and negative word lists in comparison to the neutral list (P < .05 for all comparisons).
No word list x group interaction was found.
A fourth ANOVA of 3 (groups) by 5 (trials) by 4
(word lists) was conducted. There was a main effect
of word lists [F(3,276) ¼ 6.3, P < .001] and post hoc
analyses revealed identical results as depicted in the
third ANOVA. There was also a main effect of trial
[F(4,368) ¼ 191.9, P < .001] and post hoc tests
revealed that learning increased overall from trial 1
to 5. An interaction between trial and group was also
found [F(8,368) ¼ 7.4, P < .001] and this warranted
separate ANOVAs per group. Controls showed
increased learning across all 5 trials [F(4,148) ¼
139.9, P < .001]. The MCI group also showed steady
learning across the 5 trials [F(4,144)¼ 77.3, P <
.001], and there was also a main effect of word list
for this group [F(3,108) ¼ 5.9, P < .003]. This
reflected better recall over all 5 trials for the negative
list than for the neutral list (P < .01).The AD group
also showed evidence of learning [F(4,76) ¼ 27.0,
P < .001] despite the fact that their learning curves
were flatter and more variable than those of the other
2 groups. No other significant effects emerged.
Learning curves were plotted (see Figure 1) to compare the 3 groups’ recall for all 4 word lists.
A further ANOVA was carried out to assess
whether there were any list order effects. No main
effect of list order or interactions of list order x word
list or list order x group emerged suggesting that our
counterbalancing was effective and that list order
had no effect on recall performance. Finally, ANOVAs
were carried out to assess list order effects, and repetitions and intrusions per word list in all 3 groups. Only
the significant findings are reported here. A main
group effect was found for intrusions [F(2,94) ¼ 3.8,
P < .03] with more intrusions made by the AD group
in comparison to the controls (P ¼ .06) and MCI
(P ¼ .04) groups and no difference evident between
controls and MCI. There was also a main list effect for
intrusions [F(3,276) ¼ 8.14, P < .001] with more intrusions made over all groups for the neutral (P ¼ .02) lists
compared to the standard, positive, and negative lists.
Discussion
Several interesting findings emerged from this study.
Controls had, unsurprisingly, better recall overall
than the other 2 groups and the MCI group had better recall overall than the AD group. This result
reflects the fact, especially if we consider the MCI
group to be in the very early stages of AD, that episodic memory declines as AD progresses. We also
found an EMA with better memory for emotional
than nonemotional words. Interestingly, this was the
case for all 3 groups and could not be said to be due to
any differences in anxiety or depression (see Table 2
for HADS scores). Although Fleming et al1 did not
directly measure mood, these authors indicated that
this variable may have an important bearing on how
well participants recall emotional stimuli (depressed
people being more likely to recall negative stimuli).
None of our participants were clinically anxious or
depressed so their better recall of emotional stimuli
cannot be attributed to their mood. Our findings are
partially consistent with the work of Brierly et al34
and Fleming et al1 and suggest that emotional stimuli
may help not only healthy elderly people but also
people with MCI and AD to remember better. We
did not however find any recall differences between
the negative and positive lists for any group and
therefore our results do not support the positivity
effect (see Introduction) found by some researchers
in elderly individuals.17,18
The learning curves suggested that all 3 groups
showed evidence of learning over the 5 trials. For
controls, this was the case over all 4 word lists. For
the MCI group better recall occurred for the negative
list than for the neutral list over the 5 learning trials,
a finding which supports the negative bias found for
Alzheimer patients by Fleming et al.1 These authors’
patient population had a mean MMSE score of 21
making them quite similar to our MCI group. The
AD group in this study also showed evidence of
learning while their curves were flatter and more
variable than the other 2 groups and their recall
appeared to peak between trials 3 and 4 and drop off
again by trial 5 for the 3 new word lists (for the standard word list, they showed a peak at trial 3). This
suggests that even this group can recall words in an
episodic memory test albeit at a lower level than controls or those with MCI. Severely reduced episodic
memory is a hallmark of AD and therefore this
result is not overtly surprising. Our results do suggest
however that all 5 trials may not be necessary to test
episodic memory in a moderately demented AD population, 4 trials may be adequate, especially if we are
simply interested in the best performance these
patients can achieve.
Interestingly, Brand and Jolles35 suggested that
flatter learning curves obtained in a serial list
6 American Journal of Alzheimer’s Disease & Other Dementias1 / Vol. 000, No. 00, Month 2009
Neutral word list
7
7
6
6
5
5
4
Controls
MCI
3
AD
2
Average recall score
Average recall score
Standard word list
1
4
Controls
MCI
3
AD
2
1
0
0
1
2
3
4
5
1
2
Trial number
4
5
Negative word list
7
7
6
6
5
5
Controls
4
MCI
AD
3
2
Average recall score
Average recall score
Positive word list
Controls
4
MCI
AD
3
2
1
1
0
0
1
2
3
4
5
Trial number
Figure 1.
3
Trial number
1
2
3
4
5
Trial number
The learning curves of the 3 groups for each word list.
learning task similar to the one used in this study
could be due to frontal neocortical dysfunction and
this would be reflected by more repetition errors.
Our AD group showed (nonsignificant) signs of more
repetition errors and (significantly) more intrusion
errors compared to the other 2 groups. Although
hippocampal atrophy is generally the first sign of
neuronal damage in AD,6 it is possible that some
patients in our AD group also had frontal lobe
damage. Unfortunately, we do not have magnetic
resonance imagings (MRIs) which could confirm
or dispute this suggestion. Obtaining brain scans
is therefore something to consider for future
research.
Our study also revealed that the standard 8-word
test is not a ‘‘neutral’’ test as many practitioners
believe but rather a positively valenced one (see
Table 1B). It is therefore appropriate to use in the
clinic when the neuropsychologist wants to obtain
the best performance possible from the patient.
Emotional Word List Recall in Dementia / Nieuwenhuis-Mark et al 7
There are several limitations present in our
study. The MMSE is a relatively crude cognitive
screen which cannot tell us very much about the specific cognitive functioning of our participants. We
would recommend more detailed assessment in
future studies, for example, using the Cambridge
Cognitive Examination (CAMCOG).36 This instrument can provide much more information on the
cognitive abilities of the participants and would have
helped us to determine whether the MCI group was
actually suffering from mild AD. Nothing however
can match a clinical diagnosis and we emphasize the
continuing need for such a diagnosis in future
studies.
Another limitation is that we could not adequately assess possible gender effects—there were
more women than men in our population. It is difficult to see how this could be prevented in future
studies because women do tend to live longer than
men and our population was made up of old-elderly
individuals thus perhaps exacerbating the preponderance of women. This might not be such a problem
however because Kensinger et al9 failed to find gender effects in their large demented population. Interestingly, EMAs were not found for the AD patients
(regardless of disease severity) in Kensinger et al’s
study9 while we found EMAs for all 3 groups tested
here. As suggested in the Introduction, encoding
instructions, stimulus characteristics and populations studied may all determine whether EMAs are
found or not.9 Furthermore, we only used a recall
task because these types of tasks tend to produce
EMAs more readily than recognition tasks.25,26 It
would however also be useful to include recognition
tasks in future studies.
Charles et al37 suggested that in normal aging
people would shift from a better memory for negative
information (found in young individuals) to a better
memory for positive information. This study does not
support these findings—we found better memory for
both negative and positive words (versus neutral) in
all groups. These finding have implications for treatment. More successful cognitive rehabilitation strategies could feasibly be designed, for example, by
focusing on positive feedback and using emotionally
toned words and phrases throughout treatment.
Future studies could assess the usefulness of this
idea by manipulating instructions during treatment
and measuring its effectiveness on both short- and
long-term cognitive and behavioral functioning.
In conclusion, although we were successful in
creating emotional word lists which could be used
by practitioners in the clinic as part of a standard
neuropsychological assessment, we recognize that
these lists will need to be validated and norms
obtained before they can be widely used by clinicians. It is often difficult to find suitable emotional
memory tests to use with patient groups because,
as we suggested in the Introduction, lists typically
used in laboratories are often too long and complex
to be used with elderly people and demented
patients. Our lists provide a possible solution to this
dilemma. Also, despite the fact that the average age
of our population (*80 years for all 3 groups) was
older than is found in most of the literature, our participants performed relatively well on the tests. This
gives not only elderly people hope (their memory may
not be completely damaged with advancing age) but
also suggests that memory research can be conducted even in the oldest individuals. Finally, the
present findings suggest that using emotional stimuli
may help improve memory recall in the very old even
if the participants have been diagnosed with AD.
Future research will determine whether this EMA
holds for other kinds of stimuli in these populations
and will assess how they learn and determine
whether everyday memory may also be enhanced via
manipulating the emotional connotations of the tobe-remembered events.
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